How Snakes Work Structure, Function and Behavior of The World's Snakes

How Snakes Work
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How Snakes Work
Structure, Function, and Behavior of
the World’s Snakes
Harvey B. Lillywhite
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Library of Congress Cataloging-in-Publication Data

Lillywhite, Harvey B., 1943–
How snakes work : structure, function, and behavior of the world’s snakes / Harvey B. Lillywhite.
pages cm
ISBN 978-0-19-538037-8 (alk. paper)
1. Snakes. I. Title.
QL666.O6L724 2014
597.96—dc23 2013019018
9 8 7 6 5 4 3 2 1
Printed in the United States of America
on acid-free paper
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This book is dedicated to
Rodolfo Ruibal,
George Bartholomew, and
Kenneth Norris,
who inspired and mentored my passion
for discovery and science.
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CONTENTS
FOREWORD BY RICK SHINE ix CHAPTER 6:

P R E FA C E xi I n t e r n a l Tr a n s p o r t : C i r c u l a t i o n
ACKNOWLEDGMENTS xiii and Respiration 141
CHAPTER 1: CHAPTER 7:
Evolutionary History P e r c e i v i n g t h e S n a k e ’s Wo r l d :
and Classification of the Structure and Function of Sense
Wo r l d ’s S n a k e s 3 Organs 163
CHAPTER 2: CHAPTER 8:
F e e d i n g , D i g e s t i o n , a n d Wa t e r Sound Production 181
Balance 37
CHAPTER 9:
CHAPTER 3: Courtship and Reproduction 191
Locomotion: How Snakes Move 77
GLOSSARY OF TERMS 213
CHAPTER 4: INDEX 227
Te m p e r a t u r e a n d E c t o t h e r m y 103
CHAPTER 5:
Structure and Function of Skin 117
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FOREWORD
We share this beautiful planet with an astonishing array of researchers to have focused on the physiology of snakes—
different kinds of creatures, but few are as remarkable as that is, the ways that these mysterious animals deal with
snakes. Some people worship snakes, some are terrified of basic challenges such as finding, capturing, and digesting
them, and some even keep them as pets. Despite a wide their food, maintaining their water balance, and regulating
public interest in serpents, however, we still know very their body temperature. By embedding his research in
little about the day-to-day lives of most species—including the field biology of his study animals, Harvey has revealed
really basic issues such as how they move around, find food the fascinating complexity and elegance of these much-
or mates, or influence the ecosystems in which they occur. misunderstood creatures.
Dedicated field biologists like Harvey Lillywhite are This book brings together a lifetime of experience, to ex-
shedding new light on these questions. Over his long ca- plain in easy-to-understand terms what snakes do, and
reer, Harvey has pioneered many new insights into snake how and why they do it. I am sure that this attractive vol-
biology—not just in the laboratory, but also out in the field, ume not only will educate people about snakes, but also
where he can explore an animal’s functioning in the condi- will inspire its readers and help them to understand why
tions that it actually encounters. Harvey has worked on a we need to conserve these amazing creatures for future
very wide variety of snake species, in many parts of the generations.
world, and thus brings a truly broad perspective to this en-
gaging book. Importantly, Harvey is one of the very few —Rick Shine, Sydney, January 2013
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PREFACE
Since childhood I have marveled at the sleek form, rich colors, There are comparatively few persons with rigorous training
and absolutely intriguing behaviors of snakes. Having no in physiology who focus their research on snakes, and many of
limbs, these reptiles possess incredible stealth, grace, and the persons with physiological training who do investigate
beauty. They exhibit a wonderful capacity for actions that snakes at one time or another may not have a background of
amuse, startle, or evoke intense curiosity. Snakes live in a rich knowledge that includes extensive firsthand field experience
variety of habitats, from oceans to rocky hillsides, from subter- as well as a passionate appreciation for the natural history of
ranean spaces to open sand deserts. They have evolved colors this group of animals. Thus, I hope that in some manner I
and patterns that awaken the artist, and they have inspired might bring a unique perspective to the subject matter, and to
mythical reverence and respect from many cultures. They per- cover a range of topics in this book that will interest a wide
sistently survive, and yet they are perhaps the most maligned group of readers. Snakes are wonderful animals, and they
group of vertebrates—misunderstood by far too many hu- have become very popular in the pet trade as well as a high-
mans who carry out death sentences at every opportunity. priority attraction at zoological parks. As one begins to under-
For many years I have planned to write a book about stand and appreciate their inner “workings,” snakes become
snakes, one that is intended to interest both the general even more fascinating and evoke even greater emotional as
reader and professionals. There are numerous books that well as intellectual response. My sincerest hope is that readers
have been written about snakes—gems of information as of this book will find enjoyment in discovering new knowl-
well as collections of great photographs. As more and more edge, increased curiosity, and a greater respect for a group of
books appeared with snakes as their subjects, I had cause to animals that reflect an amazing amount of innovation and
ponder how I might make a meaningful contribution in the success in life’s evolutionary game. Insofar as possible, I have
form of another “snake book.” My professional training and attempted to illustrate the many fascinating features of
much of my career as a scientist has been related to physi- snakes—sometimes related to complex or difficult concepts—
ology and the subdiscipline that is generally known as using photographs instead of relying on dense and tedious
“physiological ecology.” My perspectives are quite broad, text. I shall be extremely delighted if many persons enjoy
however, and much of what interests me as a research scien- reading this book as much as I have enjoyed producing it.
tist involves interdisciplinary investigation and integrative To assist readers with understanding the terminology
studies of structure, function, and behavior—focused with that is used throughout the book, I have defined many useful
questions related to the ecology and natural world of the and specialized terms in the glossary. I have avoided the use
animals that fascinate me. The majority of books that have of equations or complicated graphs, but I have provided lists
been written about snakes provide relatively little in-depth of additional readings that provide roads to further—often
coverage of these topics, and none to my knowledge focuses more technical—presentation of the subject matter. Such
on physiology—or structure and function—as the principal readings are listed at the end of each chapter, and they in-
subject of treatment. Thus, I decided to write this book, clude articles by the authors who are mentioned specifically
which specifically targets this “niche” of subject matter. in the text.
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ACKNOWLEDGMENTS
I owe a debt of gratitude to many persons who helped to L. Orlov, Stephen Beaupre, Guido Westhoff, Richard Sajdak,
make this book possible. First, I thank my parents, who Shauna Lillywhite, Steven Lillywhite, Jake Socha, Tracy Lang-
allowed me to keep snakes at home when I was a very young kilde, Mac Stone, Glenn J. Tattersall, William Montgomery,
boy. Reluctant at first, they encouraged me in very impor- and Kanishka Ukuwela.
tant ways as it became evident that my interest in snakes Numerous other persons were invaluable for contrib-
began to open many other doors in the world of science and uting stimulating discussions, reviews of chapters, scien-
learning. I am equally indebted to my wife Jamie, who has tific clarification, and general support of the project. These
assisted me with patience, tolerance, and also encourage- include, but are not limited to, Coleman Sheehy III, Richard
ment for a meaningful project. My son and daughter, Steve Shine, Harold Heatwole, Harry Greene, Phil Nicodemo,
and Shauna, have also been supportive in various impor- David Barker, Roger Seymour, Bruce Jayne, Natalia Anan-
tant ways. jeva, François Brischoux, John C. Murphy, Michael Thomp-
I am grateful to the many persons who have contributed to son, Paul Maderson, Michael Douglas, Bruce Means, Carl
the illustrations, both photographs and drawings. These in- Franklin, Bruce Young, Xavier Bonnet, Matthew Edwards,
clude Dan Dourson, Coleman Sheehy, Elliott Jacobson, Jason Elliott Jacobson, Stephen Secor, Brad Moon, Max Nicker-
Bourque, Rom Whitaker, Laurie Vitt, Gowri Shankar, Richard son, Sergio Gonzalez, Jennifer Van Deven, Joe Pfaller,
Shine, Indraneil Das, John C. Murphy, Sara Murphy, Joseph Li-Wen Chang, and Lauren Dibben. There are numerous
Pfaller, Xavier Bonnet, Irene Arpayoglou, David and Tracy other persons—friends, associates, and students—who
Barker, John Randall, Phil Nicodemo, Blair Hedges, Tony Cro- also deserve thanks, but who are too numerous too men-
cetta, Ray Carson, Akira Mori, Ming-Chung Tu, Erik Frausing, tion without error of missing one or two individuals.
Jesús Rivas, Dhiraj Bhaisare, Parag Dandge, Howie Choset, Finally, I also express my appreciation to the editors and
Thimappa, James Nifong, Lincoln Brower, Alejandro Solórz- other production staff at Oxford University Press who en-
ano, John Roberts, Lauren Dibben, Nicholas Millichamp, couraged me and provided professional assistance in the
Arne Rasmussen, Amanda Ropp, Gavin Delacour, Nikolai production of this book.
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How Snakes Work
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EV OLUT ION ARY HI ST ORY AN D
CL ASSIF IC AT I ON OF T HE
W O R LD’S SN AK E S
It has been truly said that we do not know a species until we know
1
everything about it, its anatomy, its physiology, its development, its habits.
The variations in structure in different families and genera, sometimes even
in species that are placed in the same genus, have no doubt their interpretation
in their varying modes of life, and the correlation of the two is a fascinating
study. It is one that has been much neglected by the field naturalist. Here is
a great field of research waiting for him, for it is upon the living creature that
all our theories concerning the function of structure must finally be tested.
—Malcolm A. Smith, Reptilia and Amphibia, vol. 3, Serpentes (1943), p. 2
What Is a Snake? some distance. Upon closer inspection, of course, the eel is
If we think about snakes we might have seen, and also seen to possess gills, mouth, skin, and other features that
about other animals that look much like snakes in superfi- allow us to recognize it as a fish and not a snake. Worms and
cial resemblance, we begin to ponder what features there limbless amphibians (caecilians) might appear very snake-
are that actually define a snake. If we focus carefully on like if we catch but a glimpse of one of these creatures as it
some of the more obvious features of snakes, we can enu- slips away quickly in moist, low vegetation, or into soil be-
merate some important and potentially diagnostic charac- neath a log or rock that we might turn while looking for
ters. A diagnostic character is an attribute that is unique to a these animals. If one of these animals is in our hand, how-
particular chosen taxon or group of related animals—in our ever, we note the creature—which might even be a slender
case the snakes. Snakes are elongate in body form, they and nearly legless salamander—has no scales, and its tongue
have no legs or arms, they are covered with scales and do is not forked. Similarly, a worm has neither scales nor a de-
not bear fur or feathers (fig. 1.1). All snakes possess a forked fined head with jaws, nor a vertebral column internally. So,
tongue, and they do not have external ear openings of any what are the characters that determine with certainty that
sort (fig. 1.2). Internally, it is important to notice that any we have a snake and not one of these other animals?
snake we might examine has a bony and segmented verte- If we explore further, we find there are other characters
bral column bearing ribs (fig. 1.3). All of these characteris- that are peculiar to snakes when compared with other verte-
tics, however, are not diagnostic because they can be found brates. The eyes of snakes appear always “open.” This is be-
in some other groups of animals as well. cause snakes have no eyelids, and the cornea is covered with
Let us think about some other animals that we know ap- a clear extension of the skin called a spectacle (also brille or
pear superficially snakelike but are not what taxonomists or eyecap) (fig. 1.5; also compare with fig. 1.2 and figs. 7.3, 7.4).
systematists call a snake. These might include eels, worms, The spectacle is fixed in place, transparent, and serves a pro-
legless lizards, and some elongate amphibians that are also tective function as do eyelids. This feature distinguishes
without limbs. Many persons, including trained biologists, snakes from many lizards, but some aquatic amphibians,
might mistake some of these animals for a snake in certain cave salamanders, and some lizards also exhibit partial fu-
circumstances (fig. 1.4). Some species of eels, for example, sion of the skin with the eye to form a spectacle or similar
resemble sea snakes in both size and color, and the distinc- structure. Thus, by itself, this feature is not explicitly diag-
tions are not clear when the animal is seen swimming at nostic of snakes, although it is helpful in most cases.
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Figure 1.2. Comparison of the external characters on the head of a
snake and a lizard. The upper photo is of a Herald Snake
(Crotaphopeltis hoamboeia), which is an African colubrid. The lower
photo features a legless Eastern Glass Lizard (Ophisaurus ventralis).
Note that unlike the snake, the glass lizard has eyelids (white arrows)
and an external ear opening (black arrow), whereas the only external
opening on the head of the snake is the nostril that is visible near the
snout. Photographs by the author.
Figure 1.1. Photograph of a reproduced antique print from the late
19th century (1890–1899) featuring cobras and a rat snake eating a
rodent. Original sources include Warne and Co. Ltd. (1895) and “Royal
Natural History” by Richard Lydekker (1896).
ecdysis (skin shedding), however, is one of the earliest phe-
nomenological observations about snakes and is another dis-
tinct and ubiquitous characteristic of these reptiles (fig. 1.6).
Many snakes also possess a lightened and highly movable Some amphibians might also slough the epidermis all at
skull with jaws that are modified to engulf and swallow large once, but the shed skin does not consist of scales like that of
prey items, although some groups of snakes such as blind snakes. Also, in snakes there is a vertical alternation of syn-
snakes are exceptions. Many snakes also are venomous; but thesized keratin proteins known as α and β during the re-
an even larger number of species are relatively harmless. newal of epidermis in shedding cycles (see chapter 5). Only in
Moreover, the Gila Monster lizard also can envenomate snakes and in other lepidosaurs is this vertical alternation of
prey, and the saliva of varanid lizards is toxic. Thus, we need keratins expressed throughout life over the entire body.
to look at still more characters. The more we examine features of snakes, the more we
Snakes are unlike other reptiles in that the skin un- appreciate that a number of characteristics are shared with
dergoes synchronous shedding cycles in which the entire other vertebrates, whereas some characters are unique at-
outer epidermis is sloughed from the body all at one time. tributes of snakes. The shared attributes suggest relation-
The underlying cycle of epidermal renewal occurs also in ships during evolutionary history, whereas the unique
other lepidosaurs—snakes, lizards, amphisbaenians, and attributes evolved exclusively in the group in question and
tuatara—but the old generation of snake epidermis is typi- are said to be derived. All of these features have been useful in
cally shed as one sheet and at one time, instead of in pieces. classifying snakes among living organisms in a manner that
Exceptions sometime occur in dehydrated, stressed, or older reflects their evolutionary history, and such a classification is
and larger snakes, which may shed patches of skin (see also reflected in a branching structure called a phylogenetic tree.
discussion of blind snakes below). Normal whole-body Increasingly, molecular data related to genetic structure and
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a more complete record. Furthermore, many specimens are
either poorly preserved or incomplete, and there are few re-
searchers who study the material. When characteristics of
snakes are considered—including fossil and living forms—
human judgments and personalities sometime lead to dis-
agreement when it comes to forming hard conclusions. With
respect to living species, there are more characters to be con-
sidered than what is present in fossilized material, including
internal organs, coloration, DNA, proteins, and other prop-
erties of tissues. But again, disagreements can emerge when
different people examine different characters and attempt to
construct an evolutionary tree. Indeed, the classification of
living snakes has been fraught with disagreement and con-
troversy. What follows is an assessment of our current state
of knowledge concerning these subjects.
Fossils and Origins

Snakes are unquestionably tetrapods, which are four-limbed
vertebrates including amphibians, reptiles (including
birds), and mammals. Thus, snakes represent a specialized
branch of vertebrates that descended from limbed ances-
tors. Representatives of some snake families possess ves-
tiges of a pelvic girdle or posterior limbs, although in living
Figure 1.3. The upper photo features a fully articulated skeleton of snakes the pelvic girdle has lost direct contact with the ver-
a water snake (Nerodia spp.), photographed by Phil Nicodemo. The tebral column or is absent altogether. The vestigial elements
lower photo shows a segment of the vertebral column of a Florida
that are present in living snakes are greatly reduced bones
Cottonmouth (Agkistrodon piscivorus conanti). Each pair of ribs
articulate with processes on the vertebrae. See also fig. 3.2 for further
representing the femur and/or pelvis. In male specimens
details. Skeleton courtesy of the Florida Museum of Natural History, of boas and pythons these are associated with external pro-
photographed by the author. trusions of keratinized tissue called spurs (see chapter 9,
fig. 9.21). There is no trace of forelimbs or an anterior limb
girdle in either living or fossil snakes.
biochemical properties are used, sometimes in combination Most paleontologists believe that reptiles shared a
with the observable structures (or phenotype), to resolve common ancestor with a prominent group of extinct am-
details of the phylogeny. This subject will be elaborated in phibians known as labyrinthodonts, named for a distinc-
the next section of this chapter. tive structure of teeth having complexly infolded enamel.
Back to the question: What is a snake? We can describe a These ancient tetrapods comprised a diverse group of ani-
snake using a list of characters that confer specificity when mals that lived during the Paleozoic era more than 300 mil-
considered collectively. We may call this an informal descrip- lion years ago (fig. 1.7). It is not clear from which group of
tion that has utility when one is inspecting a newly found an- labyrinthodont amphibians the reptiles evolved, and there
imal and wants to decide whether or not it is a snake. The other might well have been multiple origins from ancient am-
way in which the question can be answered is by what I call a phibians that appeared to be developing reptilian charac-
formal definition. In order to understand the more formal teristics. The oldest known fossils that are definitely
approach, we need first to consider the evolutionary history recognized as reptiles are from small animals resembling
of snakes and their relationships with other vertebrates. lizards and classified as cotylosaurs, also called the “stem
reptiles” (fig. 1.8). These ancient reptiles are believed to be
ancestral to all the taxa of reptiles that are living on the
Evolutionary History of Snakes earth today. The cotylosaurs appeared first during the late
There is great difficulty in determining the evolutionary Carboniferous or early Permian period over 275 million
history of snakes, including the origins and classification of years ago. Subsequently these early reptiles diversified
currently living species. There are many reasons why this is and gave rise to lineages that produced turtles, dinosaurs,
so. The fossil record of snakes is quite scattered and scanty, mammals, crocodilians, birds, tuatara, and the modern liz-
and piecing together the origins of snakes is difficult without ards and snakes (Squamata).
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Figure 1.4. Some vertebrate animals that people might mistake for a snake. Upper left: An Eastern Glass Lizard (Ophisaurus ventralis) is a
legless anguid lizard common in the eastern United States. Photograph by the author. Upper right: A Florida Worm Lizard (Rhineura floridana),
which is an amphisbaenid squamate and not a true lizard. This is a subterranean species, characterized by having degenerated eyes, a blunt
worm-like tail, and a rigid head that helps it burrow its way through soil. Photograph by the author. Lower left: Burton’s Snake Lizard (Lialis
burtonis) is a legless gekkonid lizard that lives in Australia. Photograph by the author. Lower right: A species of eel (Myrichthys colubrinus)
that very closely resembles a banded sea snake that also lives in its habitat. This specimen was photographed in Bali, Indonesia, by John E.
Randall, Bishop Museum, Hawaii.
The oldest fossil snakes come from the middle of the Cre- Because Najash rionegrina was found in a terrestrial de-
taceous period roughly 70 to 95 million years ago. Fossil posit, it supports the hypothesis that snakes evolved on
snakes are by no means abundant, and the historical record land. The idea that snakes evolved from terrestrial ances-
is incomplete, as is the case with many other vertebrates. tors, eventually losing their limbs after they adopted habits
Sometimes the fossil consists of only a few ribs or vertebrae, of burrowing in soil, was popular for most of the 20th cen-
or other bones, and a proper interpretation can be quite tury and enjoys considerable support. The skull of snakes
challenging. For example, one of the earliest fossils thought resembles that of lizards with respect to certain features,
to be a snake later proved to share some characters that also for example a moveable quadrate bone at the rear of the
existed in Cretaceous lizards and is no longer regarded as a jaw and the absence of a quadratojugal bone at the rear of
snake. The oldest unequivocal snakes have a snakelike verte- the skull. Snakes probably evolved during the Jurassic—
bral column with evidence of limbs. A fossil snake named perhaps 150 million years ago—however, there are currently
Najash rionegrina, recently discovered in Argentina’s Rio Ne- no fossils dating back that far. During the early Cretaceous
gro province, has a primitive pelvis and legs that were pre- (about 120 million years ago) these early snakes radiated
sumably functional outside the rib cage. It is purported to be into a number of forms, including some that were aquatic
the earliest limbed snake to be found in a terrestrial deposit. and some that were terrestrial. Both terrestrial and aquatic
The skeletal structure of this snake appears to be closer to species of snakes existed in the mid-Cretaceous (about 95
that of a quadrupedal ancestor than is that of previous fos- million years ago), and there is still debate about which type
sils, but the closest ancestor remains unknown. evolved first.
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Some of the earliest fossil snakes are marine forms that
have been unearthed in 95-million-year-old marine deposits
in North Africa, the Middle East, and eastern Europe. One
of these possesses a complete hind limb that extends be-
yond the body wall, but is certainly a snake. Thus, some sci-
entists argue that snakes lost their limbs in the ocean
instead of on land, the immediate ancestors being now-
extinct marine lizards called mosasaurs (fig. 1.8). Fossils
identified in marine environments are at least 8 million
years older than are those from terrestrial deposits. The
question of “Who came first?” may never be resolved with
universal consensus. And, of course, both of these alternative
evolutionary scenarios might have played out in ancient
times roughly in parallel. If this was the case, the marine
forms probably died out and the current lineages of snakes
evolved from the terrestrial ancestors. DNA sequencing and
other data suggest that the living lineages of snakes have a
monophyletic origin, which means they all evolved from a
single common ancestor or ancestral lineage.
Studies of fossil snakes and their comparisons with ana-
tomical features of modern reptiles have led a number of
scientists to suggest that snakes evolved from a family of
lizards during the time when dinosaurs were prominent.
Figure 1.5. The eyes of snakes are covered with a spectacle or brille. Varanid lizards (monitor lizards or goannas) are very sim-
The upper photo features the eye of a Florida Cottonmouth
ilar to snakes in the structure of the skull, sensory systems,
(Agkistrodon piscivorus conanti) photographed by the author. The
facial pit, an infrared thermal imaging receptor, and the nostril are also and also other features. The Earless Monitor (Lanthanotus
easily seen. This snake is largely nocturnal and has a vertically borneensis) of Borneo, Indonesia, has movable eyelids, but
elliptical pupil. The lower photo features the relatively large eye the lower lid bears a clear “window” resembling the snake’s
and round pupil of a Speckled Racer (Drymobius margaritiferus), a eyecap. As its name implies, the Earless Monitor lacks an
diurnally active forager. Note the complete absence of any sort of
external ear, just as in snakes, and also exhibits a number
eyelid or covering at the edges of the pupil. Compare this photograph
with that of the lizard that is featured in fig. 1.2. The racer was
of snakelike features in the architecture of its skull. Based
photographed in Belize by Dan Dourson. on such similarities, some scientists have theorized that
ancient lizards related to monitors adopted a burrowing
mode of life, tunneling through loose dirt or sand as do a
number of lizard species today. In this manner, a number of
features characteristic of snakes evolved, such as reduction
and eventual loss of limbs and external ears, and the devel-
opment of a spectacle to protect the eyes while moving
through earth. The various descendants of these burrowing
forms diversified and radiated into terrestrial habitats af-
ter emerging from a subterranean lifestyle to exploit a va-
riety of terrestrial niches. Once the limbs were lost during
the subterranean existence, they were not regained by
“reversals” in the other environments. Rather, the limbless
creatures we call snakes evolved many specializations and
marvelous means of living without arms or legs.
It is interesting to note that numerous losses and reduc-
tions of limbs have occurred during vertebrate evolution,
Figure 1.6. Shed skin from a Gaboon Adder (Bitis gabonica, inset)
including many species of skinks and other reptiles beside
showing dorsal scales and ventral scutes separated by interscale
tissue. The shed skin is epidermis from the entire body surface, intact
snakes. The loss of limbs and elongation of the trunk of
and inside out as it “peels” from the snake and subsequently dries. snakes is related to changes in the expression of genes called
Photographs by the author. Hox genes. These genes are known to control development
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Figure 1.7. Geologic time scale with nomenclature for major units of time in millions of years before the
present. The figure illustrates the major units of geological time related to definitive events of the Earth’s history.
The animal cartoons to the right of the table indicate approximate times of radiation and dominance, not the
earliest points of origin. Cartoons by Dan Dourson.
by specifying embryonic cell division along the long axis of the The Concept of Phylogeny
body and determine limb development and specific bound- Phylogeny refers to an evolutionary history of species, or a
aries of related morphological changes. Martin Cohn and group of species, and is represented by a branching diagram.
Cheryll Tickle have shown that the patterns of Hox gene ex- Such a diagram is called a dendrogram, cladogram, pheno-
pression along the body axis in developing embryos of py- gram, or tree, depending on the methods used to construct
thons accounts for the absence of forelimbs and the expansion the diagram and the information content it is intended to
of the thoracic axial skeleton. These authors also suggested convey. For our purposes we will call such a diagram simply
that the failure of signaling pathways to activate the develop- a phylogeny or tree. Scientists use many alternative methods,
ment of limbs might be related to changes in the expression of indeed incorporating even entire philosophies, for building
Hox genes during the early evolution of snakes. a phylogenetic tree. The process involves reconstructing
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Figure 1.8. The upper drawing illustrates a cotylosaur,
representing one of the earliest families of reptiles. Cotylosaurs were
small lizard-like reptiles that date from the late Carboniferous through
the Permian (see fig. 1.7), and they have sometimes been called “stem
reptiles” or “root reptiles” in reference to their basal position in
reptilian phylogeny. The lower drawing depicts an extinct marine Figure 1.9. Hypothetical phylogeny of several taxa of snakes,
lizard known as a mosasaur. These reptiles were powerful swimmers illustrating variation in topology and lengths of branches for different
and well adapted to living in the warm, shallow seas that were taxa. The scale of time is relative and arbitrary. Alternate scales (with
prevalent during the late Cretaceous period. Mosasaurs probably more variable branch lengths) could be expressed in terms of genetic
evolved from semiaquatic squamates and have a body shape that is substitutions assuming availability of molecular data. Two examples
similar to that of modern terrestrial monitor lizards (varanids), except of sister taxa are represented by pairs of the letter “s” above the two
for being longer and streamlined for swimming. Mosasaurs are respective branches. Drawing by Coleman Sheehy III and the author.
considered to be close relatives to snakes, judged from analysis of the
jaw and skull anatomy. Drawings by Dan Dourson.
changes, commonly expressed using molecular data as the

number of mutations in a genetic sequence. Hence, species
evolutionary events, inferred from changes in character states evolving at different rates will have unequal branch lengths.
(different forms of the same character) represented by dif- If such empirical data are not available, branch lengths may
ferent taxa or lineages. Various characters are used, usually be represented in terms of relative time, or constructed
depicting phenotypic traits such as anatomical features, or from evolutionary models. The branching order is deter-
molecular data such as properties of proteins or DNA. Phe- mined from phylogenetic methods that estimate or infer
notypic traits are observable features that are expressed ancestral phenotypes from characters studied in living spe-
from the genetic makeup of an organism. Molecular data are cies. The methods are used to optimize character states at
increasingly being used to reconstruct evolutionary histories, internal nodes (branching points) of the tree, which are hy-
and recent technological advances in genetics and genomics pothesized to represent speciation events. Comparison of
have greatly enriched the data base and helped to produce trait values at ancestral and descendant nodes of the tree
many new and sometimes radical changes in phylogenetic allow the history of phenotypic changes to be traced.
trees. This is true for many organisms, not just snakes. Species descend from each other in a hierarchical
A tree-shaped branching diagram conveys potentially fashion—that is, a branching or treelike process of specia-
two kinds of information: the tree topology, or sequential tion. So character evolution is regarded as a process of his-
order in which the taxa branch from one another, and the torical transformation from a primitive to a derived state.
lengths of the individual branches (fig. 1.9). Typically, the Primitive or ancestral traits are characteristics that resemble
length of a branch on a tree is scaled as proportional to trait ancestral or early conditions, whereas derived traits are those
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that have undergone change (phenotypic or molecular) from criterion, reptiles include the traditional divisions into tua-
the ancestral condition in relatively recent time. Thus, char- taras, turtles, crocodilians, snakes, and lizards. In recent
acter evolution is perceived as trait change on a tree. years, however, most taxonomists have begun to agree that
Because species descend from common ancestors in a hier- natural groups, or taxa, should be monophyletic to include
archical fashion, closely related species tend to resemble each all the descendants of a particular ancestral form. By this
other more than they do distantly related species. Traits can convention, “reptiles” (or the class Reptilia) would include
be shared among species through common descent (called ho- all birds because it is clear that birds and crocodilians are
mology) or by independent origin (called convergence or homo- sister taxa (fig. 1.10). Thus, traditional members of the class
plasy). Homologous characters are ones that are inherited “Reptilia” are often now referred to as “non-avian reptiles”
from a shared common ancestor, whereas homoplastic char- to emphasize the close relationship between crocodilians and
acters are convergent because of similar functional pressures birds. For clarity and ease of understanding, however, we
and natural selection. Thus, two species that are unrelated shall consider snakes as part of the traditional class Reptilia
might resemble each other in some character simply because and refer to them simply as reptiles.
of similar selection pressures in similar kinds of environ- As part of the reptiles, snakes comprise a clade or mono-
ments. For example, two independent lineages of sea snakes phyletic lineage within the order Squamata, which also in-
both evolved a paddle-shaped tail that is used as an aid in cludes lizards and amphisbaenians. The latter are essentially
swimming. These structures represent two independent highly derived lizards. Amphisbaenians are elongate and gen-
origins of the same character (see fig. 3.8). Within each group, erally limbless, and they are characterized by heavily ossified
however, paddle-shaped tails are inherited through separate skulls that are modified for subterranean digging (fig. 1.4).
lineages; each can be traced to a common ancestor, and All squamates are characterized by generally prominent and
they are therefore homologous. The concept extends to other obvious scalation, and they share some other characteristics
character states, including color and behavior (see below). as well. The tuataras of New Zealand, which superficially
Many persons will assume that the value of phylogenetic
trees is simply to provide a picture image of how snakes are
related as part of understanding their evolutionary history.
Indeed, this is the intention implicit in this conceptual Amphibians
overview and the more detailed discussion that follows in
the next sections of this chapter. However, the reader
should also appreciate that phylogenetic trees are being Mammals
used in concert with evolutionary approaches using com-
parative data to study the evolution of various characters
ranging from molecular and biochemical features to attrib- Turtles
utes of morphology, physiology, and behavior. Indeed, a
richer understanding of how snakes or other organisms
work is growing from an interdisciplinary approach to evo- Lizards
lutionary questions using tools from both phylogenetics
Amphisbaenians
and comparative anatomy or physiology.
Squamata Snakes
Classification and Phylogeny of the Lepidosauria

World’s Snakes Tuatara
Reptilia
Deciphering the evolutionary relationships among the
world’s snakes has been very challenging for scientists.
Constructing a phylogeny can be time-consuming and ex- Crocodilians
pensive, and is subject to error, reinterpretation, and con-
troversy. Certain groups of snakes, such as the speciose
colubrids (Colubridae) have been especially problematical,
Birds
and there remains disagreement and many questions about
Figure 1.10. Phylogenic tree illustrating a schematic representation
the details of relationships.
of the evolution of vertebrates. The vertical bars at the right-hand side
From a long-standing conventional viewpoint, snakes of figure encompass clades that are identified to the left: Squamata,
are classified in the class Reptilia (reptiles), which includes Lepidosauria, and Reptilia (in reverse hierarchical order). Drawing by
all the ectothermic animals with dry scaly skin. By this Coleman M. Sheehy III and the author.
10 | How Snakes Work
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resemble lizards, belong to a separate and ancient order that have a remnant pelvic girdle, but this is variably lacking in the
is a sister taxon to the Squamata having a separate evolu- Anomalepididae. Some leptotyphlopid species in Africa pos-
tionary history. Collectively, all snakes are classified as a sub- sess external spurs. The skulls are highly modified and quite
order of Squamata, called Ophidia or Serpentes. Hence, when peculiar in some species. Typically, the small, curved mouth is
people speak or write about “ophidians” (or use this term as a set well below the snout, somewhat like that of a shark, and
descriptor), they are referring to snakes. some species have enlarged, shovel-like or sharpened snouts
The following discussion is an attempt to summarize that presumably facilitate digging. The rostral scale is en-
what is currently known about these relationships, with larged and sometimes covers much of the anterior head
emphasis on broad patterns rather than details and hard- (fig. 1.11). The two lower jaws are attached anteriorly, a
ened opinions about alternate classification schemes. Thus, character state that is similar to most other vertebrates but
one may well consider the relationships to be a work in pro- unlike other snakes. Some worm snakes (Leptotyphlopidae)
gress. What is important is for the reader to acquire an ap- possess relatively large teeth on the lower jaws while lacking
preciation for the diversity and marvelous adaptations that teeth on the upper jaws, whereas others (Typhlopidae) have
characterize snakes as a living and successful group of ver- teeth only on the upper jaws or on both upper and lower jaws
tebrates. Some lineages contain only one or a few species, (Anomalepididae). Little is known about the functional
while others are extremely rich and include hundreds of biology of worm snakes, but one recent study describes an
species. There is evidence from the fossil record which indi- unusual manner of feeding (see chapter 2).
cates that some groups were more diverse in the past, so the Blind snakes are nonvenomous and harmless, although
present diversity has been impacted by past extinctions. when aroused they often emit a strong and offensive odor
Let’s now explore the living diversity of snakes. related to secretions from well-developed musk glands lo-
cated in the base of the tail. These secretions might assist
aggregation behaviors in addition to defensive functions.
Scolecophidia: The Blind Snakes Chemical stimuli as well as the sensory capacity for re-
The Scolecophidia, technically an infraorder or superfamily, sponse are probably very important to these animals, which
represents one branch of a primary dichotomy of snakes. have weak or no vision and live in a world where vision is
This is a monophyletic group of snakes consisting of three not very useful.
families: Leptotyphlopidae, known as thread snakes, worm These snakes are typically small, and so they have been
snakes, or blind snakes; Typhlopidae, also called blind snakes; difficult to study. Some species are less than 2 mm wide in
and Anomalepididae, also called blind snakes or dawn blind body girth and weigh less than a single gram. The group in-
snakes. All of the snakes classified within these families—a cludes the world’s smallest snake—Leptotyphlops carlae—
little over 300 species—are considered to be evolved from a discovered by Blair Hedges in June 2006 on the Caribbean
common ancestral form. This conclusion is inferred largely island of Barbados. Fully grown adults of this species stretch
from possession of common characters unlike those of other less than 10 cm and can coil upon a coin the size of a US
snakes, including features of the skull, eyes, and soft anatomy.
The collective vernacular name of blind snakes is derived
from the eyes being reduced or vestigial—usually buried
beneath the head scales—and in some species absent entirely
or reduced to small patches of dark pigment (fig. 1.11).
Collectively, Scolecophidians resemble each other in
having uniformly smooth scales encircling the body with-
out enlargement of the ventral scales as in other snakes.
The skin is smooth and shiny, adheres tightly around a cy-
lindrical body, and sometimes separates into discrete mul-
tiple rings of sloughed epidermis during skin shedding. This
feature is unlike other snakes in which the outer generation
of epidermis is shed generally as one entire piece. Whereas
the skin of snakes is generally without glands, some species
of blind snakes possess numerous small glands in the skin
Figure 1.11. A Brahminy Blind Snake (Rhamphotyphlops braminus,
covering the head.
Leptotyphlopidae), sometimes called Flowerpot Blind Snake,
Blind snakes generally have rounded or blunt heads as well photographed in India by Indraneil Das. The head is shown in the
as blunt tails, the latter often tipped with a harmless spine inset. Note the enlarged rostral scale, rounded snout, smooth scales,
(fig. 1.11). Members of Typhlopidae and Leptotyphlopidae degenerative eyes, and short blunt tail.
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quarter (fig. 1.12). Larger species of blind snakes generally saturating rainfall that can flood their subterranean homes.
range in length up to about 40–41 cm, but several species The Flowerpot Blind Snake (Ramphotyphlops braminus,
measure more than 60 cm, and there are two unusual species fig. 1.11) is so named because it is often transported from
of blind snakes reaching lengths approaching 80 cm. The body location to location in garden soil or plant debris. Although
color of most species is generally brown, pink, or black. Be- scolecophidians are characteristically fossorial, some species
cause of their colors and long, thin appearance, some species live among roots of tree ferns, while others crawl over veg-
of blind snakes are also called worm snakes or thread snakes. etation at night and are occasionally found several meters
Owing to their small size and tendencies to burrow, above ground. Interestingly, blind snakes can sometimes be
blind snakes are difficult to find. They feed on several life found in the nests of large birds, where they are apparently
history stages of social insects. Many species prey on the brought by the parents to feed the chicks, inadvertently or
larvae and pupae of ants or termites, so the probability of not. Blind snakes are found in the Americas, from south-
finding them increases greatly inside ant or termite nests. western United States southward to Uruguay and Argen-
All species burrow, and most spend much of their time in tina, and they also occur in parts of the Caribbean, Europe,
deep, loose soil, only to be seen when found by flipping logs Africa, southwestern Asia, and Australia.
or rocks, or when crawling on the surface of the soil at night Blind snakes reproduce by laying eggs, and the female
and especially after rainfall. They also emerge following Texas Blind Snake (Leptotyphlops dulcis) coils around her eggs
and shivers like some pythons to elevate temperatures during
egg incubation. This is an extraordinary feat considering the
small size of these snakes! Equally fascinating, the Flowerpot
Blind Snake is the only snake that is known to be parthenoge-
netic. This is a unisexual species in which eggs develop with-
out being fertilized by sperm. Probably most blind snakes are
oviparous and reproduce by laying eggs, but Diard’s Blind-
snake (Typhlops diardii) is possibly viviparous (live bearing) in
some parts of Asia. Again, because of their secretive habits,
much more remains to be learned about the reproduction,
behavior, and ecology of this primitive group of snakes.
The systematics and ecology of blind snakes are very
poorly known in comparison with other terrestrial verte-
brates. They are the closest relatives of all other snakes
(Alethinophidia). A recent molecular study of the Lepto-
typhlopidae suggests that living lineages diversified as early
as the mid-Cretaceous (~ 100 Ma), influenced by the breakup
of continents. The diversity of species appears to be much
greater than is currently recognized, and new species are
continually being discovered all over the world.
Alethinophidia: The “Modern Lineages”

This grouping of snakes is the second branch in the basal
dichotomy of the world’s snakes. These are so-called true
snakes or advanced snakes and include all of the modern
lineages except for the Scolecophidia. Within this large group
of snakes there is a primary dichotomy between what some
call Henophidia (formerly Booidea) and Xenophidia, or Cae-
Figure 1.12. The upper photo shows the world’s smallest species nophidia (formerly called Colubroidea). The former group,
of snake, Leptotyphlops carlae, the Barbados Threadsnake. This henophidians, include dwarf pipe snakes, pipe snakes, shield-
diminutive species was discovered in 2006 on the Caribbean island of tail snakes, sunbeam snakes, boas, and pythons. All of these
Barbados. The species is less than 10 cm (4 inches) in length.
are relatively basal lineages within the Alethinophidia. The
Photograph by S. Blair Hedges. The lower photo features a juvenile
Black Threadsnake, Leptopyphlops ater, photographed by the author
remaining more advanced snakes, Caenophidia, include the
in Guanacaste, Costa Rica. The 50 colones coin in this photograph well-known colubrids, elapids, and viperids; the lesser known
measures 2.7 cm in diameter and is 3 mm wider than the US quarter. homalopsids, lamprophiids, pareatids, and xenodermatids;
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plus the acrochordids, which are sister to all the others. near sources of water and can be common at rice paddies
The position of the Acrochordidae is now fairly well accepted, and other places that are disturbed by humans. Prey items
and the sister caenophidians collectively comprise the are constricted and consist of elongated animals such as
Colubroidea in current terminology. We begin with a dis- eels, lizards, and other snakes. Captive snakes also eat small
cussion of the more basal groups. mice and fish. Defensive behaviors include flattening the
body and waving a curled tail to show its colorful underside
while hiding the head beneath part of the body. When
Henophidia: The Basal Lineages touched or attacked, pipe snakes emit a foul-smelling secre-
Several taxa of basal lineages are collectively referred to by tion from their postcloacal musk glands. These snakes are
many herpetologists as “pipe snakes.” So-called dwarf pipe viviparous and give birth to living young.
snakes (family Anomochilidae) were once considered to be The family Uropeltidae contains almost 50 species of
transitional between the blind snakes and the other alethi- small snakes (15–40 cm) called shield-tail snakes, inhab-
nophidians, but this supposition is no longer supported by iting Sri Lanka and southern India. These snakes are
molecular studies (see below). There are three species of highly specialized burrowers that are closely related to
dwarf pipe snakes—also called “stump heads”—known from the pipe snakes, which they are sometimes called. The
Indonesia and all belonging to a single genus, Anomochilus head is conical, more slender than the trunk, and often
(fig. 1.13). We have very little knowledge about the natural bears a distinct keel (fig. 1.15). The tail is blunt and in
history and functional biology of these animals. Historically, many species bears a single large scale that is roughened
these snakes have long been associated with other pipe at the very end of the snake. The tail collects a plug of
snakes, but they appear to be a sister taxon to other alethi- dirt or mud and protects the snake when it is inside a
nophidians and thus have been placed in their own family. tunnel. The anterior body musculature is specialized
The other pipe snakes include a single neotropical species structurally and biochemically for sustained burrowing.
(fig. 1.14) belonging to its own family, Aniliidae, and nine spe- These muscles together with the vertebral column and
cies of Asian pipe snakes belonging to the family Cylindrophi- viscera move relative to the skin and thus allow these
idae (fig. 1.15). Pipe snakes are small to medium-size snakes, snakes to use a portion of the body to anchor within a
ranging in length from roughly 0.5 to 1 m. They are generally tunnel while the head and anterior body move forward.
somewhat stouter than blind snakes, possess smooth scales, The head is then used to enlarge and compact the sides of
rounded heads, and short, blunt tails. The head is no wider the tunnel by moving from side to side, after which it an-
than the neck; the eyes are degenerated and diminutive. Pipe chors while the posterior body is dragged forward to find
snakes are usually dark brown to black and may have colorful a new point of friction anchor. Most species of uropeltids
yellow or reddish bands, which can be pale and difficult to see. are poorly known and unstudied, while others are quite
The neotropical Red Pipe Snake, Anilius scytale, is colorful, common. These interesting snakes are thought to eat
and to some—most importantly potential predators—it re- earthworms, and most or possibly all reproduce by giving
sembles a coral snake (fig. 1.14; see chapter 5). birth to live young.
Pipe snakes burrow in loose soil or vegetation, like blind Two other small families are known as sunbeam snakes
snakes, and are strong diggers. They inhabit lowland forests because of their highly iridescent scales. These are the
Loxocemidae and Xenopeltidae. The Loxocemidae has a
single species, the Mexican Burrowing Python (Loxocemus
bicolor, fig. 1.16), which grows to a length of about 1 m, lives
a secretive and burrowing lifestyle in forests, but emerges
at night (often during heavy rains) to forage on small mam-
mals and other reptiles. Loxocemus ranges along the Pacific
coast of Mexico and Central America. This species is ovipa-
rous and oviposits small clutches of relatively large eggs.
The Xenopeltidae includes two species of Asian sunbeam
snakes in the genus Xenopeltis that grow to a length of just
a little more than 1 m. They live in burrows or beneath logs
or vegetation, and they prey on various small animals in-
cluding other snakes. Like Loxocemus, these snakes lay
eggs. Several studies place the families Loxocemidae and
Figure 1.13. A recently described species of pipe snake, Xenopeltidae as sister taxa, and both of these taxa as sister
Anomochilus monticola, photographed in Borneo by Indraneil Das. to the pythons.
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Figure 1.14. The upper photo features a beautiful Red Pipe Snake (Anilius scytale)—also called a False Coral Snake—photographed in
the Mato Grosso, Brazil. This is the only species currently recognized in the monotypic family Aniliidae. It possesses a pair of cloacal spurs,
presumably representing a vestigial pelvic girdle. The lower photos feature the head of A. scytale, which is somewhat flattened and
shows diminutive eyes. This specimen is from Pará, Brazil. All photographs are courtesy of Laurie J. Vitt.
Boas and Pythons: Big Is Beautiful snake and grows to maximum length of about 10 m (al-
The boas and pythons are snakes that are well known be- though most specimens are no longer than 6 m) (fig. 1.17).
cause of their popularity in movies, storybooks, and the South American anacondas are probably the world’s
current pet trade. They are simultaneously loathed and heaviest snake, if the measure is relative mass. Wild Green
loved for being large, and clearly certain boas and pythons Anacondas (Eunectes murinus) can grow to lengths of about
represent the world’s largest snakes. The Reticulated Py- 5 m and weigh up to 45 kg (fig. 1.18). There are reports of
thon (Broghammerus reticulatus; formerly Python reticula- longer and heavier anacondas, but their validity is ques-
tus) of Southeast Asia is probably the world’s longest living tionable. Since the early 1900s the Wildlife Conservation
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Figure 1.16. A Mexican Burrowing Python (Loxocemus bicolor)
photographed by the author at Palo Verde Field Station, Guanacaste,
Costa Rica. Note the smooth scales, stout body, and enlarged rostral
scale.
Figure 1.15. The upper photo shows the underside of a Red-tailed

Pipe Snake (Cylindrophis rufus) photographed by the author in
Thailand. This is a burrowing snake found throughout many parts of
Southeast Asia. The scales are smooth and shiny. The tail is blunt and
pointed with variable red coloration and is used defensively to deter
predators. The lower photo features a head view of a shield-tailed
snake (Blyth’s Earth Snake, Rhinophis blythii). This is a burrowing
snake, like other species of uropeltids, and it exhibits specializations
for a fossorial life. The head and skull are primitive and inflexible, with Figure 1.17. A recently described subspecies of Reticulated Python
a rigid jaw, pointed snout, and degenerative eyes that lie beneath a (Broghammerus reticulatus jampeanus) from Jampea Island in the
head shield lacking a spectacle. This is a preserved specimen from Sri Flores Sea. This is the first adult wild-caught specimen in captivity,
Lanka photographed by John C. Murphy. measuring five feet in length. Photograph by David Barker.
Society has offered a cash reward, currently about US family, but clearly they represent two to four independent
$50,000, for any snake that is 30 or more feet in length lineages that diverged from ancestral snakes leading to the
(≥ 9.1 m). To date, no one has been able to claim this prize. Caenophidia. The largest living snakes are boas and pythons
The largest fossil snake, Titanoboa cerrejonensis, is related to that inhabit the tropics of South America and Southeast
boas and was discovered recently in Colombia beneath an Asia. However, not all species of boas and pythons are large.
open pit coal mine (fig. 1.19). This snake measured nearly 13 An assemblage of about 21 species of relatively small
m and weighed in excess of one ton (1,135 kg)! It is from a snakes called dwarf boas are contained in the family Tropi-
neotropical rainforest dating 58–60 million years ago. This dophiidae, distributed in Middle America (Central America
snake could have been the largest nonmarine vertebrate including tropical Mexico and northern South America), Ca-
living at a time when the Earth was recovering from the ribbean islands, and Malaysia. These snakes grow to a max-
mass extinction of dinosaurs. imum length of about 1m, but most species are 30–50 cm and
Boas and pythons are classified into three or four sepa- usually moderately slender with a somewhat enlarged head.
rate families depending on one’s view of the classification Another species of boa (Casarea dussumieri) is placed
scheme. These snakes were previously classified as a single in the family Bolyeridae, confined to Round Island near
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Figure 1.18. A Green Anaconda (Eunectes murinus) captured by Ed George and Jesús A. Rivas at El Frio, Apure, Venezuela. Photograph by
Tony Crocetta.
Mauritius in the Indian Ocean and called the Round Island popular and well-known Boa Constrictor (Boa constrictor)
Boa or Split-jawed Boa. This species is unique among tetra- (fig. 1.21) and the anaconda (Eunectes spp.), which is special-
pods in having divided maxillary bones with movable front ized for aquatic life (fig. 1.18). All boas are viviparous and
and rear parts. A second species called Bolyeria multocari- collectively consume a variety of vertebrate prey.
nata is thought to have gone extinct only recently within There are roughly 27 species of pythons in the family
the past 30 years. Round Island Boas are oviparous and eat Boidae. These are sometimes treated as a separate family
primarily skinks and geckos. (Pythonidae) and are distributed through central Africa
There are roughly 28 species of boas and sand boas in the through Southeast Asia, southern China, and the East In-
family Boidae. Some 15 species of sand boas have been sep- dies to Australia and Papua New Guinea. Most pythons
arated from the other boas for at least 50 million years, and have premaxillary teeth directly beneath the snout, and
some scientists place these in a separate family (Erycidae) both boas and pythons have long, curved teeth for snaring
or subfamily (Erycinae). These are semifossorial small to prey that might include large mammals and birds. All py-
medium-sized snakes distributed across central and north- thons are oviparous, and some incubate their eggs by coil-
ern Africa, the Middle East, and parts of Eurasia, and also ing about them and shivering the body muscles to produce
include rubber boas (Charina spp.) and Rosy Boa (Lichanura heat. Pythons are diverse in size, color pattern, and habitat.
trivirgata) of western North America. The Old World sand Some species are arboreal or climb readily, and these are
boas (Eryx spp.) exhibit some marvelous adaptations for generally more slender than are terrestrial species (also true
living in sandy habitats, including dorsally placed eyes and for boas). Snakes of the genus Python evolved as part of an
nostrils and a countersunk lower jaw (fig. 1.20). Other boas Australasian radiation and include stout species such as the
occur largely in neotropical forests, and many of these have Ball Python (P. regius) and very long species such as the
infrared-sensitive pits commonly present on or between Burmese Python (P. molurus), African Rock Python (P. sebae),
upper or lower labial scales. Among these species are the and Reticulated Python (Broghammerus reticulatus; = Python
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Figure 1.19. Vertebra of the world’s largest fossil snake (Titanoboa cerrejonensis, right) shown side by side with the vertebra of a Green
Anaconda (Eunectes murinus, left). The length of Titanoboa was 13 m (42 feet), and the snake was estimated to weigh as much as 1.3 tons—30
times the weight of an anaconda! The scientific name Titanoboa cerrejonensis means “titanic boa from Cerrejon,” which is the region where the
fossil was found. Photograph by Ray Carson, University of Florida Photography. The inset depicts what the snake might have looked like (drawn
by Jason Bourque, Florida Museum of Natural History).
reticulatus of earlier nomenclature), which might exceed 10

m in total length. Some of the Australian species of pythons
also grow to great lengths, with Scrub Pythons (Morelia am-
ethystina) reaching lengths of around 8.5 m. Australian py-
thons of the Australian genus Aspidites comprises a sister
taxon of all other living pythons. The Green Tree Python
(Morelia viridis), common to New Guinea, is highly special-
ized for arboreal life, as is the neotropical Emerald Tree Boa
(Corallus caninus) (fig. 1.22).
Caenophidia: Advanced Snakes

The Caenophidia is a monophyletic group of snakes, including
what are generally regarded as the more advanced lineages of
Figure 1.20. A Kenya Sand Boa (Eryx colubrinus) displays some snakes (Colubroidea) and a sister group (Acrochordoidea) of
prominent characteristics of semifossorial boas. These include a
odd snakes, the family Acrochordidae. The Colubroidea also is
muscular body, dorsally placed and upward-looking eyes, a prominent
rostral scale with countersunk lower jaw beneath, and a short, blunt or
a monophyletic group and contains the families Colubridae,
spine-like tail. This is a captive specimen owned by Phil Nicodemo Elapidae, Homalopsidae, Lamprophiidae, Pareatidae, Viperi-
and photographed by the author. dae, and Xenodermatidae. The colubrids contain the most
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Figure 1.21. In the bush and in the hand. The upper photo Figure 1.22. Evolutionary convergence in the trees. The upper
captures a wild Boa Constrictor (Boa constrictor) resting on a tree photograph shows a New World Emerald Tree Boa (Corallus
branch against a steep rock face in Río de Janeiro, Brazil (photograph caninus), and the lower photograph features an Old World Green
by Steven Lillywhite). The lower photo shows William Garcia Tree Python (Morelia viridis). Both snakes are highly arboreal and
holding a Boa Constrictor, soon after its capture in Belize (photograph exhibit remarkable convergence in body form, behavior, and color.
by Dan Dourson). The inset at the top shows a juvenile Emerald Tree Boa, which often
differs in color from the adult. The juveniles are typically yellow to
orange. Both photographs are by Laurie J. Vitt.
species of any family of snakes. Caenophidia is characterized
by several osteological and anatomical characters, and the
close relationships among the inclusive groups are now marine (fig. 1.23). This snake inhabits mostly mangroves
strongly supported by molecular data. and shallow, coastal waters, but there are populations
that also occur in freshwater streams, ponds, and lakes.
All three species are entirely aquatic and rarely leave water
File Snakes: The Bizarre and the Ugly except when they occasionally become stranded on tidal
File snakes are among the more unusual snakes by almost mud flats.
any measure. They are indeed bizarre and fascinate almost All of the file snakes possess small tuberculate scales
all persons who might have the good fortune to see one. terminating outwardly in small spines, creating a rough
Three species belong to a single genus and collectively body surface that gave rise to the popular name (see chap-
comprise the family Acrochordidae. The two larger spe- ter 5). The small, granular scales encircle the body, and
cies, Acrochordus javanicus and A. arafurae, are also called there is very little enlargement of the mid-ventral scales.
elephant trunk snakes, which inhabit freshwater streams The tail is only slightly compressed, but the ventral skin
or estuaries in tropical Asia and northern Australia, re- protrudes to form a small ridge, and the body is flattened
spectively (fig. 1.23). The third species of this family, A. laterally when swimming. File snakes are capable swim-
granulatus, is smaller than the other two and is largely mers, but they mostly crawl along the muddy bottoms of
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Mole Vipers: Packing a Dangerous,
Unusual Bite
About 60 species of snakes inhabiting sub-Saharan Africa
and Arabian Peninsula are called mole vipers because of
their burrowing habits. They do not look like typical vipers,
but most possess a venom apparatus. Mole vipers were
formerly classified as a family Atractaspididae, but the
member species are now considered to be two colubroid
subfamilies within the family Lamprophiidae. The sub-
family Atractaspidinae contains about 23 species of snakes,
most in the genus Atractaspis and known as stiletto snakes.
The Aparallactinae is a sister subfamily containing about 50
species of small (less than 1 m), nocturnal, and usually se-
cretive or burrowing snakes that are distributed through-
out sub-Saharan Africa and the Middle East. Most of these
snakes eat elongate vertebrates such as snakes, skinks, and
caecilians, but species of Aparallactus eat centipedes almost
exclusively. Some of these species bear resemblance to sti-
letto snakes (Atractaspis). The composition of these two sis-
ter taxa includes several lineages of snakes previously
classified in the other colubroid families—Colubridae,
Elapidae, and Viperidae. However, these are now shown to
bear closer relationships among each other, warranting a
separate classification, although the phylogeny of this group
remains somewhat unclear. In the following discussion, we
will consider both subfamilies together.
Mole vipers are small to medium-size snakes (up to 1 m),
Figure 1.23. File snakes (Acrochordidae). The upper photo
usually black or brown, but some species have stripes or
illustrates the smaller marine species, Acrochordus granulatus, bright bands of color. The head has a compact skull and small
photographed by the author in the Philippines. The inset illustrates eyes, and it joins a cylindrical body with a short, pointed tail.
the bead-like scales and the dorsally positioned eyes and nostrils. The The scales are smooth or keeled, and those on the head are
lower photo features aboriginal women hunting the Australian relatively enlarged (fig. 1.24). Most species are oviparous,
species, A. arafurae, which they collect for food. The lower
but one species is a live bearer (Aparallactus jacksoni) and
photograph is by Richard Shine.
the reproductive habits of several species are presently not
known.
Most species of mole vipers have grooved rear fangs that
streams, ponds, or mangroves. They are secretive and hide are preceded by smaller solid teeth on the more anterior
among roots of aquatic vegetation or in holes or burrows parts of the maxillary bone, resembling some colubrid spe-
formed by other aquatic animals. The skin is loose and cies of snakes. Another species (Aparallactus modestus) lacks
very flaccid, and the body of these snakes tends to collapse grooved teeth and is possibly nonvenomous. Yet other spe-
downward against a surface when they are taken out of cies have fixed front fangs resembling those of cobras and
water. They crawl slowly with seeming effort when outside other elapid snakes. The stiletto snakes (Atractaspis spp.)
of water, and the skin collapses in various directions with possess movable front fangs resembling those of vipers, but
the body as the animal moves. The eyes are small and bead- these fangs are employed differently during prey capture. A
like, while the nostrils are upturned with an internal valve distinctive feature of these snakes is a reduced maxilla that
that is an aquatic specialization (fig. 1.23). File snakes feed bears an enormous hollow or grooved fang (fig. 1.24). These
on fish and sometimes crustaceans, and they are capable are not true vipers, but like them, the maxilla has a complex
of rapidly capturing prey by ensnaring it within a body articulation and can move to erect the fang. Because of the
coil. The snake does not constrict the prey, but the gran- nature of the jaw movement and the large size of the fangs,
ular scales assist in holding the prey until the head locates the “erected” fangs protrude just a little from the jaw mar-
the item and quickly swallows it. All file snakes are vivipa- gin and are directed posteriorly. Striking and envenomating
rous and reach high population densities in local waters. prey are accomplished by a lateral and posterior stabbing
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diverse habitats from forests to sandy semideserts. All of
these snakes burrow and are generally secluded in soil or
hiding beneath objects during the day. As with other bur-
rowing snakes, movements above ground often occur at
night, especially following rainstorms.
Other Lamprophiid African Snakes

The Lamprophiidae, of which the mole vipers are a part, also
contains many other species representing a late Eocene radi-
ation of nocturnal snakes endemic to the African continent.
These include a widespread genus Lamprophis, many mem-
bers of which are known as house snakes, water snakes
(Lycodonomorphus), racer-like sand snakes, Psammophis spp.,
and other lesser known taxa. Aside from the mole vipers
and stiletto snakes (Atractaspidinae and Aparallactinae),
the family incorporates many of the more characteristic
and widespread nonvenomous snake species of Africa. Al-
Figure 1.24. Head views of a Small-scaled Burrowing Asp together, there are more than 290 species of snakes repre-
(Atractaspis microlepidota), one of the “mole vipers” present in the sented within this family.
middle part of Africa. The upper photo illustrates the flattened head
with a blunt snout, adaptations for burrowing in soil. This species grows
to lengths between 45 and 75 cm. The lower photo shows the fangs of
this snake, which are relatively long and hollow—resembling fangs of
Vipers and Pit Vipers
viperid snakes but uniquely different. The fangs are situated such that Vipers and pit vipers (Viperinae and Crotalinae, respec-
the snake can approach its prey (say a rodent) inside a burrow and tively) are among the more spectacular, interesting, misun-
impale a single fang deep into the animal without completely opening derstood, and maligned snakes. These are all venomous
its mouth. Little is known about this behavior, but the snake can use with prominent fangs and defensive behaviors that feature
just one fang at a time. Photographs by John C. Murphy.
striking toward a threatening human or animal, as featured
popularly on movie and television screens. These are reac-
tive behaviors, however, and venomous snakes like all the
motion of the head, which is the reason for the name sti- others do not harbor aggressive tendencies toward humans.
letto snake. The ability to bear the fangs without greatly Many people believe they are aggressive, but their impres-
opening the mouth is no doubt an advantage to these sions that lead to such stories are misguided exaggerations,
snakes when they forage within subterranean tunnels where possibly with a few exceptions. Snakes are perceived as
they feed on small mammals (mostly rodents and shrews), aggressive and “on the attack” only after they have been
nestling birds, and other reptiles. attacked or treated with aggression first. The toxins of ven-
The diversity of venoms and venom delivery systems omous snakes evolved primarily in relation to prey capture,
in this group probably reflects adaptations to diverse diet and defensive functions are usually secondary with few
specializations. Many eat elongate reptiles or other small possible exceptions (e.g., spitting cobras; see chapter 2).
vertebrates, some eat earthworms, and some like to eat Collectively, vipers and pit vipers are members of the
centipedes. Most species of mole vipers present little family Viperidae, which contains some 230 species. The typ-
danger and are too small to envenomate a person effec- ical vipers or adders of the Old World represent one major
tively. However, the venom glands of Atractaspis spp. are lineage of viperid snakes, and these are placed in the
distinctive from elapids and viperids, containing unusual subfamily Viperinae. Member species of the family exhibit
toxins that subdue prey and can be dangerous to humans. “typical” viper-like appearance with relatively short and bulky
These snakes are well known and feared in parts of rural bodies, distinct and slightly triangular heads—often with
Africa where inquisitive children, snake catchers, and enlarged cheeks to accommodate the venom glands—heavily
others are often bitten because the snakes cannot be keeled scales with small scale size adorning the head, and
picked up safely using one’s hands. The stiletto snakes re- sometimes spectacular defensive behaviors. Most species feed
semble other harmless species and often respond defen- on mammalian or avian (endothermic) prey and often swallow
sively by becoming immobile but suddenly striking with relatively large items potentially harmful to the snake. Other
a slashing, backward movement. These snakes occupy species, however, consume a variety of prey including insects
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(e.g., Orsini’s Viper, Vipera ursinii), other reptiles, and carrion round pupils, and dietary specialization for eating anurans
(especially Cottonmouths, Agkistrodon piscivorus). Most vi- (frogs or toads). Some have an upturned snout (fig. 1.26),
pers, including viperine species, give birth to live young ex- perhaps of some value for digging loose earth or debris in
cept members of the genus Causus, which lay eggs. search for toads, and two species have very elongate venom
Vipers belonging to the genus Vipera, also called adders, glands extending into the trunk beneath the skin. Another
comprise a diverse group of smaller species ranging across a group of African vipers includes arboreal species known as
variety of habitats and are, at northerly latitudes, active in bush vipers (genus Atheris). The more arboreal forms largely
cool weather with rather low body temperatures (fig. 1.25). occupy the equatorial forests of central Africa, while others
There are about 20 species of Eurasian viperines that belong range further south (fig. 1.27).
to the genus Vipera, and these include the only vipers that Thirteen species of African vipers belonging to the genus
are familiar to many central and northern Europeans. Vi- Bitis, and many of these have exceptionally massive, stout
pera berus is one of only two species of snakes to range into bodies and are truly spectacular (fig. 1.28). Some of the
the Arctic Circle (the other is Thamnophis sirtalis). better known species include the Gaboon Adder (Bitis
Other groups or related lineages of vipers are distinctive gabonica), the Rhinoceros Adder (B. nasicornis), and the Puff
in various interesting ways. Six species of African vipers be- Adder (B. arietans). These snakes move slowly but can strike
longing to the genus Causus, commonly called night adders,
are distinctive in having smooth scales, large head plates,
Figure 1.26. Spotted Night Adder (Causus maculatus),

photographed in the Ivory Coast by Xavier Bonnet.
Figure 1.25. Two species of European viper. The upper photo

features a common European Adder or Viper (Vipera berus)
photographed by the author on an island off the coast of Sweden. This Figure 1.27. A female African Bush Viper (Atheris squamigera), also
scene illustrates the camouflage value of the color pattern when seen called Rough-scaled Bush Viper, found in western and central Africa,
against the rocks in the snake’s habitat. The lower photo shows a usually in low bushes. The coloration is variable, and females are
Nose-horned Viper (Vipera ammodytes) photographed by Xavier usually larger than males. This is a captive specimen photographed
Bonnet in its native habitat in Golem Grad, Macedonia. by Elliott Jacobson.
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membrane that is sensitive to heat and infrared radiation.
These pits function to detect warm prey and objects in the
environment (see chapter 7).
Rattlesnakes are familiar pit vipers, represented by some
30 species of Crotalus and three species of Sistrurus collec-
tively distributed from North to South America but with
greatest diversity in the southern United States and Mexico
(fig. 1.29). The tip of the tail bears a characteristic appendage
(the “rattle”) consisting of interlocking segments of rigid,
dead tissue (keratin) derived from successive shedding of
the outer skin. Individual segments are added to the rattle at
its base during skin shedding (chapter 5). When a rattle-
snake is disturbed or acts defensively, the tail is shaken rap-
idly and produces a loud sound (scaled to body size of the
species) that resembles the sound of escaping steam. Spe-
cialized muscles in the tail of a rattlesnake vibrate the inter-
locking rattle segments which move against each other to
produce the rattling sound. The rattle is characteristic of all
species except for its secondary loss in two insular species,
Crotalus catalinensis (Santa Catalina Island Rattlesnake) and
C. ruber lorenzoensis (San Lorenzo Island Rattlesnake). Some
rattlesnakes are very small (e.g., pygmy rattlesnakes, Sistru-
rus spp.) while the larger species (e.g., diamondback rattle-
snakes, C. adamanteus and C. atrox) may exceed 2 m in length.
Old World pit vipers contain about 50 species including
the Japanese Mamushi (Gloydius blomhoffi) and Habu (Pro-
tobothrops flavoviridis) (fig. 1.30), Malayan Pit Viper (Callose-
Figure 1.28. Two large and very heavy-bodied viperid snakes native
lasma rhodostoma), three species of Sri Lankan hump-nosed
to west-central Africa south of the Sahara, especially forested areas. pit vipers (Hypnale spp.), and the beautiful Chinese Moc-
The upper photo features a Gaboon Adder, Bitis gabonica—the casin (Deinagkistrodon acutus) (see chapter 7). There are 31
world’s heaviest viperid snake. This species also has the longest fangs species of Trimeresurus confined to Asia and numerous is-
and the highest yield of venom of any venomous species. The lower lands in the western Pacific, and some of these are arboreal
photo features a Rhinoceros Viper, Bitis nasicornis, which is stout
(figs. 1.31, 5.6). New World pit vipers other than rattlesnakes
with several prominent keratinized horns on its snout. Both species
are largely ambush foragers and are very nicely camouflaged against include snakes of the genus Agkistrodon (Copperheads and
backgrounds of dappled light and leaf litter. These are captive Cottonmouths, fig. 1.32) and numerous species of several
specimens photographed by the author. genera distributed in Middle America and South America.
The latter include more than 30 species of terrestrial lance-
heads (Bothrops spp.), the feared bushmaster (Lachesis spp.)
extremely fast and with much force. They possess unusu- (fig. 1.33), seven species of palm vipers (Bothriechis spp.) (fig.
ally long fangs—up to 4 cm in B. gabonica—and feed on 1.34), seven species of forest pit vipers (Bothriopsis spp.),
generally large endothermic prey relative to their body size and nine species of thick-bodied hog-nosed pit vipers
(see chapter 2). The color patterns are beautiful and provide (Porthidium spp.) (fig. 1.35). Three species of jumping pit
effective camouflage. When disturbed or threatened, these vipers (Atropoides spp.; fig. 1.36) are extremely stout-bodied,
snakes may emit a sharp, loud, and frightening hiss, which approaching the relative girth of the African Bitis.
is sometimes repeated at regular or irregular intervals. The Functional attributes of viperids will be discussed else-
Puff Adder derives its name from this behavior. where in this book, but there is one more viperid species
Snakes widely known as pit vipers belong to the sub- that merits mention before leaving a general introduction to
family Crotalinae, which includes a diversity of species this group of snakes. Fea’s Viper (Azemiops feae) is an inter-
distributed in eastern Asia and the Western Hemisphere. esting species native to the mountainous regions of South-
The name is derived from the presence of paired facial pits, east Asia. It has a decided non-viper-like appearance with
each located between the nostril and eye. The inner recess colorful bands, smooth scales, relatively large head plates,
of the pit bears a thin, vascular, and densely innervated and a somewhat rounded head (fig. 1.37). This species
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Figure 1.29. Some North American rattlesnakes. Upper left: Timber Rattlesnake (Crotalus horridus) at Roan Mountain, Virginia. Upper
right: Black-tailed Rattlesnake (Crotalus molossus). Middle left: An unusually light specimen of Rock Rattlesnake (Crotalus lepidus). Middle
right: A Hopi Rattlesnake, subspecies of the Prairie Rattlesnake (Crotalus viridis nuntius). Lower left: A juvenile Eastern Diamondback
Rattlesnake (Crotalus adamanteus). Lower right: Aruba Island Rattlesnake (Crotalus durissus unicolor). The Timber Rattlesnake and Eastern
Diamondback Rattlesnake were photographed by Dan Dourson. All other photographs were taken by the author.
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Figure 1.31. A female Chinese Green Tree Viper (Trimeresurus
stejnegeri) in Taiwan. This species is highly arboreal and has a more
slender body form than is typical of ground-dwelling viperid species.
The green color also is cryptic, for the snake occurs typically in green
tropical vegetation. Photograph by Ming-Chung Tu.
Figure 1.30. The often feared Habu (Protobothrops flavoviridis) is a

pit viper found in Japan and the Ryukyu Islands (upper photo). It is
the largest member of its genus and grows to a length of nearly 230
cm (7.5 ft). The body is relatively slender, and the head is quite long.
This species has a toxic venom and inflicts numerous snake bites on
humans living on certain islands. Many Habus are collected and used
to make strong liquor called awamori, which is alleged to have
medicinal properties. Photograph by Akira Mori. The lower photo
features a Jerdon’s Pit Viper (Protobothrops jerdoni), also called
Red-spotted Pit Viper. This is a captive-bred snake from individuals
originating in Vietnam. Photograph by the author.
appears to be closely related to pit vipers, but it was once

considered to be the most “primitive” (basal) living viper.
Recent molecular data place this snake in a separate sub-
family, Azemiopinae, which is sister to the Crotalinae.
Elapids: Cobras, Coral Snakes, Mambas,

and Sea Snakes
The family Elapidae includes familiar terrestrial species of
snakes such as cobras, mambas, coral snakes, kraits, and ex-
Figure 1.32. Upper photo: An adult Florida Cottonmouth
tensive radiations of Australian-Papuan snakes and marine
(Agkistrodon piscivorus conanti) rests within vegetation while
species we call sea snakes. The elapids are characterized by photographed by the author on an island near the Gulf coast of Florida.
fixed, hollow fangs located in the front of the mouth, and The lower photo features an adult Northern Copperhead (Agkistrodon
these are relatively short in the majority of species (chapter 2). contortrix mokasen) photographed by Dan Dourson in Kentucky.
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Figure 1.33. The South American Bushmaster (Lachesis muta) is
the longest pit viper in the Western Hemisphere. The longest recorded
Figure 1.35. An adult Hognosed Pit Viper (Porthidium nasutum) in
specimen measured a little over 3.5 m (about 12 feet) in length. This
Costa Rica. This species is found in mesic lowland broadleaf forest or
specimen was photographed by Laurie J. Vitt in Mato Grosso, Brazil.
rainforest. This snake was photographed by the author at the Instituto
Clodomiro Picado, University of Costa Rica, in San José.
Figure 1.36. Central American Jumping Pit Viper (Atropoides

Figure 1.34. A Blotched Palm-pitviper (Bothriechis supraciliaris), mexicanus). This species is found from Mexico south to Panama, and
arboreal and endemic to Costa Rica. This species was once thought to it occurs on the Pacific slopes of Costa Rica, where this specimen was
be a subspecies of the Eyelash Pitviper, which it resembles found. It is ground-dwelling, well camouflaged, and has a stout body.
superficially. The color pattern varies, and specimens from most parts The common name of this genus—jumping pit viper—is attributable
of Costa Rica are variably blotched in dorsal coloration. This is a to energetic defensive strikes that sometimes lift the snake off the
captive individual that belonged to Carl Franklin and was ground as if it was “jumping.” This specimen was photographed by
photographed by the author. the author in Costa Rica.
All elapids are venomous, but some are far more dangerous are enveloped in transparent fetal membranes, from which
than others. Extremely toxic venoms are characteristic of they escape over the course of a few days (see chapter 9).
mambas, some cobras, and sea snakes as well as certain larger Elapids are represented in the Americas by coral snakes,
terrestrial species inhabiting Australia. There are more than which are brightly colored with patterns of bands and rings
270 species of elapids worldwide, and they occur throughout a that are commonly mimicked by harmless species with
diversity of habitats including warm, tropical oceans and some overlapping ranges (figs. 1.51, 1.52, 5.19). There are about 65
of the world’s driest deserts. Most terrestrial species are ovipa- species of coral snakes, primarily neotropical in distribution.
rous, but viviparity is characteristic of some African and many Most coral snakes eat other reptiles, including snakes, and
Australian forms. Other species (e.g., Australian Red-bellied such dietary specialization also is characteristic of various
Black Snake, Pseudechis porphyriacus) give birth to young that other elapids inhabiting the Old World.
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Figure 1.38. The head of a Jameson’s Mamba (Dendroaspis
jamesoni), a highly arboreal species of elapid that is common
throughout central Africa. Photograph by John C. Murphy.
Figure 1.37. An adult Fea’s Viper (Azemiops feae) from Cao Bang
province, Vietnam. Photograph by Dr. Nikolai L. Orlov, Russian
Academy of Sciences.
lakes where they feed primarily on fish. Various other elapids
are arboreal, and others of varying habits resemble New
World coral snakes. Among the latter are seven species of Af-
Cobras and their relatives such as kraits and mambas rican garter snakes (Elapsoidea spp.), so-called Asian coral
occur over extensive regions of Africa and Asia. Mambas snakes (Calliophis spp.; fig. 1.41), and two peculiar species of
(Dendroaspis spp.) are native to sub-Saharan Africa where the genus Maticora having exceptionally elongate venom
they pose a particular hazard to humans because of their glands measuring up to one-third of the body length! These
arboreal habits, swift movements, and aggressive defenses. are also called coral snakes. Many coral snakes, including all
Because a mamba might be well concealed while resting in a the Old World species, may raise their tail when disturbed
shrub or low tree one or more meters above the ground, and display brilliant colors on the underside of the body.
accidental encounters might involve an aggressive bite re- More than a fourth of the world’s elapid snakes are repre-
ceived at the head or chest level (fig. 1.38). Cobras are sented by the diverse radiation of species inhabiting Austra-
common throughout much of Africa and Asia, posing po- lia, New Guinea, and nearby islands. It is interesting to
tential dangers to humans, but the perception of danger is become acquainted with these snakes, as many species have
exaggerated by the spectacular behaviors of rising erect evolved similarities with counterparts in other snake families
while spreading the neck region into a hood and emitting by the process called convergent evolution. Thus, there are
loud and abrupt hisses (fig. 1.39). The hoods of cobras often large and swift terrestrial species of elapids that are very sim-
bear markings that resemble eyes and have startling effects. ilar in behaviors and movements to colubrid whipsnakes and
Several species of cobras have evolved the habit of spitting racers; others resemble secretive or burrowing species such as
venom toward an intruder, often aiming for the eyes (see ringneck snakes, ground snakes, and Asian coral snakes; and
fig. 2.29). A number of Australian elapids also exhibit hood- still others are similar to arboreal species of colubrids, and so
ing behaviors, but the neck is seldom flattened as exten- forth. A very impressive convergence of body form and be-
sively or consistently as in cobras. One of the more havior involves three species of Australian death adders (Ac-
spectacular species of cobra is the King Cobra (Ophiophagus anthophis spp.), which resemble some terrestrial vipers (fig.
hannah) of southern and southeastern Asia (fig. 1.39). Some 1.42). The similarities include cryptic coloration, stout body
specimens reach a length of 5 m, and all feed on other with triangular head, ambush method of capturing prey, and
snakes, which is the basis of the generic name. The King luring of prey by wiggling an elevated tail. Death adders also
Cobra is the longest venomous snake living today. have evolved relatively long fangs that fit into fleshy sockets
Other Asian elapids include 13 species of terrestrial kraits in the floor of the mouth. The sockets are receptacles for the
(Bungarus spp.), which are brightly colored, nocturnal species fangs, which like other elapids are fixed in place but, like vi-
that prey on other snakes and often bite persons while they pers, have some mobility and are relatively long for snaring
sleep on the ground or in huts (fig. 1.40). Like coral snakes, and envenomating mammals and birds. Other large, swift,
kraits often live sympatrically with harmless or mildly ven- and dangerous elapids playing counterpart role to mambas,
omous colubrid snakes that mimic them. Two species of Bou- cobras, and large, diurnally active colubrid snakes include two
lengerina (called water cobras) frequent rocky shorelines of species of taipan (Oxyuranus spp.), brown snakes (Pseudonaja
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nuchalis and P. textilis), tiger snakes (No-
techis spp.), and the Red-bellied Black
Snake (Pseudechis porphyriacus).
Two radiations of elapids have
evolved marine habits (independently)
and are collectively called “sea snakes.”
These were formerly sometimes classi-
fied into two separate families, but here
are treated as two clades within the Elap-
idae. This latter classification scheme
seems most widely accepted at the pre-
sent time. Sea snakes known generally as
sea kraits (Laticaudini) include eight
species of amphibious elapids that are
oviparous and spend varying amounts of
time in humid, near-shore environments
such as rocky shores and limestone crev-
ices of islands in the western Pacific
Ocean (fig. 1.43). These snakes spend
much time at sea, however, where they
feed on fishes, largely or exclusively eels.
The other sea snakes—roughly 60 spe-
cies (Hydrophiini)—are entirely marine
and give birth to live young at sea. The
Yellow-bellied Sea Snake (Pelamis pla-
turus) is uniquely pelagic in habits and is
the only species of marine elapid to have
reached the Americas, being quite
common along the Pacific coast from Baja
California to Ecuador (fig. 1.44). Else-
where it is the world’s most widely distrib-
uted snake, ranging from the southeast
coast of Africa across the Indo-Pacific to
the Americas. Recently, Kate Sanders and
colleagues have suggested that the Yel-
low-bellied Sea Snake and several other
mostly monotypic genera be recognized Figure 1.39. Cobras with defensive hoods on display. The upper left photo features a
as a single genus, Hydrophis, based on dorsal view of an Indochinese Spitting Cobra (Naja siamensis) photographed by the author
their studies providing an improved phy- in Thailand. The upper right photo shows a ventral view of a raised Chinese Cobra (Naja
logenetic framework and evolutionary atra), photographed by Coleman Sheehy III in Taiwan. The lower photo displays the hood
timescale for hydrophiine sea snakes. I of a King Cobra (Ophiophagus hannah) photographed in India by Gowri Shankar.
believe this suggestion is adequately sup-

ported and justified, but I will retain the
name Pelamis platurus in this book simply Most hydrophiine sea snakes are moderate in size, measuring
because of its long-standing historic familiarity. usually between 0.5 and 1 m, while the largest species (Stokes’
Numerous other hydrophiine species occur generally on Sea Snake, Astrotia stokesii) reaches lengths near 2 m. Stokes’
coral reefs, where they prey on fishes or fish eggs. Some sea Sea Snake has a massive and muscular body and broad snout,
snakes have a generalist diet, consuming a variety of fishes, and its fangs are long enough to pierce a wetsuit (fig. 1.45).
while others are more specialized with prey often restricted These snakes have been reported to sometimes drift in the
to eels or gobies. Three species specialize on fish eggs and thousands together on slicks in the Strait of Malacca.
forage by probing the head into crevices and burrows. These Sea snakes as a group (both clades, or subfamilies) are
egg specialists have reduced fangs and relatively blunt faces. generally distributed throughout tropical marine and usually
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Figure 1.40. Many-banded Krait (Bungarus multicinctus)
photographed by Ming-Chung Tu in Taiwan.
Figure 1.41. Oriental Coral Snake (Calliophis sauteri), photographed

in Taiwan by Ming-Chung Tu.
Figure 1.43. Upper photo: Yellow-lipped Sea Krait (Laticauda

colubrina). Center photo: Blue-banded Sea Krait (Laticauda
Figure 1.42. Common Death Adder (Acanthophis antarcticus) laticaudata). Lower photo: Chinese Sea Krait (Laticauda
photographed by the author in Victoria, Australia. Note the superficial semifasciata). All snakes were photographed in Taiwan. Note the
resemblance to vipers, in terms of the stout body and triangular- paddle-shaped tails, which assist swimming. All three species are
shaped head. This species also has elongated fangs compared with predominantly marine, but tendencies to spend time on land
other elapid snakes, and some of its behaviors resemble those of increase from bottom to top. The upper and lower photographs
vipers (e.g., ambush foraging on prey). The resemblance of this are by Ming-Chung Tu, and the center photograph is by Coleman
species to vipers is a marvelous example of convergent evolution. M. Sheehy III.
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Figure 1.44. An exceptionally colorful Yellow-bellied Sea Snake (Pelamis platurus) photographed from beneath the ocean surface off the
Pacific coast of Costa Rica. This snake depicts a typical “float-and-wait” posture that is used when these snakes lie at the ocean surface, where
they feed on relatively small pelagic fishes. Photograph by Joseph Pfaller.
nearshore waters with greatest species diversity in the Aus- approximately 320 genera and more than 1,800 species dis-
tralasian region. Australia has an especially rich fauna of ma- tributed throughout the New and Old World land masses. At
rine snakes, which include over half of the world’s species. least seven subfamilies are recognized. It is difficult to describe
The genus Hydrophis contains by far the most species, which these snakes in general terms, and the subfamilies are not
is around 50 percent of the world’s total. All sea snakes— easily assigned to single common names. It is worth pointing
both hydrophiine and laticaudine species—characteristically out that the family Colubridae is not the same thing as the
have flattened, paddle-shaped tails (figs. 1.43–1.45; see also larger, more inclusive taxon Colubroidea.
chapter 3) and nostrils with valve-like structures that can Snakes belonging to the subfamily Natricinae (more than
close the external openings (see figs. 6.10 and 7.14). During 200 species) are a familiar element of the snake fauna of North
swimming, the body also is flattened in a dorsoventral plane America and include the water snakes (Nerodia spp.; Natrix in
as an aid to more efficient locomotion (see chapter 3). Some the Old World), garter and ribbon snakes (Thamnophis spp.),
species dive as deep as 100 m (Hydrophis), but most live in and related species (e.g., Queen Snake and crayfish snakes, Re-
relatively shallow waters ranging generally from 20 to 50 m gina spp.; Swamp Snake, Seminatrix pygaea) (fig. 1.46, 147; see
in depth. The skin of sea snakes that have been carefully in- also figs. 4.2 and 4.8). Counterparts to the North American
vestigated is modified to exchange a substantial fraction of species are represented by other genera distributed largely in
respiratory gases and also to vent nitrogen as an aid in pre- Europe, Asia, and Africa. Natricine snakes are semiaquatic or
venting the Caisson disease (known as “the bends”). More amphibious, but none are completely aquatic like the elapid
information on the diving adaptations of these remarkable sea snakes. The diets are varied, but most feed on fish and am-
snakes is given in chapter 6. phibians. Reproduction varies within this group, as North
American species tend to give birth to live young, whereas the
Colubrids: Common, Diverse, and majority of Old World species lay eggs.
Familiar Snakes More than 650 species considered to be “typical” colubrids
Many of the familiar and common “harmless” or rear- have worldwide distribution and are classified in the subfamily
fanged snakes belong to the family Colubridae, which contains Colubrinae (fig. 1.48). Some of the more familiar species
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Figure 1.46. A Bluestriped Garter Snake, Thamnophis sirtalis
similis, photographed in Levy County, Florida by Dan Dourson.
Figure 1.45. Some species of sea snakes grow large and bulky. At
the left, Arne Rasmussen holds a large adult Hydrophis ornatus,
captured in the seas near Sulawesi (photograph by Erik Frausing).
The inset shows a specimen of the largest sea snake species, Astrotia
stokesii, captured on the Australian Great Barrier Reef by Robb
Dockerill and photographed by the author.
include king snakes and milk snakes (Lampropeltis spp.), rat

snakes (Elaphe and Pantherophis spp.), racers and whipsnakes
(Coluber, Drymobius, and Masticophis spp.), various smaller
species of secretive ground-dwelling snakes (e.g., Tantilla
spp.), large indigo snakes (Drymarchon spp.), rear-fanged
mangrove, tree, or cat snakes (Boiga spp.; the Brown Tree
Snake Boiga irregularis being known for having invaded Guam
and decimated parts of the native bird fauna), specialized
feeders such as the African egg-eating snakes (Dasypeltis spp.;
see chapter 2), swift-moving arboreal species (Thelotornis, Den-
drelaphis, Opheodrys, spp. and others) including the remark-
able Asian flying snakes (Chrysopelea spp.; see chapter 3). The
latter have evolved morphological and behavioral specializa-
tions for gliding. Many of the colubrine snakes are a conspic-
uous and common element of North American vertebrate Figure 1.47. Two species of water snakes common to Florida. The
fauna and well known to may persons residing on that conti- upper photo features the Florida Banded Water Snake (Nerodia
fasciata pictiventris), and the lower photo shows the Florida Green
nent. Interestingly, there is a parallel dominance of numerous
Water Snake (Nerodia floridana). An enlargement of the head is shown
species of venomous elapids that are equally familiar to resi- in the inset. Both snakes were photographed in Levy County, Florida,
dents of Australia, where terrestrial colubrids are largely by Dan Dourson.
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Figure 1.48. A sample of characteristic colubrid species in the subfamily Colubrinae. Upper left, Central American Blacktail Cribo
(Drymarchon melanurus), photographed in Belize by Dan Dourson. Upper right, Florida Redbelly Snake (Storeria occipitomaculata obscura),
photographed in Gainesville, Florida by the author. Middle left, Central American Speckled Racer (Drymobius margaritiferus), belonging to a
clade of snakes also known as Neotropical racers. This individual was photographed in Belize by Dan Dourson. Middle right, Black Rat Snake
(Pantherophis obsoletus), photographed in Florida by Dan Dourson. Lower left, Brown Vine Snake (Oxybelis aeneus), photographed in Belize
by Dan Dourson. Lower right, Puffing Snake (Pseustes poecilonotus) named for its defensive display of laterally compressed neck. This
specimen was photographed in Belize by Dan Dourson.
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absent. The two respective faunas—elapids in Australia and Other species are fossorial or aquatic. Xenodontines prey
colubrines in North America—exhibit numerous convergences on a range of animals, mostly vertebrates. Some are rear-
in habitats that are structurally and climatically similar. Diets fanged but with relatively mild venom. Most xenodontines
of the various colubrine species are remarkably diverse, and lay eggs, but viviparity occurs in some species.
the large majority of species are oviparous with some laying A clade of snakes formerly defined as Central American
large numbers of eggs (40 or more). xenodontines are now considered to be a subfamily called
The subfamily Xenodontinae is a monophyletic taxon Dipsadinae and a sister group to the Xenodontinae. The Dip-
that contains about 300 species of medium to large (1.3 m) sadinae include about 350 species of mostly small to medium-
terrestrial snakes found in a diversity of habitats in North, sized snakes having diverse habits and diets, mostly in Central
Middle, and South America. This group includes all of the and South America. Blunt-headed vine snakes (Imantodes
endemic colubrids of the West Indies and the Galapagos Is- spp.) are extremely slender and arboreal and feed on lizards
lands. Some of the false coral snake species belong to this (fig. 1.51). Many dipsadine snakes, however, specialize on in-
group, as well as the familiar North American hognose vertebrates such as earthworms or gastropods, and include
snakes (Heterodon spp.; fig. 1.49), which specialize on eating the interesting snail-eating snakes (e.g., Dipsas, Sibon spp.;
toads. Ringneck snakes (Diadophis spp.) and Mud Snakes fig. 1.52). Nearly all of the dipsadine species are oviparous.
(Farancia abacura) are also xenodontines (fig. 1.50). The
three species just mentioned belong to a subfamily Car-
phophiinae, which also includes the genera Carphophis and
Contia. A number of the tropical species are swift and racer-
like in appearance with arboreal or semiarboreal habits.
Figure 1.50. Two North American xenodontine snake species, both

featured in a defensive posture with the tail elevated to display the
colorful underside. The upper photo with inset features a Prairie
Figure 1.49. Western Hognose Snake (Heterodon nasicus). These Ringneck Snake (Diadophis punctatus) photographed in Kansas by
photographs feature the upturned and heavily cornified snout used as the author. The lower photo shows a Mud Snake (Farancia abacura)
an aid in burrowing. Other features of this snake superficially photographed in Florida by Dan Dourson. Both species are secretive
resemble a viper.Photographs by the author. and display the red to orange underside of the tail when disturbed.
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Gastropod Feeders in the Old World slender with broad, blunt heads and large eyes (fig. 1.53).
There are about 20 species of Old World snail- and slug-eat- These snakes are primarily nocturnal, and all are oviparous.
ing snakes, ecologically equivalent to the neotropical gen-
era Dipsas and Sibon, that belong to a separate family The Homalopsidae: Snakes of Mud and Water
Pareatidae. The New and Old World gastropod feeders were Another group of colubroid snakes with partial to strong
once thought to be closely related, but the similarities are aquatic tendencies comprises the family Homalopsidae, which
now known to be attributable to convergence. The Asian is a well-defined lineage containing about 40 species distrib-
snakes belong to the genera Aplopeltura, Asthenodipsas, and uted largely in Southeast Asia and Australasia (fig. 1.54). Many
Pareas distributed through Southeast Asia and the Sunda of these species live in shallow water habitats, and they have
Shelf. Many of the species are arboreal and, like arboreal valved nostrils and dorsally directed eyes situated on the top
counterparts in some of the other subfamilies, extremely of the head (fig. 7.6). One species, the Keel-bellied Watersnake
(Bitia hydroides), superficially resembles the true sea snakes in
attributes of body form, including reduced ventral scales, rel-
atively enlarged posterior body, and a feebly compressed tail.
All homalopsids have enlarged fangs at the rear of the
mouth, which serve to envenomate prey usually consisting
of amphibians or fish. Some species (e.g., Fordonia and Ge-
rarda spp.) consume invertebrates, including hard-shelled
animals such as crabs or other crustaceans, which the snakes
Figure 1.51. A Blunt-headed Tree Snake (Imantodes cenchoa)

shown in its natural habitat of rainforest in Belize. Photograph by Dan
Dourson.
Figure 1.53. Two closely related Taiwan Slug Snakes (Pareas

formosensis) illustrating very different eye colors. Both snakes were
photographed in Taiwan and have been considered to be a single
species, although current unpublished studies may divide the species
into three. This species of the family Pareatidae is ecologically and
Figure 1.52. A Terrestrial Snail Sucker (Tropidodipsas sartorii) behaviorally convergent with various dipsadine colubrid snakes in the
photographed in its native habitat in Belize by Dan Dourson. New World. These snakes were photographed in Taipei by the author.
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snakes will be achieved through improved understanding of
both morphological and molecular data. At the time of this
writing, however, molecular studies are appearing so rapidly
that taxonomic revisions are not always adequately evaluated
by the broader community of systematists before other
studies appear and keep moving. This is sometimes confusing
to the novice for whom it is not always clear what is what.
In spite of the controversy over details, a generalized
phylogeny for snakes seems pretty well known and can be
qualified without too much debate. So here I shall present
what is simply a broad pattern of phylogenetic relation-
ships of snakes that is based in consensus insofar as
possible. The following discussion is with reference to a
Figure 1.54. A Puff-faced Water Snake (Homalopsis buccata) as
consensus phylogeny that is illustrated in figure 1.55.
seen from below when air-breathing in shallow water. Photographed
at Kota Samarahan, Sarawak, Malaysia by Indraneil Das.
What are called lepidosaurs include the ancient but still
living New Zealand tuataras and the squamates, which are
sister taxa (fig. 1.10). Sister taxa (or groups) are derived
amazingly rip apart into smaller pieces to swallow. Some from an ancestral species not shared by any other taxon,
members of this family occupy freshwater habitats such and they appear on a cladogram as lineages that arise as
as lakes, swamps, or streams (e.g., numerous species of branches from a single divergence node. Lepidosaurs are a
Enhydris), whereas others are estuarine and occur in shallow sister group to the branch of reptiles that gave rise to the
coastal marine waters (e.g., Dog-faced Water Snake, Cer- birds and crocodilians, as illustrated in figure 1.10. The
berus rhynchops). One very unusual species, popular among squamates are further subdivided into lizards, amphisbae-
some herpetoculturists, is the aquatic Tentacled Snake (Er- nians, and snakes. The snakes collectively comprise the sub-
peton tentaculatum) from southeastern Asia (fig. 7.14). This order Serpentes, which is sometimes called Ophidia. Snakes
snake has two fleshy “tentacles” on its snout, which are sen- are considered to be monophyletic but have diverged con-
sory and are likely an aid to navigation in murky water as siderably from ancestral conditions. They have diversified
well as provider of information from mechanical stimuli to form a rich assemblage of species within the squamates.
such as the disturbance to water when a swimming fish is Here you will see a simplified phylogeny of snakes based
nearby (fig. 2.10). It appears that all homalopsids give birth in consensus from a number of studies including both mor-
to live young, and some may reach incredibly high popula- phological and molecular data (fig. 1.55). The early or basal
tion densities. In some habitats, Cerberus rhynchops can divergence of snakes occurred between the Scolecophidia
reach densities up to three individuals per square meter! and all other snakes comprising the Alethinophidia. The he-
nophidian snakes are polyphyletic and diversified relatively
early into many taxa including the evolution of boas and
Toward a Phylogeny of Snakes pythons. The placement of acrochordids (Acrochordidae, or
Confusion over the evolutionary history and taxonomic Acrochordoidea) was long considered to be problematic, but
classification of snakes has stimulated both debate and con- recent taxonomic arrangements consider the only three spe-
troversy among scientists for decades. The works of Bogert, cies of acrochordids to be a lineage that is sister to the Colu-
Cope, Dowling, Duméril, Dunn, Hoffstetter, Jan, Under- broidea. Within the latter group, the viperid snakes are sister
wood, and others provided the classical foundations for snake to the collective taxa of elapids, lamprophiids, homalopsids,
phylogeny, while more recent historical reviews of the pro- and colubrids. The reader may consult recent descriptive tax-
gress made have been offered by Burbrink, Cadle, Crother, onomic and phylogenetic literature for more details re-
Greene, Rieppel, Pyron, Vidal, Wiens, Wilcox, Zaher, and garding the classification of higher snakes, much of which is
others. Knowledge of morphology continues to be helpful to still unresolved or in dispute. One recent molecular phyloge-
evaluate phylogeny, and molecular studies have provided netic analysis places acrochordids, pareatids, and xenoder-
large quantities of data that have advanced the understanding matid snakes as basally divergent from other caenophidians,
of ophidian evolution rapidly. Numerous scientists are and suggests that viperid snakes comprise a successive sister
now contributing molecular studies and adding new insights clade to all remaining caenophidians. The fairest thing I can
concerning phylogenetic relationships at all levels, including say is that one may regard all current phylogenetic trees as
specific and limited assemblages as well as higher level “fluid” hypotheses about evolutionary events that are be-
taxa. Ultimately, consensus of a comprehensive phylogeny of coming increasingly, but not entirely, understood.
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Scolecophidia
Typhlopidae
Scolecophidia
Leptotyphlopidae
Anomalepididae
Aniliidae
Tropidophiidae
Loxocemidae
Pythonidae
Xenopeltidae
Henophidia
Serpentes
Boidae
Calabariidae
Bolyeriidae
Serpentes
Alethinophidia
Anomochilidae
Henophidia
Cylindrophiidae
Alethinophidia Uropeltidae
Acrochordidae
Xenodermatidae
Pareatidae
Caenophidia
Viperidae
Colubroidea
Caenophidia
Homalopsidae
Colubroidea Lamprophiidae
Elapidae
Colubridae
Figure 1.55. A phylogeny of snakes illustrating the author’s interpretation of current consensus among
herpetological systematists, all of whom do not agree on the details of the relationships. Any such phylogeny should
be considered “fluid” (or a hypothesis) and is expected to change as new work is done based on molecular and other
methods. The phylogeny illustrates relationships among the principal families of snakes that are listed as terminal
branches at the right of the figure. Higher taxa, or groupings of families, are bracketed with bars at the right, each
corresponding to principal branchings that are identified within the phylogenetic tree. Drawing by Coleman M.
Sheehy III and the author.
Returning to our earlier question—What is a snake?—a Alfaro, M. E., D. R. Karns, H. K. Voris, C. D. Brock, and B. L. Stuart.
summary definition might be given as follows. A snake is a 2008. Phylogeny, evolutionary history, and biogeography of
Oriental-Australian rear-fanged water snakes (Colubroidea:
squamate reptile of the suborder Ophidia (or Serpentes),
Homalopsidae) inferred from mitochondrial and nuclear DNA
characterized by having a cylindrical, limbless, and scaled sequences. Molecular Phylogenetics and Evolution 46:576–593.
body with fused eyelids and no external ear. The jaws are mod- Cadle, J. E. 1987. Geographic distribution: Problems in phylogeny
ified for capturing and swallowing relatively large prey, and and zoogeography. In R. A. Seigel, J. T. Collins, and S. S. Novak
numerous species in various taxa are venomous. Other attrib- (eds.), Snakes: Ecology and Evolutionary Biology. New York:
utes will become better understood and more appreciated as Macmillan, pp. 77–105.
Cadle, J. E. 1994. The colubrid radiation in Africa (Serpentes:
the reader explores the remaining chapters in this book.
Colubridae): phylogenetic relationships and evolutionary
patterns based on immunological data. Zoological Journal of the
Additional Reading Linnean. Society 110:103–140.
Adalsteinsson, S. A., W. R. Branch, S. Trape, L. J. Vitt, and S. B. Caprette, C. L., M. S. Y. Lee, R. Shine, A. Mokany, and J. F. Down-
Hedges. 2009. Molecular phylogeny, classification, and bioge- hower. 2004. The origin of snakes (Serpentes) as seen
ography of snakes of the family Leptotyphlopidae (Reptilia, through eye anatomy. Biological Journal of the Linnean Society
Squamata). Zootaxa 2244:1–50. 81:469–482.
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Cohn, M. J., and C. Tickle. 1999. Developmental basis of limbless- advanced snakes (Colubroidea), with discovery of a new sub-
ness and axial patterning in snakes. Nature 399:474–479. family and comparison of support methods for likelihood
Greene, H. W. 1997. Snakes: The Evolution of Mystery in Nature. trees. Molecular Phylogenetics and Evolution 58:329–342.
Berkeley: University of California Press. 351 pp. Sanders, K. L., M. S. Y. Lee, Mumpuni, T. Bertozzi, and A. R. Ras-
Gutberlet Jr., R. L., and M. B. Harvey. 2004. The Evolution of New mussen. 2012. Multilocus phylogeny and recent rapid radiation
World Venomous Snakes. In J. A. Campbell and W. W. Lamar of the viviparous sea snakes (Elapidae: Hydrophiinae). Molecular
(eds.), Venomous Reptiles of the Western Hemisphere, vol. 2. Phylogenetics and Evolution 66:575–591.
Ithaca, NY: Comstock (Cornell University Press), pp. 634–682. Scanlon, J. D., and M. S. Y. Lee. 2011. The major clades of snakes: Mor-
Head, J. J., J. I. Bloch, A. K. Hastings, J. R. Bourque, E. A. Cadena, phological evolution, molecular phylogeny, and divergence dates.
F. A. Herrera, P. D. Polly and C. A. Jaramillo. 2009. Giant boid In R. D. Aldridge and D. M. Sever (eds.), Reproductive Biology and
snake from the Palaeocene neotropics reveals hotter past equa- Phylogeny of Snakes. Vol. 9 of Reproductive Biology and Phylogeny,
torial temperatures. Nature 457:715–718. B. G. M. Jamieson, series editor. Enfield, NH: Science Publishers,
Heatwole, H. 1999. Sea Snakes. Malabar, FL: Krieger Publishing. pp. 55–95.
Hedges, S. B. 2008. At the lower size limit in snakes: Two new spe- Shine, R. 2009. Australian Snakes: A Natural History. Frenchs For-
cies of threadsnakes (Squamata: Leptotyphlopidae: Leptotyph- est, New South Wales, Australia: Reed New Holland.
lops) from the Lesser Antilles. Zootaxa 1841:1–30. Slowinski, J. B., and J. S. Keogh. 2000. Phylogenetic relationships
Heise, P. J., L. R. Maxson, H. G. Dowling, and S. B. Hedges. 1995. of elapid snakes based on Cytochrome b mtDNA sequences.
Higher-level snake phylogeny inferred from mitochondrial Molecular Phylogenetics and Evolution 15:157–164.
DNA sequences of 12S rRNA and 16S rRNA genes. Molecular Townsend, T. M., A. Larson, E. Louis, and J. R. Macey. 2004. Mo-
Biology and Evolution 12:259–265. lecular phylogenetics of squamata: The position of snakes,
Highton, R., S. B. Hedges, C. A. Hass, and H. G. Dowling. 2002. amphisbaenians, and dibamids, and the root of the squamate
Snake relationships revealed by slowly-evolving proteins: Fur- tree. Systematic Biology 53:735–757.
ther analysis and a reply. Herpetologica 58:270–275. Vidal, N. 2002. Colubroid systematics: Evidence for an early ap-
Hoso, M., T. Asami, and M. Hori. 2007. Right-handed snakes: Con- pearance of the venom apparatus followed by extensive evo-
vergent evolution of asymmetry for functional specialization. lutionary tinkering. Journal of Toxicology: Toxin Reviews
Biology Letters 3:169–172. 21:21–41.
Keogh, J. S. 1998. Molecular phylogeny of elapid snakes and a con- Vidal, N., and S. B. Hedges. 2002. Higher-level relationships of
sideration of their biogeographic history. Biological Journal of snakes inferred from four nuclear and mitochondrial genes.
the Linnaean Society 63:177–203. Comptes Rendus Biologies 325:977–985.
Knight, A., and D. P. Mindell. 1994. On the phylogenetic relation- Vidal, N., and S. B. Hedges. 2002. Higher-level relationships of cae-
ships of Colubrinae, Elapidae and Viperidae and the evolution nophidian snakes inferred from four nuclear and mitochon-
of front fanged venom systems in snakes. Copeia 1994:1–9. drial genes. Comptes Rendus Biologies 325:987–995.
Kraus, F., and W. M. Brown. 1998. Phylogenetic relationships of Vidal, N., and S. B. Hedges. 2004. Molecular evidence for a terrestrial
colubroid snakes based on mitochondrial DNA sequences. Zoo- origin of snakes. Proceedings of the Royal Society of London B (Sup-
logical Journal of the Linnean Society 122:455–487. pl.) 271:S226–S229.
Lee, M. S. Y. 2005. Molecular evidence and marine snake origins. Vidal, N., S. G. Kind, A. Wong, and S. B. Hedges. 2000. Phyloge-
Biology Letters 1:227–230. netic relationships of Xenodontine snakes inferred from 12S
Lee, M. S. Y., A. F. Hugall, R. Lawson, and J. D. Scanlon. 2007. and 16S ribosomal RNA sequences. Molecular Phylogenetics and
Phylogeny of snakes (Serpentes): Combining morphological Evolution 14:389–402.
and molecular data in likelihood, Bayesian and parsimony Wiens, J., and J. L. Slingluff. 2001. How lizards turn into snakes:
analysis. Systematics and Biodiversity 5:371–389. A phylogenetic analysis of body-form evolution in anguid
McDowell, S. B. 1987. Systematics. In R. A. Siegel, J. T. Collins, and lizards. Evolution 55:2303–2318.
S. S. Novak (eds.), Snakes: Ecology and Evolutionary Biology. Wiens, J. . ., C. A. Kuczynski, S. A. Smith, D. G. Mulcahy, J. W.
New York: Macmillan, pp. 3–50. Sites Jr., T. M. Townsend, and T. W. Reeder. 2008. Branch
Pough, F. H., R. M. Andrews, J. E. Cadle, M. L. Crump, A. H. Sav- lengths, support, and congruence: Testing the phylogenomic
itzky, and K. D. Wells. 2004. Herpetology. 3rd edition. Upper approach with 20 nuclear loci in snakes. Systematic Biology
Saddle River, NJ: Pearson Prentice-Hall. 544 pp. 57:420–431.
Pyron, R. A., and F. T. Burbrink. 2011. Extinction, ecological op- Zaher, H., F. G. Grazziotin, J. E. Cadle, R. W. Murphy, J. C. de
portunity, and the origins of global snake diversity. Evolution Moura-Leite, and S. L. Bonatto. 2009. Molecular phylogeny of
66:163–178. advanced snakes (Serpentes, Caenophidia) with an emphasis
Pyron, R. A., F. T. Burbrink, and J. J. Wiens. 2013. A phylogeny and on South American Xenodontines: A revised classification and
revised classification of Squamata, including 4161 species of description of new taxa. Papéis Avulsos de Zoologia (Museu de
lizards and snakes. BMC Evolutionary Biology 13:93. Zoologia da Universidade de São Paulo) 49:115–153.
Pyron, R. A., F. T. Burbrink, G. R. Colli, A. N. Montes de Oca, L. J. Zug, G. R., L. J. Vitt, and J. P. Caldwell. 2001. Herpetology. 2nd
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FE EDING, DI GE ST I ON, AND
WAT E R BALANC E
There are many and ridiculous stories about the swallowing feats of the
big snakes. The tales relating to giant pythons engulfing animals as large as
an ox are utterly fallacious, nor do the big snakes ever wantonly attack large
2
mammals. The limit of their swallowing capacity would be a moderate-sized
antelope—an animal about the size of an American white-tailed deer—and
nothing but an unusually large specimen could engulf such prey. A twenty-
foot python has been observed by the writer to swallow a forty-pound pig
and the process was by no means an easy one.
—Raymond L. Ditmars, Reptiles of the World (1943), p. 140
Feeding is one aspect of snake behavior that generally fasci- effective means by which they capture and utilize prey? As-
nates people. There are perhaps two root causes that elicit pects of these questions have fascinated people for cen-
both interest and awe in the feeding habits of snakes. First, turies (fig. 2.3).
the animals are limbless and must overpower their prey by
such unusual means as constriction or envenomation. Sec-
ond, snakes are intermittent feeders, and most of the Constraints Related to a Limbless and
common and usually larger species that are familiar to Elongate Body Form
people consume prey that is larger in girth than the mouth The following discussion is essentially speculative, but it
of the snake. Many persons are fascinated that snakes provides a conceptual basis from which to launch consider-
swallow relatively large prey and manage to do so by what ations of feeding and digestion in snakes. Fundamentally,
appears to be amazing elastic properties of the jaws (figs. because snakes are lacking arms and legs, they cannot
2.1, 2.7). The skin also stretches an amazing amount as the catch, handle, and manipulate prey in the same manners
prey item is swallowed beyond the jaws. that are employed by many other animals. Moreover, with-
A snake is basically a long tube and possesses an elon- out an effective “anchor”—or means of stable stance—it is
gated digestive system (fig. 2.2). Thus, a snake could more somewhat problematic or difficult for an animal to browse
or less continually process numerous small items, such as or graze on vegetation. So what are the most likely foods
insects or small eggs, or it could feed intermittently on that are available to snakes?
larger items that are accommodated by stretch of the gut, Insofar as snakes are elongate creatures without limbs,
body wall, and skin. Most snakes utilize the second option we may consider them to be a long tube with a head at the
and swallow the prey entire because they have not evolved front end and a tail at the rear. There are three ways in which
teeth that are specialized for tearing, shredding, breaking, such an animal might capture food: (1) seize it with the
or mashing the food into smaller pieces. It is interesting to mouth, (2) wrap the body around it, or (3) wrap the tail
consider the evolutionary reasons why snakes have evolved around it. Two further considerations are important. First,
the feeding habits they employ, and to ask: What is unique the head is at the end of the animal that first encounters the
about snakes that constrain or limit the prey they exploit environment. Second, regardless of the manner of capture,
and the manner in which they feed? On the other hand, the prey object must be seized by the mouth before swal-
one can ask: What attributes of snakes have provided evo- lowing. For these reasons, it seems reasonable to expect the
lutionary opportunities for employing the exceptionally head end of the snake to evolve a mouth with associated
| 37
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evolutionary radiation of snakes involved a diversification
of feeding specializations for capturing animal prey ranging
in size from smaller organisms such as insects, fish, frogs,
or lizards to larger avian and mammalian prey having a
range of body sizes. Because of the central role of the head
in capturing prey, snakes evolved either venoms or con-
stricting mechanisms that subdue prey rapidly in order to
avoid potential harm that might be inflicted by the prey.
This is especially important for the capture of larger species
that are capable of inflicting considerable damage to a snake.
Snakes are well adapted for swallowing relatively large
prey entire, without reduction to smaller pieces. There is,
however, at least one documented exception to this state-
ment. Gerard’s Water Snake (Gerarda prevostiana), a homalop-
sid species, eats crabs by tearing them apart and ingesting
the individual pieces. Reducing the prey to pieces is accom-
plished by holding a crab by the mouth and pulling it through
a loop of the body that is formed around it, thereby straining
the joints of the crab and causing them to separate. This be-
havior was reported by Bruce Jayne, Harold Voris, and Peter
Ng, but it is rare as far as we know.
The majority of snakes are characterized by compara-
tively high mobility of the jaws and a large gape size. More
basal groups of snakes feed primarily on elongate prey such
as earthworms, lizards, or invertebrates, whereas innova-
tions of the feeding apparatus enabled larger snakes to
consume heavier and bulkier prey, particularly mammals.
Furthermore, snakes or other animals that specialize on
eating particular prey typically possess behavioral and mor-
Figure 2.1. Photos illustrating the distensibility of jaws and skin
phological traits that facilitate successful foraging. These
when snakes ingest relatively large objects. In the upper photo an
Indian Egg-eating Snake (Elachistodon westermanni) swallows a bird
are generally less important in snakes that have a relatively
egg, with amazing stretch of both mucosal tissue and scales on the broad diet, and especially ones that might include carrion
lower jaw. The lower photo illustrates a Green Anaconda (Eunectes as well as living prey.
murinus) swallowing a deer. The upper photo is courtesy of Parag
Dandge; the lower photo is courtesy of Jesús A. Rivas.
The Kinetic Skull and Prey Transport

Many persons have witnessed dramatic scenes of snakes
jaws and teeth that are adapted for seizing prey, in con- swallowing animals that are larger around than their head,
trast to cutting or masticating prey. Also, we must remem- and it is well known that these prey are swallowed whole
ber that snakes evolved from lizard-like ancestors and and then moved to the stomach by muscular actions called
thus inherited lizard-like attributes both of dentition peristalsis. The swallowing of prey is called prey transport by
and gape. functional morphologists, and it is accomplished in snakes
Snakes as a group exhibit a propensity to grasp prey only because of unusual mobility of various elements of the
items using the mouth, and this involves having an appro- skull and jaws. The term, of course, implies movement of
priate gape and a good set of recurved teeth. Without having prey and also includes “transport” through the esophagus
appendages for grasping, holding, and manipulating prey, to the stomach.
the teeth must hold the prey firmly, or there must be an al- The skulls of snakes are derived from those of lizards and
ternative means to immobilize the prey. Immobilization is have been further modified for kinesis (joint mobility) and a
achieved either by injecting the prey item with toxic venom, functional need to better enclose the brain cavity. Anyone
enwrapping the prey item in body coils, or holding the who has watched a snake swallow a prey item such as a mouse
item firmly within the mouth. Whatever the reasons, the appreciates the mobility of jaws and skull that are necessary
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for the animal to manipulate the prey
without having arms or hands, and to
swallow something that is large in terms
of its relative girth. In living reptiles ex-
cept for turtles, the skull has two postor-
bital or temporal openings (termed
fenestrae), known as a diapsid condition.
Thus, bony elements of the skull form two
temporal arches, one below the lower
opening and one between the lower and
upper opening. Most lizards have lost the
lower temporal arch, whereas snakes have
lost both of the temporal arches (fig. 2.4).
This feature lightens the skull and in-
creases the potential for mobility (fig. 2.5).
Some of the skull bones form mov-
able joints with one another. Typically,
the quadrate bone articulates loosely to
Figure 2.2. Internal anatomy of a young Florida Cottonmouth (Agkistrodon piscivorus
join the lower jaw with the skull above
conanti). Photograph by the author.
Figure 2.3. Historic drawing depicting large constrictors subduing large mammals, which are imaginary exaggerations of the snakes’
abilities to swallow large prey. This antique print was originally from History of the Earth and Animated Nature, by Oliver Goldsmith (1774),
and used in a later edition A History of the Earth and Animated Nature, by Oliver Goldsmith, published by A. Fullarton (1850) and Blackie
and Son (1862).
Feeding, Digestion, and Water Balance | 39
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bone and the braincase. These generate a three-joint system
that facilitates lowering the lower jaw and increasing the
size of the gape. Other movable bones include the ectopter-
ygoid, maxilla, and prefrontal (figs. 2.5, 2.6). In other rep-
tiles these skull bones are fixed to the braincase or have
restricted movement, whereas in snakes these form a
linkage of bones having extensive motion relative to the
braincase. The parts are joined by ligaments and muscles,
characteristically with greater mobility than is seen in
lizards. The mechanical linkages include many units, and a
variety of movements is possible. Collectively, these permit
the capture and ingestion of relatively large prey, which
must be swallowed entire. The elements are loosely joined
together and operate independently on each side of the
head.
For all the movement and potential harm that could be
inflicted by the prey, the brain must be protected. The brain
of snakes is enclosed in a rigid structure that is formed by
downward extensions of the frontal and parietal elements
which are sometimes fused and articulate extensively with
bone that lies below the brain (fig. 2.6). These structures
form a rather solid braincase protecting the brain, and also
provide much of the surface area for the attachment of
muscles that power much of the movements that are in-
volved in feeding.
The conversion of much of the skull into a rigid box
necessitated the losses of certain hinges in the roof of the
skull that were present in lizards. The only movable part of
Figure 2.4. Fenestrae (openings) in the bony skull of representative
the skull roof of snakes is in the facial region where the
diapsid reptiles. The upper drawing illustrates a primitive diapsid nasal bones are hinged to the frontal elements (fig. 2.6). In
condition in which there are two complete temporal fenestrae, with the majority of living snakes the snout can move about this
each fenestra bounded by a bony temporal arch. This is characteristic joint, and the condition of having a kinetic joint anterior to
of some primitive reptiles (e.g., dinosaurs) and the living tuatara. The the eyes has been termed prokinesis. The palatomaxillary el-
middle drawing illustrates the skull of a lizard, representing
ements are movably attached to each other and to the snout
secondary loss of the lower temporal fenestra. The lower drawing
illustrates the skull of a snake with secondary loss of both the upper and prefrontal, which are capable of movement relative to
and lower temporal fenestrae. The evolutionary changes illustrated the braincase. Additionally, however, in natricine snakes
here eventually allowed extreme reduction of bone mass and the (Nerodia and Thamnophis), there are four movable elements
associated flexibility of the snake skull that is used during feeding. in the snout, and these impart a special condition of mo-
Drawings by Dan Dourson.
bility that has been termed rhinokinesis. In these snakes,
movements of the snout bones themselves allow the teeth
of the right and left sides to separate further, thereby in-
it. The condition of a movable quadrate is called strepto- creasing the extent of movement involved in each cycle of
styly, and this condition allows the quadrate to move for- swallowing (see below). Mobility of the nasal elements ac-
ward and rearward and, to a lesser extent, mediolaterally counts for the unusual rotations of the snout tip that are
with respect to the braincase. Streptostyly is associated sometimes seen during swallowing movements made by
with the loss of the temporal arches, and this allows the garter snakes.
quadrate to swing on a complex articulation between its The most uniquely important feature of kinesis in snakes
upper end and the side of the skull. Compared with liz- is its association with unilateral mobility of the jaws. Inde-
ards, the quadrate bone has extraordinary movement in pendent movements of the two sides of the lower jaw, cou-
snakes (fig. 2.5). pled with the fact that skin and other tissues connecting
There is also some degree of motion between the quadrate them are distensible, permit swallowing of prey that are
and the supratemporal bone, and between the supratemporal much larger than the normal size of the snake’s head (fig. 2.1
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and below). Most snakes transport prey
through the mouth using ratcheting move-
ments of the upper jaws, each jaw on right
or left side of the head alternately moving
over the prey. Characteristically, a snake
works prey (and that is whole prey) into its
mouth by alternately advancing and re-
tracting each of the jaws. During a unilat-
eral cycle of movement, the braincase of
the snake is advanced over the prey, rather
than the prey being “pulled” into the
mouth. The teeth-bearing elements of the
upper jaws are “walked” over the prey by
alternating shifts of their position, and the
prey is never free of grip during the swal-
lowing process. In most snakes the lower
jaws have little direct role in transporting
prey, but they serve to control the position
of the prey in the mouth and to press it
against teeth of the overlying palatine and
pterygoid bones (fig. 2.6). A detailed ex-
ample of a snake swallowing prey is shown
in fig. 2.7.
Basal or earlier-evolved snakes gener-
ally have more limited unilateral exten-
sion of the jaws, and the transport of
food appears to be the role of the maxil-
lary bone as well as the palatopterygoid
bar. However, feeding movements in the
basal (scolecophidian) thread snakes be-
longing to the Leptotyphlopidae exhibit a
unique feeding mechanism in which the
anterior tooth-bearing elements of the
lower mandibles (lower jaws) rotate syn- Figure 2.5. Skull of a Bearded Dragon lizard (Pogona vitticeps, upper photo)
chronously in and out of the mouth, compared with a skull of an Eastern Diamondback Rattlesnake (Crotalus adamanteus,
lower photo). The quadrate is movable in both animals, but much more so in the
thereby dragging the prey into the mouth
rattlesnake. Note that many elements of the rattlesnake skull are longer, and the skull is
and esophagus. The prey is transported lighter, compared with the lizard. Each maxilla of the rattlesnake bears a long fang, and
exclusively by movements of the lower there is an additional replacement fang also in view. The rostral end of the pterygoid
jaw, and such a transport mechanism is functions as a lever during erection of the fangs. Photos courtesy of Elliott Jacobson;
unusual among vertebrates. The authors skulls courtesy of Jeanette Wyneken (lizard) and Michael Sapper (rattlesnake).
of the study in which this mechanism was
reported—Nathan Kley and Elizabeth
Brainerd—named these feeding move- angular bones, which renders the joint between these
ments mandibular raking. Two joints in each lower jaw have elements extremely mobile.
unusual mobility and allow their distal half (splenial) to Thread snakes feed primarily on the larvae and pupae of
rotate backward into the mouth, something like swinging social insects and often face dangers during foraging be-
doors. In most other snakes these joints conform passively cause large, aggressive ants defend their nests tenaciously
to the shape of the prey being swallowed and thus maxi- and can easily kill small snakes. Mandibular raking allows
mize the “fit” of the gape to the prey item. In contrast, these snakes to feed quickly and to minimize the time they
mandibular raking in Leptotyphlops involves active flexion are exposed to potential attack. Studies show that cycles of
of these joints. Moreover, there is a rather wide dorsal gap mandibular protraction and retraction occur at frequencies
between the anterior splenial bone and the posterior that can exceed 3 Hz (cycles per second). This represents
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Figure 2.6. Skull and mandibles of a Black
Mamba (Dendroaspis polylepis). The fangs are
supported by the maxillae, which are relatively long
compared with vipers and pit vipers. As shown
here, the maxillary and palatine bones are capable
of erecting the fangs. Note the solid braincase
formed by downward extension of the frontal and
parietal bones. The photograph is by Elliott
Jacobson, and the skull was provided by Michael
Sapper.
exceptionally rapid feeding movements in a snake, and thereby Sibon, and Sibynomorphus (also called tree snakes), to the
reduces the “handling time” involved in swallowing the prey. Asian pareatine genus Pareas and Aplopeltura, and to the
Another example of feeding in which the mandibles have African genus Duberria. Additionally, there are many spe-
a primary role in transporting prey involves evolutionary cies of natricine snakes that occur sympatrically with slugs
modifications in advanced, rather than basal, snakes. Sev- and include them in their diet.
eral species of tropical colubrid snakes are specialized for Kinesis of the skull and jaws presumably enables more
feeding on snails. These snail eaters cannot crush the shell, effective apprehension of food by use of jaws in the absence
so they must extract the soft body of the snail from its of using the tongue. The tongue has assumed predomi-
shell. The snake carefully targets the soft body of a snail, nantly sensory functions in snakes and is not used to sub-
grasps it, and then uses its mandibles to extract the fleshy due or handle prey. Mobility of the jaws has another
body from its hard shell (fig. 2.8). The mandibles are in- important consequence. Transport of food in more special-
serted into the interior of the snail’s shell and pull the an- ized (less “primitive”) colubroid snakes has shifted to
imal into the mouth using movements that are at least varying extents from the maxillary bones to the more me-
superficially similar to those involved in mandibular raking. dial pterygoid bones (fig. 2.5). This uncoupling of structure
Research has shown that snail-eating snakes have ev- and function allowed for further evolutionary “innovation”
olved specializations that maximize the effectiveness with involving uses of the maxillary bone in prey capture and the
which snails are extracted from their shells. The snail body parallel evolution of specializations for the injection of
is asymmetric, and the shell of a snail opens either to the venom. These consequences for prey capture are discussed
right- or the left-hand side. There is a simple genetic basis in the next section.
for whether a shell is “right” or “left-sided.” Examination of
snake’s mandibles reveals that they differ in the number of
teeth on the right or left side. This asymmetry is present in Modes of Capturing and Subduing Prey
all 12 snail-eating specialists in the Pareatidae whereas the There are several ways in which snakes capture and subdue
jaws of two non-snail-eating species in the same subfamily prey. In nearly all cases, the head is all important and first
are symmetric. The asymmetry of the snail eaters matches meets the prey. One exception occurs in the file snakes,
the “sidedness” of the snails that predominate in their hab- particularly the Little File Snake Acrochordus granulatus,
itat, and it is easier for “right-mandibled” snakes to extract which capture fish using looping movements of the body
“right-sided” snails from their shells, and they experience trunk or tail. I have watched this behavior many times in
more difficulty if a snail is “left-sided.” captive snakes. Usually these snakes are rather sluggish in
Feeding on gastropods has evolved independently nu- many of their movements, and they are inclined to crawl
merous times among colubrid snakes. These species have around on a muddy substratum at the bottom of a water
vernacular names that include slugsnakes, slug-eating column rather than swim rapidly in the open water col-
snakes, snail-eaters, and snail-eating snakes—terms that umn. This is fitting, as this species lives largely in shallow
apply especially to the neotropical dipsadine genera Dipsas, coastal waters such as mangroves. When a fish swims near
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Figure 2.7. Sequence of jaw movements by a California King Snake (Lampropeltis californiae) swallowing a mouse that has been immobilized
by constriction. The jaw movements progress in sequence from left to right, each stroke advancing the upper jaw and skull of the snake over the
mouse (A through E). Note also the mouse is positioned within a loose coil of the snake, thereby “anchoring” the prey so that it does not shift
away from the snake during advances of the jaws. Except for the tail and the rear limbs, the entire mouse is within the neck of the snake in F.
At all stages, stretching of the skin between the scale rows can be seen. Photographs by author.
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Figure 2.8. A Cloudy Snail Sucker (Sibon nebulatus) in Belize
extracting a snail from its shell. The mandibles are inserted deeply Figure 2.9. A Yellow-bellied Sea Snake (Pelamis platurus) lies near
into the shell, and the recurved teeth are used to extract the snail the ocean surface in a “float-and-wait” posture, waiting to capture a
while the upper jaws grasp the shell. Photographs by Dan Dourson. small fish when it swims nearby (upper photo). The inset illustrates
the relatively long jaw that characterizes this species. In the lower
photo, a snake is shown with the mouth open to illustrate the gape
associated with the elongated jaws, effective for snaring small fishes
the snake and disturbs the water in a characteristic way,
from the water. These snakes were photographed on the Pacific coast
the snake rapidly throws part of its body around the fish, of Guanacaste, Costa Rica by Joseph Pfaller and Coleman Sheehy III
entrapping it with its spiny-keeled scales (see chapter 5). (inset).
These snakes often cruise in shallow waters of low tides,
hunting for fish that have become concentrated and more
easily captured because of the confinement of shallow movements of an open mouth. Small fishes are captured
water. In one instance I observed a snake that was swal- somewhat similarly by the pelagic Yellow-bellied Sea Snake,
lowing a fish while holding a second one it had captured Pelamis platurus. These snakes lie floating on the ocean sur-
within a loop of its trunk at midbody. While swallowing face using what has been called a “float and wait” strategy
and holding the second fish, it rapidly captured a third fish for snaring small fishes. When a fish swims nearby, the
by means of rapid coiling movements of its tail. Wow! snake captures it in its jaws by rapid sideward swiping
Three fish at a time! movements of the open mouth (fig. 2.9).
Other snakes possibly employ a similar strategy in using Recent studies by Kenneth C. Catania have demonstrated
loops or coils of the body to restrain a prey item—or at least that Tentacled Snakes (Erpeton tentaculatum), which are
slow its escape—while the head of the snake zeros in for a aquatic homalopsids, can take advantage of their prey’s es-
bite. Nerodia clarkii, the Gulf Salt Marsh Snake, for example, cape response by startling fish with their body before striking
forage for fish in shallow waters similarly to Acrochordus, them. During float-and-wait foraging, a snake assumes a po-
but in all circumstances where I have observed these snakes sition with the head end forming a J-shaped position and
capture their prey, the fish are grabbed by swift lateral the head forming the base of the J. The snake waits for a fish
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snake. The tentacles of these snakes are sensitive mechano-
receptors that respond to nearby movements in water (see
chapter 7). Vision also is important, but the tentacles pro-
vide additional sensory information that becomes increas-
ingly important when vision is diminished by nightfall or
turbid water.
Generally, the more commonly employed methods that
are used to capture and subdue prey include the following:
(1) biting and swallowing; (2) constriction; and (3) enven-
omation. Of course, the first method is always part of prey
capture at some stage of the process. Many snakes simply
grasp a prey item and swallow it. The examples of this be-
havior are far too numerous to mention, but primarily
these include snakes that feed on smaller ectothermic prey
such as insects or other invertebrates, eggs, carrion, and
small vertebrates such as frogs or lizards. Larger, swiftly
moving snakes such as racers and whipsnakes, indigo
snakes, and even some garter snakes, may capture endo-
thermic prey such as mice or smaller bird species by
grasping with the mouth and swallowing the prey directly.
I have watched captive Central American indigo snakes
(Blacktail Cribo, Drymarchon melanurus) chase full-grown
mice around in cages, simply grabbing each one with the
mouth and rapidly swallowing the animal while it kicked
and attempted to bite the snake. Once past the mouth,
muscular movements of the neck quickly moved the still-
live and wiggling mouse toward the stomach, and one
could still see movements of the mouse as it passed poste-
riorly within the esophagus. One after the other, the snake
would swiftly swallow each of several mice in rapid succes-
Figure 2.10. Schematic representation of a Tentacled Snake sion. Indigo snakes have a broad, generalist diet and prob-
(Erpeton tentaculatum) capturing a fish in water. When a fish ably capture many small animals in this manner as they
approaches the snake (upper drawing), the snake jerks part of its move through their habitat in the wild. What I am left to
neck (arrow) such that a segment of the body disturbs the water and wonder is how many cuts or scratches are inflicted on the
sends a compressional wave (arrow) toward the fish. This movement
snake’s internal soft parts as these live animals pass
disturbs the fish, which in turn moves its head to begin swimming
away from the snake (curved arrow). The snake anticipates the
through the snake’s mouth and esophagus! Of course
movement of the fish and rapidly captures the fish in its jaws (lower these ingested animals will suffocate rather quickly once
drawing). The strike of the snake (arrow) is guided by vision and by they are inside the gut.
water movements (especially at night). The scaled tentacles are And this brings us to a very important consideration. As
sensitive mechanoreceptors that respond to water movements. The snakes evolved feeding behaviors that included increasingly
stippled fish in the lower figure shows the original position of the fish
larger and dangerous prey (in the sense of inflicting serious
before it engages in the escape movement. Drawing by Dan Doursen
(after fig. 2 in K. C. Catania, Born knowing: Tentacled snakes innately damage to a snake in self-defense), there arose a dire need
predict future prey behavior, PLoS ONE 5:1–10, 2010). for parallel evolution of means to subdue such prey while
minimizing the possibility of harm. Also, remember the
snake is without limbs and must overcome larger animals
to approach, and when a fish is nearby—usually within the without the use of arms or legs—no easy feat if the prey is
concave region between the head and the snake’s body—the relatively large! There appear to be no measurements of
snake startles it with jerky movements of the body that ini- biting force in snakes, but observations suggest that indigo
tiate an escape response by the fish (fig. 2.10). The snake then snakes and some other species that neither constrict nor
strikes to capture the fish and adjusts the strike to the future envenomate their prey have strong jaws and can bite with
location of the fish as it moves rapidly in an escape trajectory considerable force. Ophiophagous snakes often kill their
that is judged quite accurately by the sensory system of the prey by using powerful jaws to hold and subdue them
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Figure 2.12. A Green Anaconda (Eunectes murinus) constricting a
turtle. Photographed in Hato el Cedro, Venezuela, by Jesús A. Rivas.
Figure 2.11. A King Cobra (Ophiophagus hannah) shown eating a

rat snake it has captured and subdued with strong biting prior to
ingestion. This snake was photographed in India by Dhiraj Bhaisare. subjected to inadequate oxygen or blood flow to the brain,
whereas ectothermic prey require less oxygen for lower
metabolic rates and also are more tolerant of oxygen defi-
(fig. 2.11). Clearly, there are limitations to this method of ciency at the brain. Snakes that are specialized for constric-
immobilizing prey considering the range of sizes and the tion have generally thick bodies and move relatively slowly.
dangers posed by various prey in comparison with the sole Perhaps in part because of these characters, envenomation
mouth of the predator. The problem of subduing potentially evolved as a very effective alternative means of subduing
harmful and larger prey was solved in a historical sense by large prey (see below).
the evolution of constriction or venom as a central part of
the prey acquisition process in different lineages of snakes Foraging Behaviors
(fig. 2.3). Generally, these two means of prey capture are ex- There are various means by which snakes seek out and cap-
clusive. That is, snakes that constrict their prey do not en- ture prey. So-called active foragers move through the envi-
venomate them, and vice versa. ronment searching for prey, which they attempt to capture
Constriction is an important means of subduing large or at the moment of encounter. There are many examples of
potentially harmful prey, prior to swallowing the item (fig. this behavior, and it is characteristic of probably most snake
2.12). Harry Greene and Gordon Burghardt—two herpetol- species—at least to some degree. Many natricine snakes pa-
ogists who are interested in natural history and behavior— trol the edges of streams or ponds seeking frogs, or some-
have emphasized this is a key behavioral innovation that times enter the water to hunt for fish. Sea snakes are fish
evolved during the early history of snakes. Constriction is specialists, and many species move slowly over coral reefs
characteristic of relatively more basal snakes, and has been probing holes and crevices for eels or other fish. Some probe
lost in many of the advanced snakes. If one thinks about it, bottom substrates in search of fish eggs. Various species that
constriction is a rather obvious means by which a limbless are called racers or whipsnakes move through terrestrial ter-
animal might subdue and kill prey, especially if the head is rain alert to the movements of lizards or other small verte-
relatively small. Earlier views supposed that the prey an- brates, striking or chasing them with rapid movements.
imal was crushed by the act of constriction, but it is now Similar behaviors characterize various species of elapids.
widely accepted that the coils that tighten about an animal Coral snakes and many other species search for, and follow,
either kill it or render it unconscious by means of suffoca- the scent trails of small animals using head movements and
tion or blockage of adequate blood flow to the brain. It is tongue flicking to locate chemical cues that are left behind
possible, of course, that some prey might be crushed faster by the recent movement of potential prey. Florida Cotton-
than they are suffocated when falling victim to large con- mouth snakes, Agkistrodon piscivorus conanti, are attracted to
strictors, but this might also depend on one’s subjective dead and rotting fish that are located by airborne chemical
definition of the word “crushed.” cues possibly from considerable distances (fig. 2.13).
Constriction is considered to be generally more effective Many snakes seek out particular microenvironments
in overcoming endothermic birds and mammals than it is where prey is likely to be concentrated. Examples include
for ectothermic prey. Perhaps this is because of the higher cobras, rat snakes, and other species with abilities to climb
metabolic rate of the former, which succumb quickly if trees, where they seek out bird nests. Florida Cottonmouth
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Figure 2.14. Unusual photographs of an Eastern Coachwhip
(Masticophis flagellum flagellum) foraging on hatchling Loggerhead
Sea Turtles (Caretta caretta) at St. Lucie Inlet State Park, Florida. The
upper photos show the snake with a hatchling in its mouth (inset)
while emerging from the beach sand in which the turtle eggs were
laid. The lower photo shows the snake’s body, which clearly reveals
the snake has swallowed several individual hatchlings. The arrow
indicates a point of peristalsis where body muscles were being used
to push the prey further along the gut. Photographs are courtesy of
Irene Arpayoglou.
Figure 2.13. Florida Cottonmouth snakes (Agkistrodon piscivorus

conanti) swallowing dead fish on which they forage beneath bird
beach and prey on hatchling sea turtles moving to the sea;
rookeries at the Gulf island of Seahorse Key. In the lower photo a
snake attempts to swallow a long-dead and dried toadfish.
they also ambush hatchlings by lying on the sand just above
Photographs by the author. the nest point where the tiny turtles emerge; and they poke
their head into the sand and capture hatchlings just before
emergence, or eggs before hatching. Similar behaviors have
snakes living on some Gulf islands forage beneath bird been observed recently involving an Eastern Coachwhip
rookeries where fishes are dropped or regurgitated by colo- (Masticophis flagellum) at a beach in Florida (fig. 2.14).
nial nesting sea birds (fig. 2.13). These same snakes, as well In contrast with active foragers, ambush foragers are
as various natricine, homalopsid, and acrochordid species, snakes that literally lie in ambush for prey, usually at loca-
are attracted to dried-down pools, or shallow waters that tions where unsuspecting animals are likely to appear. Var-
are created by low tides, where fishes are likely to be ious pit vipers, for example, coil in positions at the side of
concentrated during drought. Rattlesnakes, Bullsnakes, rat rodent trailways or at the base of trees or logs where small
snakes, and many other species seek rodent nests where mammals might pass. Studies in which the activity and
young as well as older occupants might be found. And many movements of snakes have been assessed usually employ
snakes in various taxa enter burrows, where they seek out radiotelemetry methods whereby an animal with an im-
prey items that might be hiding or living within. The elon- planted radio transmitter can be located using radio signals
gate body form of snakes enables them to be very effective that are picked up with a receiver (see fig. 4.5). Ambush for-
predators on burrow- or soil-dwelling animals (fig. 2.14). aging pit vipers have been noted to spend much of their
Akira Mori and his colleagues have documented an un- time at a single location without moving. For example,
usually interesting foraging behavior in the colubrid snake Harry Greene studied a bushmaster in Costa Rica that
Dinodon semicarinatum, which exploits the eggs and hatch- spent only 1 percent of alert time moving about during a
lings of sea turtles. These snakes actively crawl around the period of 35 days in which the snake rested for various
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times at three locations. This snake ate a meal on the 24th
night of observation.
Generally, the size of prey increases as the body size of a
snake increases during growth to adult size. It might seem
self-evident that snakes switch prey items as they grow
from very small babies to much larger adults, and these
changes are sometimes associated with alterations of for-
aging behaviors. Some of the better studied examples of
ontogenetic prey switching (changing prey with growth) are
various species of vipers and pit vipers, which may switch
from consuming largely ectothermic prey (e.g., lizards)
as juveniles to endothermic prey (e.g., small mammals) as
adults. The Common Death Adder, Acanthophis antarcticus
(an elapid species) also switches from ectothermic lizards
to small mammals when juvenile snakes grow to adulthood.
This is particularly interesting because this species of elapid
shares many characters in common with vipers as a result
of convergent evolution (fig. 1.42).
Shifts in prey type are also particularly evident in popu-
lations of snakes living on islands. For example, Australian
tiger snakes, Notechis spp., living on the mainland feed
principally on frogs, whereas conspecifics on islands con-
sume mostly mammals and birds. Insular water snakes
(Nerodia sipedon) and Cottonmouths (Agkistrodon pisci-
vorus) feed largely on fish, whereas conspecifics consume
more amphibians and other prey on the mainland. Most ex-
amples of such dietary differences reflect differences in the
prey that are available on an island versus mainland.
Figure 2.15. Many sea snakes are not inclined to bite when handled
Gape and Striking or in contact with humans. In the upper photo Micheal Guinea
Many persons are somewhat familiar with the striking behav- gently extracts a Yellow-lipped Sea Krait (Laticauda colubrina) from
limestone rocks on a small Pacific island. The snake is handled gently
ior of snakes, due in part to the tendency of filmmakers usu-
and does not attempt to bite. Photographed in Fiji by the author. The
ally to feature snakes that are engaged in defensive behaviors. lower photo features Julia Bonnet holding a Turtle-headed Sea
Indeed, while snakes might exhibit alternative defensive be- Snake (Emydocephalus annulatus) which gently accommodates to the
haviors, one is often greeted with biting or striking if he or contact. Photographed in Nouméa by Xavier Bonnet.
she approaches a wild snake and attempts to touch or handle
it against its will. These circumstances can vary a lot, however.
Many harmless snakes can, in fact, be handled without biting strikes can involve hissing, gaping of the mouth, and star-
if they are approached slowly and without aggressive move- tling but undirected movements intended to frighten off a
ments. Placid behaviors also characterize some venomous person or other animal without making actual contact or
snakes, although no one should ever make this assumption inflicting a bite. On the other hand, predatory strikes are
and handle a venomous snake with bare hands! This being more carefully executed and more accurately directed at an
said, there are a number of species of sea snakes that rarely or animal that is intended to be captured for a meal (fig. 2.16).
never bite in defense of being handled. I have watched chil- While these differences are well evident to persons who
dren at Suva Harbor in Fiji fearlessly playing with Yellow- have observed snakes carefully, the details and mechanisms
lipped Sea Kraits, Laticauda colubrina, which appear never to involved in the two categories of strikes have proven diffi-
inflict any harm to their exuberant captors (see also fig. 2.15). cult to demonstrate and to quantify.
We must distinguish two categories of striking by Predatory strikes that might be very carefully executed
snakes. A defensive strike is often more a display and may by a snake also may not be perfect. Strikes can be flawed in
not be directed at an intruder as accurately or rapidly as is a various ways, and in some studies David Cundall found that
predatory strike that is intended to capture prey. Defensive up to 47 percent of strikes by rattlesnakes result in neither
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Figure 2.16. A predatory strike executed by an
Amazon Tree Boa (Corallus hortulanus) in a
laboratory setting. The kinematic sequence of the
strike is illustrated with progression of photos from
top to bottom. In the upper photo the body of the
snake is drawn into several S-shaped loops in
preparation for striking the mouse, while vision
and thermal cues play key roles in aligning the
snake’s strike trajectory from the position of its
head to the mouse on the platform at the left. The
middle photo illustrates the “propulsive” force
produced by the muscle actions of the snake,
which creates an equal “reaction” force acting in
the opposite direction to accelerate the snake’s
head and forebody in the forward direction. The
reaction force is essentially equal to the force of
friction, which acts opposite to the propulsive
force and is dependent on both the mass (weight)
of the snake and the nature of the surface with
which it interacts. In the middle and lower
photos, note the gape of the snake’s mouth as its
lower jaws engage the mouse and the head moves
forward to bite forcefully and immobilize the prey.
The images are taken from a video sequence
produced by Phil Nicodemo.
fang penetrating the prey. The probability of missed fang The trailing behaviors of rattlesnakes and other viperid
contact or penetration increases with the distance of the species following envenomation of prey are even more
strike. This might explain why snakes are observed to strike complex and fascinating than one might suppose. Recent
only when prey animals come into very close range. studies by Eli Greenbaum, David Chiszar, and others have
Predatory behaviors that involve striking by snakes in- demonstrated that rattlesnakes and Copperheads can rec-
clude (1) visual, mechanical, or chemical location of prey, (2) ognize prey that is envenomated by conspecific animals and
preparation for the strike—usually by means of intense prefer it to non-envenomated prey. However, prey that is
sensory focus on the prey item and drawing the neck into envenomated by a distantly related species is not preferred
S-shaped curves, (3) rapidly extending the body during the over non-envenomated prey or prey that is envenomated by
strike, (4) grasping the prey item with the mouth upon con- another individual of the same species. The behavior of
tact, followed by either (5a) continuing to bite or grasp the sensing and trailing envenomated prey enables a snake to
prey while subduing it with constriction, envenomation, or distinguish an animal, say a mouse, from trails that are
biting force, or (5b) releasing envenomated prey and trail- made by other mice living in the vicinity. This leads the
ing it for later ingestion following its death or paralysis. snake to the animal that will succumb to the venom instead
Kenneth Kardong and others have shown that the trailing of wasting time and energy following other trails. An en-
behaviors of rattlesnakes (Crotalus spp.) following a strike venomated rodent can move considerable distances before
can be induced by the strike itself, after which the struck succumbing to venom, so anything that facilitates the task
prey is discriminated from others using a distinctive che- of finding the prey is likely to be adaptive. Thus, phylogeny,
mosensory profile during trailing. Subtle as it might seem, genetic differences between snake species, and the evolu-
the odor of the struck prey is changed by the fang penetration of venom composition might all interact in complex
tion and the injection of venom. Envenomation is the most but meaningful ways.
important factor contributing to the chemosensory “image” Observations of anatomy and analysis of filmed move-
of the prey following the strike. ments by Thomas Frazetta, Kenneth Kardong, David Cundall,
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and others have revealed some general similarities of striking take a wide range of prey. If the prey is a dead or small fish,
in pythons and in several species of vipers. Predatory strikes a frog, or even a baby mouse, the items are swallowed im-
are extremely rapid. The reaction times involved for the head mediately upon being bitten, whereas larger rodents are
and trunk muscles to activate or deactivate during striking struck and envenomated, then released to be followed and
movements are less than 15 msec, and possibly half that time. eaten later. This latter behavior appears to be a common
As a snake strikes, both mandibles are lowered and the pala- strategy among viperid snakes that prey on larger rodents
tomaxillary arches are moved upward while the head is rap- or small mammals that might inflict considerable harm if
idly accelerated toward the prey. The pterygoids move forward they are not immobilized. Another example of “bite and re-
with the ectopterygoids, raising the maxilla and pushing the lease” is the tactic employed by sea kraits (e.g., Laticauda
prefrontals forward. This flexes the snout and braincase up- colubrina) to envenomate dangerous fishes like moray eels
ward and tends to slant the teeth forward in a stabbing mo- while minimizing the probability of being harmed. These
tion. Movements of the head are considered to be important snakes search for moray eels by entering holes among
for erection of the fangs, while the mandibles are the first ele- corals, and if one is found the snake quickly bites and en-
ments to contact the prey. These movements are reversed as venomates the eel, then quickly withdraws and waits for
the jaws close, bringing the teeth-bearing bones closer and the venom to act. The snake reenters the hole somewhat
engaging the teeth in the prey. The lower jaw is thrust forward later to swallow the eel after it has succumbed to the venom.
during the strike and is retracted as the mouth closes. On the other hand, nonvenomous constrictors such as
The total duration of typical predatory strikes that boas and pythons necessarily retain a bite on their prey,
have been studied in viperid snakes varies from 150 to 500 which must be quickly enveloped and subdued with con-
ms, and the time between the beginning of a strike to stricting coils. Arboreal snakes that eat birds tend to bite
making contact with the prey is typically about 50 to 100 and hold because it would be difficult to follow the prey if it
ms. These times can vary as a function of the size of the was released. Finally, rear-fanged snakes (see below) tend
snake and its prey. One should always remember that to hold onto prey items that must be worked to the poste-
however slowly some of these snakes move during routine rior aspect of the open jaws in order to inject venom. These
movements and other nonfeeding behaviors, their strike snakes often bite with much force and may “chew” or close
can be lightning fast! hard on the prey for some while in order to effectively en-
In some crotaline snakes (e.g., Crotalus horridus), rotation venomate the prey (fig. 2.17).
of the prefrontal bone around its attachment to the frontal
bone elevates the snout and helps to elevate the fang base rel-
ative to the braincase during the extension phase of the strike
(fig. 2.5). Elevation of the prefrontal decreases the distance be-
tween the tip of the fang and the roof of the mouth, which
better enables each fang to be carried over the dorsal surface
of the prey before it impales the animal. The fangs are brought
down on the prey’s surface and often penetrate during the
contact or bite phase of the strike when the jaws are below
their maximum displaced positions. If the prey is released fol-
lowing envenomation, the maximum gape involving displace-
ments of both mandibles and the fangs is usually achieved
after envenomation when the prey is released.
In the case of venomous snakes, there is a tendency for
larger species possessing elongated fangs to envenomate
and quickly release the bite of the prey if it is large and po-
tentially dangerous. This is especially true for mammalian
prey that can struggle vigorously, bite, tug, and scratch. If
the prey item is relatively small or innocuous, however, the Figure 2.17. A Cat-eyed Snake (Leptodeira septentionalis) eating a
snake often maintains a grasp on the animal and holds it tree frog (Smilisca baudinii) in Belize. The frog inflates its lungs to
firmly in the mouth (before swallowing) until the prey enlarge the body in an effort to prevent being swallowed. The snake,
in turn, patiently “chews” on the frog to impale the posterior maxillary
ceases to struggle. Indeed, the biting tactics of snakes are
teeth, which function as fangs to envenomate the frog. The venom
dependent on the nature of their prey. eventually causes paralysis and deflation of the lung, so the frog can
Cottonmouths are an excellent example of striking vari- be pulled further into the mouth and eventually swallowed.
ability, insofar as these snakes have a generalist diet and Photograph by Dan Dourson.
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The striking and biting behaviors of snakes can be very movement attributable to propulsive forces (fig. 2.16) can be
different when we consider species that are adapted to for- provided by anchoring against irregularities in the substrate
aging in different media. Whereas various prey items on or by the inertia attributable to large mass, or both. Striking
terrestrial surfaces are generally struck head-on, fishes in performance might be assisted in large-bodied snakes such
water are often struck by lateral movements of the open as vipers through relatively large posterior mass, which
mouth. Studies of Cottonmouths have demonstrated that also increases the frictional resistance to movement. More
terrestrial strikes exhibit higher angular velocities during
closure of the mouth and higher angles of gape during the
retraction phase of a strike when the head pulls back from
the prey, compared with strikes when the snakes are in
water. Shawn Vincent and colleagues have demonstrated
that the success of strikes is considerably greater in terres-
trial situations than in water.
The size of the prey that can be swallowed depends, of
course, on the gape of the mouth, and this varies among
different taxa of snakes. Fundamentally, snakes exhibit
very large gape compared with other vertebrates owing to
several features of the jaws and skull (figs. 2.9, 2.18). The two
mandibles are fused by a rigid joint in most amniotes, but in
snakes the distal tips of the jaw are connected by ligaments
and can move independently of one another. Moreover,
each mandible can bow outward and adjust to the shape of
the prey owing to a joint at or near its center (where the
dentary meets the compound bone of the lower jaw) and to
the kinetic attachment of the quadrate, which connects the
lower jaw with the skull (figs. 2.5, 2.18). The muscles that
move the various skull and jaw elements are complexly
elongate, representing conditions that favor a large gape
and mobility of the teeth-bearing bones. The extreme gape
of snakes is perhaps best seen and appreciated when a snake
swallows a rigid-shelled egg of a bird (figs. 2.1, 2.19).
Vipers, in particular, exhibit morphological specializa-
tions that enhance the ability to capture and swallow rela-
tively large prey. These include a stout body, relatively large
head with elongate jaws, long fangs, and comparatively
small-size scales on the head that favor kinesis. The ante-
rior and posterior excursions of the palate and maxillary
bones in vipers exceed those that have been recorded for
any other major clade of snakes. Such movements are re-
lated to features of the floor of the braincase and its at-
tached constrictor muscles. The upper-jaw movements of
some rattlesnakes can exceed those in nonviperid snakes by
a factor of two. One measure of how these features trans-
late into swallowing performance and efficiency is that vi-
pers use fewer cycles of jaw movements than do colubrids Figure 2.18. Defensive displays illustrating the large gape of snakes.
to transport prey through the mouth, if the prey are equiv- The upper photo illustrates a Brown (or Mexican) Vine Snake
alent in terms of relative mass. (Oxybelis aeneus) with open mouth that is specialized for snaring
The mechanics of striking varies with the size and shape lizards or small birds. The middle and lower photos depict a
Neotropical Bird Snake (also called Puffing Snake) (Pseustes
of a snake. Two considerations are most important. First, ei-
poecilonotus) which displays a menacing mouth, showing the
ther high inertia or some amount of anchoring is required extreme width while the tips of the mandibles are separated. The
for snakes to avoid inaccurate or totally flawed strikes. Con- open glottis (entry to trachea) can be seen in the middle photo. Dan
sequently, on horizontal surfaces resistance to unwanted Dourson photographed these snakes in Belize.
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Figure 2.19. A sequence in which an Eastern Rat Snake (Pantherophis alleghaniensis) swallows a chicken egg. The rows of teeth in the lower
jaws can be seen at the margins of the mandible in the upper two photos. In the photograph at right-center, note the glottis is open and
protruded from the mouth (arrow) to enable breathing while the egg is in the mouth. Photographs by the author.
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answers to this question. In some cases, experimental ma-
nipulation of prey size during the growth of young snakes
does not result in any differences in growth of the
head skeleton, for example in the Boa Constrictor (Boa
constrictor). On the other hand, the jaw length of Australian
tiger snakes (Notechis spp.) living on islands is different
from conspecifics that live on the mainland, and the differ-
ence appears to be controlled both by genes and by the en-
vironment. Neonates of the insular tiger snakes have larger
heads than do counterparts living on the mainland, despite
similar body sizes. This geographic difference is apparent at
birth and presumably reflects genetic adaptation to dif-
ferent diets, the insular snakes feeding on relatively large
chicks of nesting birds and the mainland snakes feeding
mainly on frogs. Moreover, the relative size of the jaws of
insular snakes that feed on large prey (large mice) increases
during growth to become larger than those of siblings that
are fed on smaller prey (small mice). These tiger snakes ap-
pear to be highly adaptable predators that can track prey
resources by means of a complex response that involves ge-
netically “hard-wired” traits as well as developmental plas-
ticity of these traits.
The growth of head shape in Cottonmouths (Agkistrodon
piscivorus) is especially interesting. The size of prey gener-
ally increases with body size of Cottonmouths, as occurs in
other snakes generally, but shifts of prey type during on-
togeny have not been detected. Cottonmouths undergo a
Figure 2.20. A Grenada Bank Tree Boa (Corallus grenadensis) on the
developmental change in head shape, in which juveniles
island of Grenada, shown in a striking position while its body is tend to have relatively broader and higher, but shorter,
anchored on a tree branch. Note how the prehensile tail anchors the head shapes compared to adults. Relatively small head size
snake to a part of the tree branch. Photograph by Richard Sajdak. appears to characterize the adults, in which the gape scales
with negative allometry relative to body size according to a
recent study by Shawn Vincent and coworkers. That is, the
gracile species—for example, many arboreal snakes—can head becomes relatively smaller as the body grows larger.
also anchor by coiling a prehensile tail or part of the trunk The authors of this study suggest that the gape and head
around a branch or other object (figs. 1.31, 2.20). shape characteristics of Cottonmouths likely reflect the
David Cundall has suggested that the body form of generalist nature of their diet. My own studies of Florida
snakes has been adapted to optimize striking in relation to Cottonmouths on islands emphasizes that dietary breadth
momentum of the head and anterior body. The mass of the exhibited by these snakes increases the probability of en-
head is accelerated and increases momentum as it propels countering usable energy resources in situations where
toward the prey. If the momentum is too high, there will be these can be ephemeral, transitory, and variable in quality
a tendency for the head to continue beyond the point of and quantity. Specialization of diet or strongly selective for-
contact with the prey. This might explain why many snakes, aging behaviors could be disadvantageous in such environ-
especially vipers, have a reduced mass at the anterior trunk ments, whereas the acceptance of a range of prey increases
in addition to attributes of the head that increase shock- the foraging opportunities.
absorbing ability. These adjustments are especially impor-
tant for larger-size snakes. Generally, larger species exhibit
relatively greater mass and velocity of their heads. Teeth and Fangs
One question that has intrigued biologists and snake Teeth are very important for the capture and swallowing
specialists alike is whether a character such as predatory of prey by snakes. The dentition of the earliest reptiles is
gape is “plastic” and can be induced to change with an ex- poorly known, but appears to have consisted usually of
perimental change in the size of prey. There are mixed simple, conical teeth that correlated with a carnivorous or
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Figure 2.22. A Crayfish Snake (Regina rigida) swallowing a crayfish
in Florida. This species lives in swampy, low, wetland areas where it
specializes on eating crayfish. It has chisel-shaped teeth that help to
ingest this hard-shelled prey. However, these snakes have a
preference for crayfish that have recently molted and are therefore
relatively soft-bodied compared with animals in which the cuticle has
mineralized. Photograph by Joseph Pfaller.
xenopeltid) and at least five genera of colubrids that have

hinged teeth adapted for feeding on hard-bodied and nonde-
formable prey such as skinks. These lizards are covered with
stiff, strongly cycloid scales underlain by osteoderms. Such
armor poses dangers of breakage to long, sharp, and firmly
anchored teeth. Therefore, the teeth of these snakes are at-
Figure 2.21. A schematic image showing a pleurodont condition of
tooth attachment. The tooth does not have a “root” but is anchored by
tached to bone by flexible connective tissue fibers, and they
fibrous attachment largely to the inner (lingual or medial) wall of the fold backward against the jaws. The teeth are also modified
bone and within a groove of the bony element on which it is to be typically small, numerous, flattened at their ends, and
supported. Drawing by Dan Dourson. extremely smooth on their leading surfaces. There are also
other modifications of the head in these snakes, which, to-
gether with the teeth, enable them to grasp and to swallow
piscivorous (fish) diet. These evolved in snakes to become very hard prey. There are exceptions to these statements,
adapted for seizing prey. In most snakes the teeth are and numerous snakes swallow both soft- and hard-bodied
long, thin, sharp, and recurved—ideal for piercing and prey depending on the relative size (fig. 2.22).
grasping (figs. 2.5, 2.6). They are firmly anchored to the jaw
and are often set in deep grooves, but usually against a Replacement
higher “outer” (labial) than “inner” (lingual) wall (fig. 2.21). The dentition of snakes is not static, but rather the func-
This is known as a pleurodont condition of tooth attach- tional teeth are continually being replaced. Hence, new
ment, which is characteristic of lizards and snakes. The teeth take the place of older ones that are lost or damaged.
maxillary teeth are attached to the jawbone by mineral- The replacement process begins very early in life and con-
ized tissue, and the attachment morphology is known as tinues throughout the life of the animal. The organization
ankylosis. of teeth begins early in the embryo where precursors of
There are exceptions to this basic form. Highly special- teeth appear on bands of specialized epithelium. The ear-
ized tubular teeth evolved in elapid and viperid snakes to liest formed teeth are often reabsorbed at a rudimentary
deliver venom (figs. 2.5, 2.6). Teeth are reduced in both size stage of development. Subsequently, teeth form as new
and number in the egg-eating snakes, Dasypeltis and Elachis- buds, often in successive waves along the length of the jaw.
todon, so the eggshell is more easily enveloped by a mouth The teeth continue to grow until they become full size, at
having an interior that is very “fleshy.” And there are several which time they attach to bone and become functional. Af-
genera of snakes including the primitive genus Xenopeltis (a ter some time, the teeth begin to undergo reabsorption and
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are replaced, a process that is not depen-
dent on wear. The pattern of replacement
usually is such that the teeth undergoing
replacement are flanked by new, more or
less intact, teeth that develop at the
bases of the functional teeth and will
contribute the next generation. The re-
placement occurs in “waves” except in
some taxa.
Visible evidence of the replacement
process for teeth is the common occur-
rence of one or more smaller “replace-
ment” fangs just behind the functional
fang of a viperid snake (fig. 2.5). The
paired fangs are replaced alternately, and
the new fang becomes anchored and con-
nected to the venom duct before the
functional fang is shed. Such shed fangs
are frequently found undigested in the
feces of these snakes! Hmm . . . Certain Figure 2.23. Palatal view of the skull and medial profiles of the mandibles of a
Reticulated Python (Broghammerus reticularis) illustrating the teeth-bearing bones.
enterprising persons might not have re-
The outermost elements in the photograph (dentary) represent the lower jaw, which
alized they could use this as a renewable articulates with the upper jaw shown in the center. Note that some replacement teeth
source of fangs to be used for jewelry, can be seen at the end of the lower dentary. Photograph by Elliott Jacobson; skull
rather than killing snakes for their fangs. courtesy of the Florida Museum of Natural History.
Patterns of Dentition
The primitive pattern of teeth in snakes evidently consisted have a limited number of teeth on the maxilla and den-
of a single row of sharp, conical teeth numerously distrib- tary, none on the premaxilla, and rarely on the palate.
uted on the premaxilla, maxilla, dentary, pterygoid, and pal- Boas and pythons, on the other hand, have a moderately
atine bones. This pattern of distribution is observed in large number of teeth on all of the usual teeth-bearing
living pythons (fig. 2.23). It has generally been conserved, bones (fig. 2.23). The teeth are usually long, recurved, and
except for the evolution of long, recurved teeth, reductions lacking compression. In various more derived lineages,
or expansions of tooth number, and the development of the maxillary teeth become regionally enlarged, anteriorly
grooved or tubular fangs on the maxilla in various lineages or posteriorly, either as part of a continuous series of
of snakes (figs. 2.5, 2.6). teeth or with gaps in dentition where teeth are absent.
In the majority of living snakes the premaxilla is reduced The enlarged teeth are solid, grooved, or tubular in various
and without teeth, except in boas and pythons. Teeth have groups of snakes (figs. 2.5, 2.6).
persisted on the pterygoid and palatine bones (palate), but Colubrid snakes have undergone extensive adaptive
are reduced in size or number in certain colubrid species. radiations, reflected in part by variation of dentitions. All
Teeth are present on the dentary in most snakes, but they colubrids lack teeth on the premaxilla, but there are usu-
may be absent, reduced in number, or limited to the ante- ally well-developed teeth on the dentary and in a long row
rior part of this element in some taxa. on the palatine and pterygoid. The maxillary teeth are
The structure and dentition of the maxilla is very im- rather uniform and form a fairly long row of simple con-
portant in snakes, and maxillary characters have been ical structures. Elapid snakes vary in the arrangement of
very useful for interpreting phylogeny. In the more basal dentition on the maxilla, some having a series of teeth
snakes, the maxilla bears rather simple and uniformly that become reduced in size posteriorly (front to rear),
shaped teeth. In scolecophidians, the dentition is special- whereas others exhibit well-developed tubular fangs on a
ized in relation to the burrowing habits of these animals. greatly abbreviated maxilla. In mambas (Dendroaspis),
In Typhlops, the maxillary teeth are small, slightly com- the maxilla usually bears but a single prominent fang,
pressed, simple cones, and there are no teeth on the den- and there is an enlarged tooth on the anterior end of the
tary. The maxilla of Leptotyphlops is without teeth, and the dentary (fig. 2.6). The elongated fangs and anterior teeth
dentary bears only a few small teeth. Uropeltid snakes of mambas are likely to be adaptations for securing prey
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without dropping it, insofar as these snakes are arboreal.
In vipers and pit vipers, the maxilla is highly specialized
as a reduced bone that is short and hinged, bearing an
elongate fang that rotates with movement of the element
(fig. 2.5).
Feeding on slugs and snails (malacophagy) has arisen in-
dependently in several lineages of colubroid snakes, most
notably the Asian pareatids and the neotropical dipsadines
and xenodontines (fig. 2.8). Long, slender teeth tend to be
typical on the anterior dentary and posterior maxilla of
malacophagous snakes and are hypothesized to be speciali-
zations for gripping the slippery, mucus-covered skin of the
prey. However, Eric Britt and his colleagues could not dem-
onstrate such features in certain garter snakes (Thamnophis
spp.) when their teeth were compared with congeneric spe-
cies having different dietary preferences. Numerous teeth
that are narrow and prominently recurved tend to be char-
acteristic of fish specialists, which often have elongated
jaws (figs. 2.9, 2.24).
Examples of greatly reduced dentition include the colu-
brid egg-eating snakes, Dasypeltis, and the elapid sea snake
Emydocephalus. Dasypeltis has at most four or five very
small curved teeth on the maxilla, three or four teeth on the
palatine, and another three at the extreme rear of the den-
tary. The reduction of teeth is associated with the habit of
eating eggs, which have relatively flat and hard surfaces
(figs. 2.1, 2.19). Sea snakes belonging to the genus Emydo-
cephalus are specialized for feeding on fish eggs and also ex- Figure 2.24. Prof. Mahmood Sasa and Jazmín Arias, University of
hibit extreme reduction of teeth. The dentary and palate Costa Rica, extract venom from the fang of a Yellow-bellied Sea Snake
(Pelamis platurus). Note in the lower photograph how the teeth are
both lack teeth, and the maxilla bears no teeth except for
elongated and recurved for snaring fishes, and the fang is equivalent
the fangs. in size to other teeth on the maxilla. Clear venom can be seen in the
upper part of a capillary tube that covers the left fang of the snake.
Fangs Photographs by Coleman Sheehy III (upper) and Philipp Figueroa
Fangs evolved to inject venom into the prey of various (lower).
snakes that possess them. The term fang refers to a grooved
or tubular tooth that is used to inject venom, although nu-
merous teeth could well serve the same purpose in species tubular fang. When the fang is not erected, it folds against
in which the fangs are small and venom secretions are dis- the roof of the mouth. Snakes with such fangs include the
persed during chewing actions on the prey. Fangs are func- viperid and atractaspidine species. In the viperids, the tips
tionally best developed in representatives of the Elapidae of the fangs are directed toward the prey during striking
(e.g., cobras) and Viperidae (e.g., rattlesnakes) (figs. 2.5, and effectively “spear” it, rather than biting prey in a down-
2.6). The fangs of viperids are the largest and most effective ward movement. Unlike the viperids, stiletto snakes (Atrac-
structures that have evolved in nature for injecting venom taspis) envenomate prey by moving a fang sideward out of
(fig. 2.25). one side of a closed mouth and slashing it sideways or back-
Snakes that possess completely tubular fangs are reward into the prey. The fang movements are very agile and
ferred to collectively as solenoglyphs. During development, considered to be adaptations for envenomating prey that
these fangs begin as conical teeth with a pulp cavity. As they are encountered inside earthen burrows. These fangs are
develop, one wall of the tooth pushes inward and the side relatively long and associated with a relatively short max-
walls grow over it to form a tube. Each fang is erected by illa. Other species of atractaspidine snakes curiously ex-
rotation of a reduced maxilla on the prefrontal bone (fig. hibit every known type of fang dentition, some having
2.5). The maxilla bears no teeth other than the hollow, fangs resembling those of elapids and others having
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grooved posterior fangs. One species
(Aparallactus modestus) appears to lack
grooved fangs altogether (aglyphous con-
dition) and may not produce venom.
The fangs of viperid snakes are excep-
tionally long, hollow teeth that rotate
through extremely large angles due to
mobile connections between the upper
jaws and the braincase. Recent analysis
of video records by David Cundall indi-
cate that vipers representing 86 species
in 31 genera reposition fangs after they
contact the prey in more than a third of
750 recorded strikes. A snake may repo-
sition a fang when it misses the prey en-
tirely, or when it initially contacts prey
regions that do not permit adequate
penetration. Repositioning is prevalent
even in species that normally release
prey following a strike. The rapidity of
fang repositioning suggests there is ex-
traordinary development and sensitivity
of the neuromuscular system that con-
trols the fang movement, including sen-
sitive detection of fang penetration and
very rapid modulation of antagonistic
muscle contractions.
Elapid snakes possess single, hollow, Figure 2.25. Freeze-dried heads of viperid snakes illustrating fang erection and gape
in three species: top, Southern Pacific Rattlesnake (Crotalus oreganus helleri); center,
or grooved fangs at the anterior end of
Rhinoceros Viper (Bitis nasicornis); bottom, Gaboon Adder (Bitis gabonica). There is a
each maxilla, which is relatively long (fig. fleshy sheath that covers each fang, normally folded flat against the roof of the mouth
2.6). Each fang is fixed and does not fold when not erected. The Gaboon Adder has the largest relative fang size of any species of
back because of the relative immobility snake. Photographs are of freeze-dried heads and taken by the author.
of the maxillary unit. This condition is
known as proteroglyph. In many species
the fangs of elapids are relatively short, Venom
sometimes hardly distinguishable from the other teeth (fig. One cannot adequately consider the mechanisms and strat-
2.24). If one looks inside the mouth of many elapid snakes egies of feeding in snakes without discussing the subject of
(not recommended), it is difficult to imagine the snake is venom. Venom is a term that is used to describe some form
dangerous in comparison with the appearance of fangs in of potentially toxic secretion produced by one organism to
viperid species. In Australian death adders (Acanthophis the detriment of another. The secretion is delivered to an-
spp.), however, the fangs are quite long and represent one other animal through some form of specialized structure—
of the morphological characters of these snakes that are in the case of snakes, a fang. Venoms are often confused or
convergent with those of viperids. categorized with poisons, but the latter must be ingested to
Various colubroid snakes possess posterior maxillary alter the physiology of the consuming organism. The princi-
teeth that are enlarged or grooved to function as fangs. In pal difference between venom and poison is that venomous
Boiga, for example, the maxilla bears a pair of alternately animals actively deliver their toxic secretions (through a
functioning fangs, preceded by a series of relatively small fang or stinger), whereas poisonous animals generally rely
and simple anterior teeth. In this and other opisthogly- on passive means of afflicting another organism.
phous colubrids, there may be a few small teeth behind the Venoms also should not be confused with toxins. These
fangs and a gap between the fangs and the more anterior are chemicals of biological origin that can adversely alter
teeth. the physiology of an organism. Toxins are pure substances,
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whereas venoms are mixtures of biologically active and diverse, and they vary among taxonomic group, ecology,
inert substances. Both venoms and poisons generally con- diet, population, and even within individuals. Some of the
tain toxins. The oral secretions of snakes that contain important components of venom follow.
toxins and are used to immobilize prey are considered to
be venoms. There is debate, however, concerning whether • Proteolytic enzymes (proteases) are components of venom
similar oral secretions that are not known to have an eco- that degrade structural proteins into component
logical role should be considered venoms. Recent publica- peptides or amino acids, often leading to damage in the
tions have championed the view that all oral secretions walls of blood vessels. They are involved in the tissue
having biologically active compounds and arising in spe- destruction that is present in necrosis, and many have
cialized glands should be considered venoms. There is important actions on blood coagulation. They are found
little question that many snake species that are now con- in the venoms of all known venomous species, and the
sidered to be “harmless” may eventually prove to have concentrations are particularly high in the venoms of
venom. A tragic instance of such reclassification occurred viperid snakes.
when Dr. Karl P. Schmidt of the Field Museum of Natural • Hyaluronidases are commonly called “spreading factors”
History in Chicago was killed from the bite of a Booms- because they degrade hyaluronic acid, which is a ubiquitous
lang (Dispholidus typus), which previously had been con- component of the extracellular matrix of tissues and helps
sidered to be harmless. to cement cells together. When hyaluronic acid is degraded
Snake venoms occur only within the families of snakes by hyaluronidase, the remaining venom components are
comprising the Colubroidea. Thus, it is generally held more easily spread throughout tissues, including blood
that venom arose in the ancestor(s) of this clade and vessels that are rendered to be “leaky.” This enzyme is
subsequently underwent modifications in composition, common in most snake venoms.
glandular morphology, and tooth shape as the basal • Phospholipases hydrolyze phospholipids, which are im-
snakes of this group radiated and speciated. However, portant components of cell membranes. These can weaken
venoms are found in multiple lizard families, and per- cell walls and lead to numerous physiological effects
haps only the type of modified venom apparatus, and including edema and damage to muscle. These enzymes
not venom itself, is of unique origin in the Colubroidea. are found in nearly all snake venoms.
Bryan Fry, an Australian venom specialist, has suggested • Acetylcholinesterase is an enzyme that hydrolyzes
that venom had an earlier reptilian origin than was pre- acetylcholine, a chemical that is important for mediating
viously supposed. the transmission of nerve signals. This enzyme is a
Generally, snake venoms consist largely of soluble poly- common component of elapid snake venoms and
peptides in water, but may also include carbohydrates, contributes to the neurotoxic actions of those venoms.
lipids, metal ions, and other organic compounds such as • Toxins are proteins of variable molecular weight, but
amines. Polypeptides comprise about 90 percent of the dry generally smaller than that of enzymes. They are highly
weight of most venoms, and many of these have enzymatic variable in structure and function, but most affect the
activity. Enzymes vary in their specificity and have catalytic nervous system by altering the transmission of nerve
properties that induce biochemical transformations with- signals at the neuromuscular junction. The venoms of
out themselves being modified. Various components of elapid snakes are particularly rich in toxins.
venom affect a wide range of physiological functions. The • Nerve growth factors are proteins that stimulate growth
numerous actions of venoms include effects on cells and of nerve cells and are found in elapid and viperid venoms.
cell membranes, transmission of nervous signals, muscular The actions and biological function of these components
contraction, blood pressure, blood components and coagu- of snake venom are not well understood.
lation, inflammation, and necrosis. • Disintegrins are peptides found in viperid venoms, and
Historically, venoms have been considered to be either they act to inhibit integrins. These are proteins in
hemotoxic, affecting the blood, or neurotoxic, affecting the membranes that transfer messages across cell mem-
nervous system. However, these terms do not adequately branes to the intracellular cytoplasm.
describe the variation and complexity of venom, and spe- • A large variety of other factors display a range of actions,
cific venoms may contain compounds that produce both including inhibition or activation of enzymes, vasodilation
effects. Although the potency of venoms varies, recent of blood vessels, destruction of cells and receptor sites,
studies (e.g., Susanta Pahari, Stephen Mackessy, and lowering of blood pressure, and cessation of breathing.
Manjunatha Kini) suggest that there is greater composi-
tional similarity among advanced snakes than has been The efficacy of venoms and the diversity of their phar-
previously recognized. The many effects of venom are macological properties have fascinated humans since the
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Figure 2.26. A snake shop in Taiwan where the proprietor and a cobra entertain people who visit and purchase snake products that are sold
for various supposed health benefits. A live Chinese Cobra (Naja atra) is displayed on the table next to jars containing snake parts and fluids.
To the left one can see two snakes that are suspended while blood is being drained from a cut tail. The photo to the lower right features other
snakes—rat snakes and a cobra—that are having their skin removed. The skin of each snake, as well as other internal organs, is used for
commercial products. Photographs by the author.
time of Aristotle, and the ancients developed many snake and specialized teeth that are used for delivery of the
products—including venom, blood, and viscera—that were venom (fig. 2.27). The evolutionary origin of venom pre-
used in various medical remedies of the time. Some of these sumably involved a co-opted salivary gland, modifications
practices are still thriving in parts of Asia, and treatments of teeth, and natural selection for improved abilities to cap-
using snake venom are still an important part of mystical ture and subdue prey. Most evidence suggests that venoms
healing and folklore (fig. 2.26). Today components of snake are most important for aiding the capture of prey, although
venoms are used in basic research, pharmacology, diagnos- other uses of venom include defense and the possible en-
tics, and therapeutics. Venom properties have enabled sci- hancement of digestion. Indeed, it is conceivable that a di-
entists to achieve numerous advances in medical diagnosis gestive function could have led to increasing toxicity of
and treatment related to hypertension, vascular disease, salivary secretions that secondarily became effective in
muscular dystrophy, cancer, hemorrhage, congenital neu- capturing prey.
ropathies, and many other disease states. They have also Venom injected into prey reduces the time that a snake
contributed useful applications for such things as surgical is in contact with something that is alive, either because the
sutures and enhancement of drug delivery. The famous bi- animal is struck, released, and followed later to its point of
ologists James Watson and Francis Crick used nucleotidase death, or because the envenomated animal ceases strug-
enzymes from cobra venom to help elucidate the structure gling while being held in the snake’s mouth. The reduction
of the DNA molecule. of contact time with living prey is important because strug-
gling and biting prey can be injurious or even lethal to a
Venom Delivery Systems hungry snake. A reduction of prey handling time reduces
The production and effective use of venom depends on the the energy involved in subduing the prey and significantly
venom delivery system, which consists of the venom itself, decreases the potential for injury to the snake. This is al-
an associated gland that produces and stores the venom, most certainly the reason that so many snake venoms are
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ejected through the compressive action
of an adductor muscle that extends from
the parietal bone around the posterior end
of the gland to the corner of the mouth.
The venom (or Duvernoy’s) gland of col-
ubrids, when present, is relatively small in
most species and located posteriorly and
ventrally to the eye. This gland is somewhat
oval, laterally compressed, and considered
to be the ancestral state of the Colubroidea.
In Boiga irregularis (one of the few colubrid
species in which the venom gland has been
examined), the gland is multilobed with
secondary branching within each lobe. The
Duvernoy’s gland contains either purely se-
rous cells or a mixture of serous and mu-
cosal cells in different species. There is a
small central cistern analogous to the lu-
men of other venom glands, but is gener-
ally greatly reduced in comparison. A single
Figure 2.27. Schematic illustration of the venom delivery apparatus in a viperid
primary duct empties the central cistern
snake. The upper drawing is an enlargement featuring details of the venom gland and into the oral epithelium near the corner of
ducts, shown in association with the skull and fang in the lower drawing. Drawings the mouth. Usually there are no compressor
by Dan Dourson, after fig. 13.36 in K. V. Kardong, Vertebrates: Comparative Anatomy, muscles associated with the gland.
Function, Evolution, 4th ed. (McGraw-Hill, 2006). Elapid snakes possess an oval-shaped
serous gland that is associated with a mu-
cous-secreting accessory gland. The main
very potent: they have evolved to paralyze or kill prey gland is located ventrally and posterior to
quickly, and the potential harm to humans who might be the eye and is composed of tubules with simple or complex
bitten by a snake acting defensively is a secondary factor in branching patterns. These tubules empty into a narrow
relation to the evolution of venom properties. The more lumen that is surrounded by the accessory gland. Venom is
dangerous the prey item of a snake, the more likely the ten- discharged to the anterior fangs after passing through the
dency for the snake to strike and envenomate the animal, accessory gland, powered by muscular compression of the
release it, and consume it later after it has died. Some spe- dorsal and ventral aspects of the gland. It appears that in
cies have a demonstrated capacity to track envenomated elapid species of snakes the venom is stored mostly within
prey by sensing and following trails that bear chemical cues cells, rather than in the lumen of the gland.
related to the unique chemical signatures of the venom. The viperid venom gland is the most intensely studied
Since the origin of a rudimentary venom gland, the mor- and appears to have a rather consistent morphology (fig.
phology of the gland has been altered in different lineages. 2.27). The gland is large, triangular in profile, and divided
Generally, differences in the morphology of venom glands into several lobules by folds in the surrounding tissue. There
can be categorized in four general types: (1) the atractaspi- is a large lumen that is fed by multiple, complexly branched
dine type; (2) the colubrid type, historically referred to as tubules. The lumen connects by means of a primary duct to a
Duvernoy’s gland; (3) the elapid type; and (4) the viperid mucosal accessory gland, which in turn leads to a secondary
type. The more consistent gland structures are found in the duct that empties into large, tubular fangs at the anterior
Elapidae and Viperidae, whereas there is more variation in end of the mouth. The viperid venom gland stores large
the atractaspidine and colubrid species. quantities of venom, which are ejected by a complex pattern
The atractaspidine type of venom gland generally is large, of muscle sometimes referred to as the compressor glandulae.
tubular, and elongated posteriorly behind the eye (extending Venoms that are produced by the various glands are de-
beyond the head in some species). These glands consist of livered to prey by means of specialized teeth that aid in rup-
largely unbranched tubules radiating from a central lumen. turing of the skin and/or conducting the venom by means
The terminal duct of the gland typically empties venom into of dental grooves or canals. These include (1) aglyphous
anterior, tubular fangs, and venom appears to be forcibly (small, ungrooved) teeth throughout the oral cavity (many
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Figure 2.29. Jets of venom being “spat” by an Indochinese Spitting
Cobra (Naja siamensis). The venom can be rapidly expelled from the
fangs and aimed at the eyes of a threatening animal at distances up
to about 3 meters. Photograph by Guido Westhoff.
Figure 2.28. A young Florida Cottonmouth (Agkistrodon piscivorus
conanti) gaping its mouth in a defensive display. The common name
is attributed to the white appearance of the fleshy mouth that is it can keep its adversary at bay without contacting it. This
shown during these defensive gaping behaviors. Photographed in is the reason that snakes have evolved concealing colora-
Florida by Dan Dourson. tion or behaviors, and stereotyped threatening displays
such as inflating the neck, hissing, or gaping the mouth
(fig. 2.28). Unfortunately, humans sometimes misinter-
colubrids); (2) opisthoglyphous (grooved) teeth located in pret these displays as aggressive actions or attacks be-
the dorsal, posterior aspect of the mouth (many colubrids cause they can be frightening. Chances are, however, the
and some atractaspidines); (3) proteroglyphous fangs fixed to snake prefers simply to be left alone rather than to strike
the anterior maxilla (all elapids and some atractaspidines); or bite.
and (4) large, rotating solenoglyphous fangs located on the Spitting venom is a highly specialized behavior that has
anterior maxilla (viperids and some atractaspidines). evolved multiple times in species of African and Asiatic co-
The various venom delivery systems represent a progres- bras. The term “spitting” refers to the expulsion of venom
sion from simpler teeth and less specialized venom delivery as a pressurized horizontal stream, usually aimed at the
to more specialized fangs and venom glands that are ca- eyes of a harasser or predator (fig. 2.29). Some cobras can
pable of delivering large volumes of highly toxic venom in spit venom as far as 3 meters and can “aim” the spit quite
species of snakes that feed on larger and more dangerous accurately. During spitting, muscle contractions rotate the
prey. The latter are capable of inflicting considerable damage maxilla and elevate the palatomaxillary arch, which moves
to envenomated prey, and to potential predators! the fang sheath dorsally and removes a physical barrier of
An interesting problem is how the venom gland can syn- soft tissues to the expulsion of venom. Simultaneously,
thesize and store a suite of toxins that can be mobilized al- contraction of muscles associated with the venom gland in-
most instantaneously to subdue prey, yet can be stored creases pressure on the venom within the gland and forces
without the components of venom harming the snake or de- the venom through the venom duct and fang. The elevated
stroying each other. Several mechanisms are protective during venom pressure propels the venom as an airborne stream
storage, including acidic pH of the venom and the presence of beyond the orifice of the fang, but only after physical dis-
components that inhibit enzymatic activity during storage of placement of the fang sheath allows venom to flow through
the toxins. However, the toxins are activated spontaneously the fang. The fang opening of a spitting cobra has a more
upon their being injected into prey. Venom glands are struc- circular aperture than does that of nonspitting cobras,
turally complex, and the accessory gland might be a site where which assists the venom stream to exit forward rather than
venom components are activated. downward (fig. 2.29).
Spitting Venom The Allocation of Venom

Venom is used defensively during bites inflicted when a The amount of venom that a snake injects into a target (or
venomous snake defends itself and bites an attacker or spits at a target) can vary with the size of a snake, whether
threatening animal. Even better for the snake, however, if the situation is defensive or predatory, the size and nature
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of the target, and a variety of other factors. There is dis- of the venom. The manner in which venoms evolve differ-
agreement regarding whether snakes have the ability to ences has been debated, and clearly venom composition can
control, or “meter,” the expenditure of venom, or whether be influenced by different modes of evolution including
the expenditure of venom is related more to the nature of natural selection, patterns of gene flow, and genetic drift.
a “strike” and the features of the surface of the target. In some cases it has been proposed that some variation of
There appears to be rather good evidence supporting the venom composition might simply have no adaptive value.
abilities of snakes to meter the quantity of venom they ex- The toxin components of snake venom evolve with rela-
pel. William Hayes and colleagues have demonstrated that tive rapidity, and this is usually viewed as an adaptation
spitting cobras, for example, expend larger quantities of related to feeding. However, molecular research indicates
venom during biting than during spitting, related to a ca- that proteins of opossums that counteract the effects of
pacity for regulating the contraction of the venom gland snake venom have evolved rapidly in species of this mammal
according to the context. It seems likely that such regula- that eat venomous snakes. This suggests that venom has a
tion is widespread in snakes and that selection favors be- defensive role as well as one related to prey capture. Recent
havioral or physiological mechanisms that expel the data published by researchers associated with the American
appropriate amount of venom depending on the target Museum of Natural History now support the hypothesis
and the context. that there is a biochemical “arms race” between venomous
animals and their prey.
Factors Affecting the Variation and Evolution of Venom The variability in the biochemical composition of venom
The variability of snake venoms is widely known and has can, of course, alter the immunological sites that are recog-
been reported since antiquity, based on the observations nized by antibodies that are used in the treatment of snake-
of snakebite victims and confirmed more recently using bite. Thus, the effectiveness of a given antivenin might vary
molecular and immunological techniques. Research has depending on the geographic location where a particular
demonstrated there is much variation in venom composi- snakebite occurred. Further, the random mixing of venoms
tion and toxicity at multiple taxonomic levels and within a that are obtained from different populations of snakes has
single species. There are important variations in venom been found to be an insufficient solution to the problem.
within a population—even within a small group of related Envenomation of humans by snakes continues to be a glo-
individuals. In some snake species certain components bal problem, especially in developing tropical countries of
have been found in individuals of one sex but not the Africa, Asia, and Latin America. However, the actual
other. There is usually stability of various components frequencies of snakebite and their severity throughout the
throughout the age of an individual, but some studies have world remain largely unknown.
shown there are changes in venom properties during
aging. For example, the venom of juvenile Bothrops jara-
raca was shown to have a higher toxicity for frogs than that Digestion
of adults, and this difference correlates with the diet of
young snakes including frogs and lizards, which are not Gut Structure and Function
eaten by the adults. It has also been noted that certain Digestion refers to the mechanical and chemical breakdown
proteins appear, disappear, or become modified during the of food prior to the absorption of the resulting nutrients
life span of an individual snake. for further modification and distribution to the body. The
In many cases the reasons for variation in the chemical organ that functions in the digestion of food is called the
components of venom are not well understood, and there is digestive tract, alimentary canal, gastrointestinal tract, or
tremendous variation that needs to be explained. However, simply gut (fig. 2.2). The digestive tract of snakes is funda-
in well-studied examples the properties of venom have mentally similar in its anatomical features to that of other
been shown to correlate with variation in the local diet, ge- vertebrates. The food is passed (transported) from the
netic relatedness, and geographic location (including ge- mouth through the esophagus, which connects the throat,
netic drift related to random mutations following the or pharynx, with the stomach. The prey item is transported
isolation of snake populations on islands). In one case it through the esophagus by muscular contractions involving
was shown by Jenny Daltry and coworkers that variation in the trunk muscles of the neck, which “push” the prey into
the composition of venom in different populations of the the stomach (fig. 2.30). Salivary secretions from the mouth
Malayan Pit Viper (Calloselasma rhodostoma) correlated and mucous secretions in the esophagus lubricate the prey
strongly with the nutritional status of the population. and help it to “slide” through the esophagus in front of the
These results suggest that the availability of certain prey wave of muscle contraction. From the stomach food passes
species could exert selection pressures on the composition through the small intestine to the large intestine, and
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Figure 2.31. A partially digested rat as it was found in the stomach
of a juvenile Mexican Boa Constrictor (Boa constrictor). The digestion
of the animal is in its very early stages. The upper photo and the
inset in the lower photo illustrate the size of the rat in relation to
that of the snake, internalized and externalized respectively. This
snake was found freshly dead from unknown causes in Puerto Angel,
Mexico. Photographs by Coleman Sheehy III.
the action of digestive enzymes and thereby enhancing the

efficiency of the process. Because prey items are swallowed
whole by snakes, digestion generally takes longer than it
does in humans or many other mammals depending on the
exact nature of the food (fig. 2.31). The injection of venom
Figure 2.30. A sequence wherein an Eastern Rat Snake into animals that fall prey to venomous snakes introduces a
(Pantherophis alleghaniensis) moves an egg through its neck toward cocktail of enzymes to the internal body, where they are dis-
the stomach. Contraction of the body muscles create a wave where tributed by “spreading factors” of venom and blood circula-
first the left side of the neck pushes against the egg (upper photo),
tion. Thus, some herpetologists speculate that enhancement
followed by the right side of the neck pushing against the egg
(middle photo). Photographs by the author. of digestion might have been one of the early factors in nat-
ural selection that helped to promote the evolution of venom
and venom delivery systems. Recent studies by Marshall Mc-
finally to the cloaca, where the feces are formed and evacu- Cue have shown, however, that injection of venom into mice
ated from the animal via the cloacal opening. that are fed to rattlesnakes does not speed up or facilitate
Generally, snakes swallow their prey entire and do not their digestion. Thus, some persons may well doubt that
chew or otherwise tear and break the items into smaller venom facilitates the breakdown and digestion of food.
pieces. Therefore, when the prey reaches the stomach where
chemical digestion begins, the digestive enzymes must act Stomach
on the prey from the outside to in. As humans, we appreciate The swallowed prey item passes from the esophagus into
our parents’ advice to “chew our food” so that it is broken the stomach, which is the first (or most anterior) expanded
into smaller pieces, thereby increasing the surface area for part of the digestive tract. Its walls are highly distensible,
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and its expanded size helps to accommodate large food stomach and partly within the esophagus rather than en-
items during the initial period of digestion (figs. 2.31, 2.32). tering the intestine (fig. 2.33). Of the two compartments,
In cases where multiple, very large, or especially long prey however, only the stomach has capacity for digestion. When
such as fish are eaten by a snake, the swallowed items the stomach is not distended with food, its wall relaxes into
are accommodated only partly within a greatly stretched folds called rugae—something after the manner of an ac-
cordion. These folds, as well as generally thickened tissue
relative to the esophagus, help to delineate the stomach
portion of the digestive tract (fig. 2.34).
The epithelium lining the inner wall of the stomach is
glandular and characterized by the presence of gastric
glands (gastric refers to stomach). Various of these gastric
glands secrete mucus, hydrochloric acid, or proteolytic en-
zymes. The enzymes digest the food with aid from the acid
medium. The food eventually becomes a liquefied and par-
tially digested soup-like slur (called chyme or digesta) before
entering the intestine. The lowermost part of the stomach
that meets the intestine is called the pylorus, and the entry
of chyme into the intestine is regulated by a pyloric valve.
The gastric pH that is maintained during digestion
ranges from 1.5 to 4 in several species of snakes that have
been studied. Unlike mammals, which maintain an acidic
stomach environment between meals, after food leaves the
Figure 2.32. A Timber Rattlesnake (Crotalus horridus) rests while
stomach of snakes the pH increases to around 7 to 7.5. The
engorged with a recently ingested small mammal (likely a squirrel,
chipmunk, or rat). The prey item has greatly distended the stomach
duration of gastric acid and enzyme production is a func-
and surrounding body wall. This snake was photographed in Arkansas tion of body temperature and both the size and composi-
by Steven Beaupre. tion of a meal. The duration of gastric pH and enzyme
Figure 2.33. A neonate Florida Cottonmouth (Agkistrodon piscivorus conanti) has cannibalized a littermate of approximately the same size.
The ingested littermate has been curled back on itself, and the stomach of the predatory snake has been stretched exceptionally thin to
accommodate the meal. The lower photograph shows a closer view in which the ingested snake can be seen abutting against the duodenum
of the intestine (arrows). Photographs by the author.
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products are absorbed into the blood circulation. The surface
of the intestinal mucosa bears numerous fingerlike strictures
called villi (villus singular), and the mucosal cells covering the
surfaces of individual villi are in turn covered with numerous
smaller projections, termed microvilli—perhaps several thou-
sand per individual cell (fig. 2.34). Collectively these greatly
enlarge the absorptive surface area that is exposed to the
chyme within the lumen. The membrane of the microvilli has
embedded enzymes that act strictly in the local environment
of the microvilli. The anterior part of the intestine also re-
ceives digestive enzymes via a small duct that conveys these
enzymes from the pancreas. The liver secretes bile, which is
stored in the gall bladder and conveyed by a duct to the intes-
tine, where it serves to emulsify lipids, or fats (fig. 2.2). Collec-
tively these various secretions neutralize the acids from the
stomach, break fats apart, and further digest the chyme
within the lumen of the intestine. Because snakes are carni-
vores, many of the digestive enzymes—both in the stomach
and in the intestine—are proteases that digest protein.
The chyme is broken, mixed, and moved in a net posterior
direction by the peristaltic actions of smooth muscle in the
intestinal wall. The arrangement of these muscles involves an
inner circular layer and an outer longitudinal layer (fig. 2.34).
Contraction of the circular layer and simultaneous relaxation
of the longitudinal layer both constricts and elongates the
intestinal tube. Alternately, relaxation of the circular layer
coordinated with active shortening of the longitudinal layer
results in shortening and distension of the intestinal tube.
The intestine consists of two principal regions, the ante-
rior small intestine and the posteriormost segment called
the large intestine. The large intestine is much shorter than
the small intestine and usually has an enlarged diameter.
Figure 2.34. Photomicrographs illustrating histological sections Following the acidic phase of digestion in the stomach, the
through portions of the stomach (upper photo) and small intestine final stages of digestion and mixing occur in the small intes-
(lower photo) of a Dumeril’s Ground Boa (Acrantophis dumerili). The tine. Absorption of the digestive products, including water,
absorptive epithelial cells of the mucosa are arranged on mucosal folds occurs largely within the large intestine. The undigested
(stomach) or villi (intestine), and the latter especially increase the
parts of the chyme that are not absorbed are formed into
absorptive surface area. Arrows point to the layers of smooth muscle
in the intestine. The smooth muscle of the mucosa is thin and feces, which become increasingly more solid in composition
consists of a single cell layer in the intestine (m). The outer smooth due to the intestinal absorption of water. The feces also
muscle is circular in arrangement (c), with outer longitudinal muscle contain large amounts of bacteria that are passed along
(l) being thinner and shown only for the intestine. The histological from the upper parts of the gut where bacterial populations
stain is Masson’s trichome. Photomicrographs by Elliott Jacobson.
flourish and participate in digestion.
The feces empty into the cloaca, which is the most posterior
secretion increases with the size and structural composi- segment of the gut (fig. 2.35). It is a common chamber that
tion of food. Digestion is prolonged at lower temperatures receives digestive products from the intestine and urinary
and is critically slowed or ceases altogether if the tempera- products from the kidney, and is also a passageway for prod-
ture falls below about 10°C. The precise temperature thresh- ucts from the reproductive tract. As such, the cloaca typically
old varies in different species (see chapter 4). contains the feces together with a slurry of uric acid and urates
from the kidney. Urates are salts of uric acid. Together these
Intestine form a crystalline waste product of nitrogen metabolism,
The intestine is a very important segment of the gut where which is excreted by the kidney. Uric acid is poorly soluble in
the final digestive breakdown of food occurs, and the resulting water and can be eliminated in a precipitated form, which is
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the physical presence of food in the gut, and by gastrointes-
tinal hormones secreted from endocrine cells in the walls of
the stomach and intestine. Compared with some other ver-
tebrates (especially mammals), very little is known about
the control of digestive secretions in snakes, although it is
assumed to be quite similar.
Periodic Feeding
Snakes are characterized as discontinuous, intermittent, or
periodic feeders. Because rates of metabolism, and therefore
energy requirements, are relatively low, snakes do not re-
quire a lot of food—at least in comparison with endothermic
birds and mammals (see chapter 4). Further, because many
snakes have the capability for feeding on comparatively large
Figure 2.35. Cloaca of a Florida Cottonmouth (Agkistrodon prey, which they swallow entire, snakes do not need to feed
piscivorus conanti). This is the posteriormost aspect of the digestive often. However, one other consideration is very important.
tract and receives the digestive wastes from the intestine, fetuses The period of annual time that is available for feeding and
from the paired oviducts, and urine from paired ureters. Each oviduct
growth is variously limited in temperate climates, because
connects to one of the paired ovaries, and where the terminal
segment enters the cloaca it is termed vagina or vaginal pouch. The
snakes are dormant or inactive during the colder months and
vagina at the left has been cut to reveal the ureter that runs alongside cannot digest food at low temperatures. Therefore, there are
of it. One also sees the mucosal folds where sperm can be stored. circumstances in which many species of snakes do not eat as
Each of the paired ureters communicates with one of the kidneys. frequently as their digestive systems might otherwise per-
This snake died from unknown causes and was frozen until the mit. The requirement for energy varies with many factors
tissues were observed following thawing. Photograph by the author.
including temperature, activity, growth, and reproduction.
Generally, snakes ingest about 6 to 30 meals per year,
totaling 55 to 300 percent of their body mass, to meet their
the familiar white to yellow solid material that is seen together overall energy needs according to estimates by Harry
with the fecal elimination of snakes. If a snake is in good water Greene. Very little is known about the frequency of feeding
balance both the feces and the urates might appear quite soft by wild snakes in their natural environment, and whether
or fluid, especially if these are eliminated after the snake has prey is sufficiently abundant for a given snake population
had a good drink of water. On the other hand, if a snake is or whether it is limited. Studies in which rattlesnakes (Cro-
partially dehydrated and has not drunk recently, the feces and talus atrox and C. horridus) were artificially fed supplemental
the urates appear more solid and can actually be very hard and food demonstrated that such food supplementation led to
compressed. This is due to extra water absorption, which prob- increased rates of growth and reproduction. Of course the
ably occurs in the cloaca as well as the small intestine. Occa- foraging success of individual snakes in a wild population
sionally, excess water absorption from a large volume of feces will vary, and some may do very well while others may be-
can result in a compaction that forms a blockage and is not come emaciated and die from malnutrition. Here we can
easily passed by the snake. Thus, access to water is important appreciate the advantage of the low metabolic rate, however.
with respect to adequate digestive function in snakes. If mammals cannot find food, generally they will perish
The various enzymes, venom toxins, acid secretions, and within a few days or weeks, whereas some species of snakes
bacteria chemically reduce the food to elemental compo- in captivity can survive for more than a year without a
nents of carbohydrates, proteins, and lipids, which are ab- meal. Some rattlesnakes can survive without food for pe-
sorbed into the blood circulation across the wall of the riods up to two years. Further, if we consider only the en-
intestine. The digestive tract can be regarded as an input- ergy required for routine maintenance, a 50 g garter snake
output system, with food entering the mouth and feces ex- in Michigan requires only the equivalent of one 44 g frog to
iting the cloacal opening (vent), while water and nutrients sustain itself for an entire year according to estimates by
are taken up and distributed to the body from the digestive Warren Porter and C. Richard Tracy. In another study, Mar-
regions that lie between these “in” and “out” terminal shall McCue and I estimated that an insular adult Cotton-
points of the gut. The mechanical motions attributable to mouth in Florida requires only 1 kg of fish for annual
smooth muscle are coordinated largely by nerves that acti- maintenance and activity. This would be equivalent to only
vate the smooth muscles in the wall of the gut. The simulta- a few small to medium-size fish. In a study of foraging
neous coordination of digestive secretions is controlled by modes comparing a “lie and wait” Sidewinder Rattlesnake
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(Crotalus cerastes) with a widely “active foraging” Coach-
whip (Masticophis flagellum), Stephen Secor and Kenneth
Nagy found that the more active Coachwhip consumed prey
energy at a rate about 2.1 times greater than did the less
active sidewinder.
The digestive tract is a highly dynamic organ that re-
sponds dramatically to changes in the quantity and quality
of food. Different sections of the gut become immediately
active upon the arrival of food or chyme. Additionally, the
demands for digestion related to feeding lead to changes in
morphological and physiological features of the gut, in-
cluding increases in metabolic activity and changes in the
mass and shape of the epithelial lining that double or triple
the absorptive surface area. Simultaneously, there is an in-
crease in the capacity to secrete digestive enzymes and for
molecular “transporters” to take up nutrients across the in-
testinal wall. Such a response to feeding is termed up-
regulation and may occur within 24 to 48 hours of ingesting a
meal. The responses are fully reversible, and down-regulation
occurs in the absence of food or during voluntary fasting. Ex-
tended periods of fasting are characterized by reductions in
metabolic rate and in the atrophy of the digestive tract.
The responses to feeding have been especially well studied
in the Burmese Python, Python molurus, by Stephen Secor.
Within one to three days after ingesting a meal, the intestinal
Figure 2.36. Relative increases in metabolic rate and wet mass of
capacity for nutrient uptake increases from 11 to 24 times that the small intestine, measured as mean changes in Burmese Pythons
of fasting levels, while the intestinal mucosa more than doubles (Python molurus) following the ingestion of rodent meals. The original
in mass (fig. 2.36). There are also considerable increases in the units were measured as rates of oxygen consumption and grams,
masses of other organs, such as the liver, that are active in pro- respectively. These graphs are approximations of the original data and
are intended only to show relative changes through time (see
cessing nutrients. The up-regulated condition of the intestine
references for Stephen Secor and Jared Diamond). Drawing by the
returns to fasting levels by the time of defecation at 8–14 days. author.
Similar up-regulation occurs in the digestive responses of
snakes that feed infrequently (four- to six-week intervals).
In contrast, snakes that feed more frequently (one- to only up to some limit. Thus snakes at low body tempera-
two-week intervals) exhibit very little changes in the intes- tures digest more slowly than do those at higher tempera-
tinal mass or capacities for nutrient uptake. Consideration tures, other factors being equal. Further, it seems intuitive
of digestive costs suggests that saving energy has probably as well as based in observation that for a given tempera-
driven the evolution of low mass and low activities of the ture, it takes a snake longer to digest a large meal (remem-
digestive organs during fasting, and of large up-regulated ber, swallowed whole) than it does to digest a smaller
responses to ingestion of a meal in species that feed infre- meal. But within certain limits the size of prey seems not
quently. Generally, the dichotomy of responses I have de- to affect digestion rates in some species of snakes (e.g.,
scribed is seen between ambush foraging snakes (mostly Thamnophis elegans, Vipera aspis). However, the nature or
pythons, boas, and vipers) and actively foraging snakes that composition of the prey can definitely influence the diges-
feed relatively more frequently in the wild (e.g., many colu- tion rate. Softer prey such as a frog or fish is digested
brid and elapid snakes). quite rapidly, within 36 to 72 hours depending on size,
whereas harder items such as crustaceans or hard-shelled
insects take longer. Mammals and birds are digested more
Rates, Costs, and Efficiency of Digestion
slowly than are fish or frogs owing to the presence of hair,
Rates of Digestion feathers, claws, or beaks (figs. 2.31, 2.37). Hard, keratinous
Rates of digestion in snakes vary considerably depending proteins are more difficult to digest than are softer tis-
on both the external and internal conditions of the an- sues, and these are typically passed and eliminated intact
imal. Generally, digestion increases with temperature, but in feces.
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Digestive Efficiency
Scientists usually quantify the “efficiency” of digestion in
terms of the net energy that is absorbed into the body by
the digestive tract. That is, digestive efficiency can be ex-
pressed as the ratio of the absorbed energy to the total en-
ergy that is present in the intact prey before digestion,
expressed as a decimal fraction or as a percentage. The en-
ergy that is neither digested nor absorbed is what appears
as feces, together with some added bacteria. Generally, di-
gestive efficiencies of most squamate reptiles that have
been studied approach or exceed 90 percent. The few mea-
surements in snakes are generally between 85 to 95 percent
and vary with species, individuals, meal size, and tempera-
ture. If the indigestible hair component is excluded from
calculations, the digestive efficiencies can be extremely
high—between 99.3 and 99.8 percent! Perhaps the high di-
gestive efficiencies are important in species with long inter-
vals between feeding and reflect the longer passage times
for feces in these species (see below).
The high efficiencies of digestion have some important
implications for how snakes increase their acquisition of en-
ergy when there is need. Because the amount of energy ex-
tracted from meals is relatively high, there is not much
room for improving the energy gain per meal. Further, some
studies indicate that digestive efficiency varies little with
temperature. Therefore, the manner by which snakes are
able to increase their input of chemical energy is to increase
the rate of feeding and passage of feces, rather than to in-
crease the amount of calories that are absorbed from indi-
vidual meals. That is, increasing energy gain from food is a
game of increasing rate rather than efficiency of extraction.
The efficiency achieved depends on the composition of
the prey. Fur, feathers, and mineralized structures such as
teeth and some bones are indigestible, as are most plant
materials. Plants with thin and relatively soft cellular walls
can be digested by some species, however (fig. 2.38).
Fecal Passage Time

The formation, storage, and evacuation of feces are impor-
tant features of the digestive processing of food. If we con-
sider the relatively large size of meals that are eaten by
snakes, the time that feces are held within the lower diges-
tive tract adds a potentially considerable component to the
overall mass of a snake. The time elapsed from ingestion to
defecation, known as the gut passage time, typically varies
from a few hours or a few days in birds and mammals to
several weeks or longer in other species of vertebrates.
Figure 2.37. Radiographs of a Black Rat Snake (Pantherophis However, snakes are clearly champions when it comes to
obsoletus) digesting a chick that was injected with barium. The
the range and maximum passage time for fecal matter.
uppermost image shows the position of the chick in the stomach
shortly after being swallowed. The descending images that follow
Stout and heavy species of terrestrial snakes, especially
illustrate the condition of the chick during sequential times following ground-dwelling viperid and boid species, retain and accumu-
ingestion. Photographs by Elliott R. Jacobson. late fecal material for periods of months while on a regular
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are known in various captive snakes, and have been re-
ported, albeit rarely, in wild-caught animals.
In summary, the storage of fecal mass in snakes varies
positively with the structural body mass of species, which
in general reflects their habitat and foraging mode. For
whatever reasons arboreal species have evolved slender
body shape with low mass, the frequent defecation exhib-
ited by these species helps to keep the mass low. On the
other hand, for whatever reasons the stout, ground-dwell-
ing, ambush predatory vipers and pythons have evolved
heavy bodies, the accumulation of feces adds to the struc-
tural body mass especially at the posterior end of the an-
imal. The posterior trunk of these snakes usually remains
on the ground as an important anchor during striking, and
perhaps this is nature’s reason for the evolution of ex-
tremely long passage times. Thus, extremely prolonged re-
Figure 2.38. A captive Florida Cottonmouth (Agkistrodon piscivorus tention of feces possibly functions as metabolically inert
conanti) eating marine algae (Ulva lactuca) that was tainted with fish
ballast in the heavier species, while simultaneously en-
odor. This alga species has soft cell walls and is digestible by the
snake. Such consumption of plant material probably rarely happens, hancing the maximum uptake of water and nutrients. Void-
but is possible when Cottonmouths forage along island beaches and ing a large mass of feces that might be stored in this way is
consume dead fishes that might be washed ashore along with other potentially risky and is greatly facilitated by access to
objects including much marine plant material. Photograph by the drinking water.
author.
The Energy Cost of Digestion

feeding schedule. My investigations of the Gaboon Adder, Bi- When snakes consume a prey item and digest it, there is an
tis gabonica, indicate that these snakes accumulate feces to energetic cost that is reflected in an increase in the rate of
what appears to be a maximum of storage capacity regardless metabolism (fig. 2.36). The increment of metabolism above
of the rate of feeding. Thus, at slower feeding rates the pas- normal resting levels is called specific dynamic action (abbre-
sage time can be as long as a year or more, whereas at faster viated SDA), postprandial metabolic response, postprandial
feeding rates the passage time is reduced to about 1.5 months. thermogenesis, or postprandial calorigenic response. SDA rep-
In either case, feces are accumulated to the extent they repre- resents the sum total of energy that is expended on the in-
sent about 5 to 20 percent of the total mass of the snake. The gestion and processing of a meal. These energy costs reflect
maximum defecation interval that has been observed in the the mechanical and biochemical processes involved in di-
Gaboon Adder is 420 days! Other maxima include 174 days in gestion and the assimilation of digestive products.
Python molurus and 386 days in Python curtus. The digestion of an intact meal is an expensive under-
In contrast to the heavy-bodied species just mentioned, taking, especially for snakes that consume large prey items.
slender arboreal species of snakes are characterized by rela- For example, SDA responses of Burmese Pythons charac-
tively rapid passage times—the known minimum being 23 teristically involve 5- to 44-fold increases in the rate of
hours in a Haitian tree snake, Uromacer oxyrhynchus, to my metabolism measured in these snakes. Stephen Secor
knowledge. There is also a trend among snakes for more ac- estimated that in Burmese Pythons activities of the stom-
tive species to have shorter passage times than do seden- ach contributed about 55 percent of SDA, protein synthesis
tary species. It appears to make sense for more active contributed another 26 percent, gastrointestinal up-
species to void excess fecal mass and thereby lighten the regulation contributed about 5 percent, and other activities
load in locomotion. This appears to be especially important about 14 percent.
in arboreal species that climb within, or over, foliage that Characteristically, the postfeeding rate of metabolism in-
might provide weak and unstable support. creases rapidly within 24 hours after feeding, and then de-
There is one possible penalty that snakes might pay clines more slowly. The response peaks early, usually within
when they retain fecal mass, especially without adequate 24–48 hours, and declines to normal after about 4–12 days
intake of water. Compacted fecal matter can form an intes- depending on the species and prey item (fig. 2.36). Generally,
tinal obstruction if the mass of material is large, and/or if species of snakes that feed infrequently have lower rates of
the material is very dense and hard due to removal of water metabolism when fasting but greater increases of metabo-
(that is taken up by the gut). Gastrointestinal obstructions lism in SDA, longer durations of elevated metabolism, and
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higher total extra energy expenditure in SDA than do spe- leaks across the skin surfaces either in evaporation, or in
cies that feed relatively frequently. Stephen Secor and the case of aquatic animals, water that leaks across the skin
Jared Diamond found that in various species, SDA repre- or exposed membranes in response to osmosis. The latter
sents from 13 to 33 percent of the total energy that is in- can be potentially important for marine animals. These in-
gested with a meal and tends to be higher in infrequent ward and outward fluxes of water are summarized in figure
feeders compared with frequent feeders. Evidently, how- 2.39 and are discussed in more detail in the sections that
ever, down-regulation of the gut (fig. 2.36) and other organs follow.
following feeding contributes to the low rates of fasting
metabolism and saves long-term energy during the periods The Kidney
between meals in the infrequent feeders. Arguably, it ap- The kidneys of snakes are paired structures located in the
pears there has evolved an association between natural dorsal body cavity with the right kidney more anterior in
feeding intervals and the regulation of gut performance in location than the left kidney (figs. 2.2, 6.5). The kidneys fil-
snakes. ter the blood and remove waste products. They are simpler
than those of mammals, and they cannot produce urine
that is more concentrated than the body fluids. Snakes do
Water Balance in Snakes not have a urinary bladder, and the urine is carried by ducts
Water is an essential resource for snakes, just as is food or from the kidneys and empties directly into the cloaca.
energy. Like other vertebrates, it is important for snakes With respect to water balance, urine is liquid derived
to maintain an appropriate content of body water so that from blood plasma and therefore contains water. Thus, ex-
the composition of cells and body fluids are kept within a cretion of wastes in urine requires losses of water. However,
range that is compatible with living processes. Generally, water can be a waste product in need of excretion if it is
the tissues of snakes consist of about 65 to 80 percent present in excess amount. In this case, the urine will be less
water, and dehydration below this range can be deleterious concentrated and greater in volume to remove body water.
or lethal. Therefore, snakes require water for living just as On the other hand, if water is in short supply the urine will
they do food. be more concentrated and produced in smaller quantities to
There are three sources of water available to snakes (or conserve water. Once urine enters the cloaca it can be fur-
any other animal). First, there is a certain amount of pre- ther modified by the uptake of water—either in the cloaca
formed water that is available in the food that is eaten. This or hindgut—and held for some while or excreted with less
is called dietary water. Second, small amounts of water are water. Also, snakes produce uric acid as the principal form
formed during the metabolism of food, after it is broken of nitrogenous wastes that result from the metabolism of
down during digestion and assimilated into tissues. This is protein. The white or yellow mass associated with urine or
called metabolic water. The third source of water is free feces consists of urates, and these may be present as a slurry
water in the environment, which ultimately comes from of soft material or as a solid mass, sometimes nearly stone-
rainfall. All three sources of water are part of a snake’s like. The differences in fluidity depend on how much water
“water budget,” but most species depend to some degree on has been reclaimed from the urine and urates before their
drinking fresh water in the environment in order to main- elimination. Thus, a dehydrated snake will eliminate solid
tain water balance. and very dry urates (and also feces) as a result of water re-
To remain in water balance, an animal must replenish tention prior to elimination. Uric acid is an advantageous
water that is lost from the body. Hence, averaged over form of nitrogenous excretion because it easily precipitates
time, the input of water must equal the summed outputs and can be eliminated with minimum loss of water (com-
or losses of water, just as the same is true of energy inputs pared with the other forms of nitrogenous waste, urea and
and outputs with respect to the food that is required for ammonium).
fueling an animal’s metabolism. The inputs of water for a As a husbandry issue, adequate water is important for
snake include dietary water, metabolic water, water that is the normal elimination of feces and urates. If a snake be-
obtained by drinking from the environment, and water comes dehydrated, these products tend to form a more
that might leak across the skin or other membranes from hardened mass that can sometimes create a blockage that
the environment. The latter is potentially quite important can be harmful or even lethal to a snake. It can be surmised
for aquatic animals, which also accidentally ingest water that there are very effective mechanisms for conserving
that “leaks” through the mouth during the process of swal- water by withdrawing and retaining water that is normally
lowing food. This latter water has been referred to as “inci- eliminated with urine and feces, and this occurs in the
dental drinking.” On the output side, the losses of water hindgut and cloaca. These processes are not well studied in
include water that is lost in feces and urine, and water that snakes, however.
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Salt Glands
Salt glands are excretory structures that
are accessory to the kidney and have the
capability to secrete concentrated salt so-
lutions. These have evolved in various
taxa of tetrapods that live in dry habitats
and are lacking a kidney with a capacity to
excrete very concentrated urine, which
include birds and various reptiles. Among
snakes these occur in various lineages of
marine species living in habitats where
ingestion of excess salt creates an osmotic
problem and compounds the tendency to
lose water to a salty environment. The salt
concentration in the body fluids of
snakes, including marine species, is only
Figure 2.39. Hypothetical water fluxes in and out of a Central American Rattlesnake
about one-third or less of that present in
(Crotalus simus). The net exchange (over time) determines whether the snake will be in
seawater. Thus, marine snakes will tend positive or negative water balance. This rattlesnake was crossing a road in Guanacaste
to lose water and gain salt from the envi- Province, Costa Rica. Photograph by Shauna Lillywhite.
ronment, which can greatly disturb water
balance. Salt glands help to alleviate this
dual problem, but they are variously ef- permeability barrier consisting of layered lipids sandwiched
fective in different species depending on the size of the in between alternating layers of keratin inside the stratum
glands and their rate of secretion. corneum of the epidermis (see chapter 5). Within the skin,
The salt glands of snakes are relatively small structures lipid bodies (termed lamellar granules) are secreted from dif-
that are located in the lower jaw beneath or anterior to the ferentiating α-cells and subsequently become organized
tongue casing (acrochordids, laticaudines, and hydrophi- into lamellar “sheets” that fill the extracellular spaces.
ines), or in the case of homalopsids there is a premaxillary Both the quantity and organization of these lipids gener-
location. In other taxa of tetrapods, salt glands are associ- ally correlate with the aridity of the habitat in which a
ated with other locations in the head, including nasal, or- species lives. The drier the environment, the greater the
bital, and oral cavities. quantity of lipids that occur in the permeability barrier.
The presence of salt glands in marine snakes may help to This appears to be the mechanistic basis for the generaliza-
confer the ability of these animals to live in seawater. In- tion that species of snakes living in drier terrestrial habitats
deed, François Brischoux and his colleagues have demon- tend to have lower rates of cutaneous evaporative water
strated that species residing in ocean water of higher loss, compared with those living in more mesic habitats.
salinity generally possess salt glands that have been shown Among sea kraits (Laticauda spp.), studies by the author
to secrete salts at higher rates than do those of other spe- and his colleagues have demonstrated that rates of water
cies inhabiting lower salinity water. However, some species loss across the skin are much lower when snakes are in sea-
of marine snakes (Acrochordus granulatus, Laticauda spp. water than when they are in air. Sea kraits are partly terres-
and Pelamis) require fresh water to avoid dehydration, so in trial, however, and species that spend more time on land
these species salt glands might help to regulate salt balance tend to have lower rates of evaporative water loss than do
and slow the rate of dehydration, but they are not sufficient those that are more thoroughly aquatic. Finally, those spe-
alone to maintain water balance. These subjects need to be cies of sea kraits that are relatively more aquatic tend to
investigated more thoroughly in a broader range of species. have lower rates of water loss across the skin when in sea-
water than do the species with more terrestrial tendencies.
Water Flux across the Skin In other words, the properties of the skin tend to be “ad-
The skin is a complex organ that has many functions, in- justed” for conserving water relative to the habitat in which
cluding regulation of the amount of water that moves a species spends more of its time.
across the skin, either as a bidirectional osmotic flux (e.g., In the embryos of egg-laying species of snakes, the em-
aquatic species) or as evaporation from skin surfaces to bryonic epidermis tends to slough within the egg, and a
surrounding air (fig. 2.39). These movements of water— permeability barrier of partial competence is formed within
either in or out of the skin—are regulated in large part by a the epidermis prior to the snake’s hatching. The resistance
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of the skin to evaporative water loss improves with subse- David Cundall and his colleagues have investigated the
quent skin-shedding events, which indicates there is some biomechanics of drinking in snakes. Many advanced species
capacity for the skin to improve its barrier effectiveness. of snakes drink by sucking water into the mouth followed
There is some indication that the effectiveness of the per- by compression of the mouth cavity that forces the water
meability barrier can be improved or “adjusted” during ec- into the esophagus. However, some of these species are ca-
dysis in response to the aridity of the environment. Further pable of drinking without sealing the margins of the mouth,
research is needed on this subject before it can be general- which implies that water can be ingested without being de-
ized, however. pendent on buccal pumping. Opening and closing move-
ments of the jaws are variable, as is the volume of water
that is ingested with each cycle of jaw movements. Snakes
Drinking Behaviors of Snakes drink using a variety of movement patterns, and the jaws
Many persons who have maintained snakes in captivity have might be variably “sealed” (or not) in different circum-
noted that occasionally certain individuals will stop feeding, stances. In addition to the use of periodic buccal pumping,
and that some species are reluctant to eat at all. However, a mucosal folds in the mouth of snakes act like a sponge to
thirsty snake will always, in my experience, drink water. The trap water or attract water by capillarity. Cundall and his
voluntary “will” to drink implies a snake is thirsty, and the colleagues have proposed a second model for drinking—
sensation of thirst implies there is a physiological signal re- termed the “sponge model”—in which water is moved by
lated to dehydration and negative water balance. In wild the rhythmic squeezing and relaxation of parts of the
populations, snakes have various opportunities to drink. mouth having channels or surfaces with sponge-like prop-
These include standing bodies of water such as ponds or erties. Some of the adhering water can move in an anterior
lakes, freshwater streams, rainfall, and water that might col- direction, but water that moves in a posterior direction
lect on the body of a coiled snake, or on leaves, small depres- goes toward the esophagus. The rear part of the mouth
sions, and so on, during rainstorms and persist for some cavity contains expanded regions that are sponge-like and
while thereafter. If water is not available, for example during overlain by muscles. Complex movements of these and
a seasonal drought, snakes might go for long periods with- other muscles drive the water.
out a drink. In these circumstances, dehydrating snakes The mucosal folds in the mouth that entrap and move
might become reclusive and remain down burrows or in water are features that likely evolved in relation to the
other places where evaporative losses are mitigated and stretching of mouth parts around relatively large prey. The
body water is conserved. Generally, snakes that are living in function of these features in drinking is therefore likely to
arid environments have a suite of adaptations to conserve represent a secondary use of anatomical traits having an-
water and/or tolerate a considerable degree of dehydration. other, perhaps principal, function related to feeding.
Some species might be able to depend largely, or perhaps ex-
clusively, on dietary and metabolic water. However, such
ability has not yet been demonstrated for snakes.
Terrestrial species of snakes will generally drink water Additional Reading
on a somewhat regular basis whenever water balance be- Aubret, F., R. Shine, and X. Bonnet. 2004. Adaptive developmental
plasticity in snakes. Nature 431:261–262.
comes slightly negative. In some cases the consumption of
Bedford, G. S., and K. A. Christian. 2000. Digestive efficiency in
water increases following feeding. Digestion requires water, some Australian pythons. Copeia 2000:829–834.
followed by production of urine to eliminate nitrogenous Bels, V., and K. V. Kardong. 1995. Water drinking in snakes: Evi-
wastes that result from the metabolic processing of the ab- dence for an esophageal sphincter. Journal of Experimental
sorbed food products. If snakes have access to water, feces Zoology 272:235–239.
are eliminated in a moist or wet condition, which also re- Bonnet X., and F. Brischoux. 2008. Thirsty sea snakes forsake ref-
uge during rainfall. Australian Ecology 33:911–921.
flects these water losses. In contrast, recent studies by the Brischoux, F., R. Tingley, R. Shine, and H. B. Lillywhite. 2012. Sa-
author and his associates have demonstrated that sea linity influences the distribution of marine snakes: Implica-
snakes are reluctant to drink fresh water unless they have tions for evolutionary transitions to marine life. Ecography
been dehydrated to a considerable extent (10 to 20% or 35:994–1003.
more loss of body mass in several species). This probably Britt, E. J., A. J. Clark, and A. F. Bennett. 2009. Dental morphol-
ogies in gartersnakes (Thamnophis) and their connection to
reflects an evolutionary suppression of the drinking stim-
dietary preferences. Copeia 43:252–259.
ulus related to the influence of other traits that conserve Catania, K. C. 2009. Tentacled snakes turn C-starts to their advan-
body water and increase the tolerance to dehydration as tage and predict future prey behavior. Proceedings of the
these snakes adapted to marine existence. National Academy of Sciences (USA) 106:11183–11187.
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Catania, K. C. 2010. Born knowing: Tentacled snakes innately pre- Gartner, G. E. A., and H. W. Greene. 2008. Adaptation in the Afri-
dict future prey behavior. PLoS ONE 5:1–10. can egg-eating snake: A comparative approach to a classic
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L O COMOT ION: HOW SNAK E S M O V E
There has been much conjecture about the methods of locomotion of

serpents. The speed, strength and agility of many species appears
astonishing. . . . Here is true specialization, presenting a group of creatures
which have lost their limbs yet acquired remarkable dexterity with apparently
3
little effort, through no visible means.
—Raymond L. Ditmars, Snakes of the World (1943), p. 16
Limbless Movement resembling a low-pitched whirring noise as a magnificent

One of the truly remarkable attributes of snakes is how large Eastern Coachwhip snake undulated across damp sand
well these limbless animals move through a variety of to escape into nearby vegetation. I was surprised, and simul-
landscapes—over, through, or around features of their taneously delighted, by the sound that was produced when
highly varied habitats. Snakes swim, dive, move rapidly the belly scales of the snake met the damp sand of the beach.
through bushes or across rocks, crawl across featureless sand Of course, occasional captures or sightings of snakes con-
terrain, climb vertically up trees where they move swiftly firmed the meaning of these particular sounds, which are
through canopy, and, in some species, catapult from great available to anyone who is alert to his or her surroundings
heights and glide through the air to land without harm on while enjoying a summer walk.
the ground below. Even the more usual or common move- The more one thinks about how snakes move, and their
ments over terrestrial landscapes can be extraordinary in ability to move rapidly and gracefully over many surfaces,
their appearances. I recall vividly on several occasions while the more we are in awe at the amazing, swift, and seem-
looking for snakes that might be crossing country roads, ingly effortless locomotion of snakes when moving with-
when a large, dark-colored snake such as a Southern Black out limbs. How do snakes perform the amazing and
Racer or Southern Pacific Rattlesnake moved on pavement impressive feats that anyone can witness in the appro-
and progressed without interruption to cross to the other priate circumstances? Obviously, we need to learn more
side. In many such cases the snake’s movement conjured the about the structure of the snake’s body, especially the
image of black oil pouring onto the road and flowing, seem- skeletal elements and their attached muscles with over-
ingly frictionless, across the road surface. A similar scene lying skin.
was witnessed on numerous occasions while driving slowly
and looking for snakes during the evening on paved roads in
the California desert. Sidewinder Rattlesnakes, appearing Muscle and Skeletal Adaptations
white when illuminated by the headlights of an automobile, The body of a snake is elongated and limbless, and these
appeared to glide across the road as they were watched from conditions have evolved many times in various vertebrate
a distance. On other snake hunts, off-road, I recall hearing lineages—for example fishes, salamanders, and lizards.
countless “swishes” in dry, summer grasses as racers or Snakes, however, exhibit marvelous variation and seeming
whipsnakes moved off rapidly in advance of my walking, perfection of these attributes. To simplify matters, one
never to be seen as they disappeared into the drying vegeta- might consider a snake to be a simple tube with elongated
tion. I was only aware of their presence because of the sounds organs inside, separated by numerous supporting bones
that were created by undulating, slender bodies moving with muscles to move them and a tough but pliable skin cov-
through stems and leaves of the summer grasses. Once at a ering the outside (figs. 2.2, 6.9, 6.12). Relative to standing
beach near Naples, Florida, I heard a distinct sound quadrupedal vertebrates, snakes have a low center of mass
| 77
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that is close to the ground. The limbless body presents a can also affect the locomotion of snakes. Snakes with more
large area of frictional contact with the ground (but see be- vertebrae are generally slower than those having fewer.
low), and the mass of the snake is distributed over an ex- All movements of snakes are dependent on the interac-
tended area, rather than two or four points of contact that tions between the elongate skeleton and the muscles that
are associated with feet, as in mammals. attach to them. A common feature that is present in most
One obvious problem with elongating the body is the (but not all) patterns of snake locomotion is that vertebral
internal organs must be adjusted, reshaped, and reorga- bending is used in various ways to generate propulsive
nized to fit into the narrow body without sacrificing mo- forces. Commonly, undulating forms of locomotion depend
bility. Thus, many of the internal organs of snakes are on waves of lateral bending that are propagated from head
elongate in comparison with those of less attenuated ani- to tail. The vertebrae of snakes have many accessory ele-
mals (fig. 2.2). This condition is especially true for the lung, ments that resist torsion, and the various parts are aligned
liver, the kidneys, and the testes. The heart is also elon- such that lateral bending is generally easier than is bending
gated and comparatively slender in arboreal species of in the dorsal-to-ventral plane. Exceptions are the ability of
snakes, many of which are exceptionally thin. the neck to bend during displays of the well-known “hood”
In most snakes the internal organs are contained within of cobras (fig. 1.39), and the prehensile tails of various arbo-
an elongated body cavity that is surrounded by skeletal el- real species such as rat snakes, vine snakes, and many boas
ements above and on both sides. These skeletal elements (fig. 2.20).
consist of vertebrae and attached ribs. The latter in most Many aquatic and fast-moving terrestrial species of
cases are curved outward and downward, with their free snakes possess vertebrae with articulating parts called zyg-
ends positioned at or near the ventrolateral edges of the apophyses that are prominently broad with lateral extension
snake just above the ground (fig. 1.3). The belly plates are (fig. 3.2). Presumably, this increases the effectiveness of the
underlain within the snake by connective tissue and lever systems involved with muscles that flex the vertebral
muscle, so the ribs and vertebral column surround the in- column laterally. In these snakes the articulating surfaces
ternal organs except for the ventral aspect of the animal. also tend to be relatively small, and the vertebrae tend to be
In many terrestrial snakes the ventral boundary of the in- long and narrow. In arboreal species of snakes, the structure
ternal body cavity is relatively wide, but in some other of the zygapophyses provides a bony shelf on which attach-
groups, for example, sea snakes, the body is considerably ments of muscles can act to lock the otherwise flexible verte-
compressed in the vertical plane for swimming and the tips bral column into a rigid beam to facilitate the snake extending
of the ribs on each side of the body lie relatively closer to- the unsupported body considerable distances when it climbs
gether (figs. 3.1, 5.7). In any event, the evolutionary elonga- from one branch of a tree to another.
tion of a limbless body has resulted in an extended The axial musculature of snakes is extremely complex
vertebral column with many well-developed vertebrae. Hu- with many muscles and tendons that have origins and in-
mans, for example, have 12 vertebrae articulating with ribs sertions at various locations with respect to the axial skel-
that enclose the thoracic cavity, and these elements are ab- eton (fig. 3.3). Collectively, these muscles have segments
sent from much of the body length (if the legs are in- that form longitudinal columns and span many ribs. If one
cluded). Many species of fish typically have 30 to 60 thinks about it, the central nervous system of a snake must
vertebrae, including the body and the tail. In contrast, do an amazing job of integrating information about the
snakes usually have more than 100 vertebrae in the body landscape across which it moves, and simultaneously acti-
alone, and some species have more than 400 vertebrae ex- vate the requisite muscles in an appropriate pattern all
tending from the neck to near the tip of the tail. As a re- along the length of the body. For long-bodied species, espe-
sult, snakes are extremely flexible. Ribs are distributed cially, this requires superb neural control to ensure that the
along the length of the body, but not the tail (fig. 1.3). appropriate muscles are activated with precise timing at
The number of vertebrae possessed by a snake is related variable distances from the brain, which serves as a “com-
to its maximum length, and it therefore appears that the mand center.”
number of vertebrae has evolved in response to selection on Various muscles act as coherent units. For example, the
body size. Studies by Lars Lindell also show, however, that spinalis-semispinalis, longissimus dorsi, and iliocostalis con-
the number of vertebrae can be related to behavior and sist of overlapping segments that form longitudinal col-
ecology, apart from being affected by body size. For ex- umns (fig. 3.3). These are epaxial muscles and have been
ample, constricting species have more vertebrae per unit of shown to be activated to provide most of the power and
size than do nonconstricting species, and burrowing spe- control that are required for the undulatory movements of
cies tend to have fewer vertebrae per unit of size than do snakes. The various muscle actions cause bending of the
species that occupy other habitats. The number of vertebrae body and also stabilize the ribs against pulling when the
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Figure 3.1. Underwater views of the Yellow-bellied Sea Snake (Pelamis platurus) illustrating the vertically flattened body when the snake is
swimming or floating in the ocean. Individual ribs can be seen in the upper photo, and the absence of broad ventral scutes can be seen in the
lower photo (arrow). The skin below the ribs is flattened into a ventral body keel. These snakes were photographed in Costa Rica by Joseph Pfaller.
body bends laterally. Some of the axial muscles extend over are thought to facilitate the force of constriction, which
large numbers of vertebrae, and elongated tendons form tends to be associated with slower-moving snakes. Con-
connections between these muscles (fig. 3.3). In fast-mov- strictors are relatively less “stiff ” and have greater flexibility
ing species, the distances spanned by some muscle-tendon than many faster-moving snakes. The evolution of vertebral
chains extend over 40 consecutive ribs (or vertebral units), number and, in some cases shorter muscle segments, seems
whereas in slower species the same muscle units may span to account in part for this difference. In contrast, the longer
fewer than 9 vertebral units. Relatively short muscle units muscle-tendon units characteristic of the faster snakes
Locomotion: How Snakes Move | 79
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to the inadequate structure and function
of the human skeleton and the muscles
attached to it. Similarly, one can also try
this in water. Again, after a short time
making serious attempts to glide for-
ward like a snake, one appreciates the
fact that the human body, while capable
of bending at the waist, is not designed
for effective undulating movements that
are capable of creating forward propul-
sion in water. But we are limbed crea-
tures, so we swim using our arms and
legs. Following these simple and enter-
taining games, watch a snake carefully as
it moves, and think about the amazing
movements you see in context of the fea-
tures that are described in this chapter.
Aquatic Locomotion:
Swimming in Water
All living aquatic reptiles—including
crocodilians, turtles, and lizards, as well
Figure 3.2. A segment of the vertebral column of a Cottonmouth snake (Agkistrodon
as snakes—are secondary swimmers, in-
piscivorus) showing several vertebrae with articulating ribs. The head of each rib
(capitulum) articulates with a single vertebra. The zygapophyses provide surfaces for
sofar as these aquatic species evolved
articulation between successive neural arches, allowing some degree of horizontal (and from terrestrial ancestors. Interestingly,
lesser vertical) movement but preventing undue torsion. Skeleton courtesy of the all snakes can swim—some better than
Florida Museum of Natural History and photographed by the author. others—and all species have the ability to
undulate in water, usually with the head
held up while floating due to inflation of
might enable a snake to utilize longer undulations, theoret- the elongated lung. Sometimes, the conscious and pur-
ically with more efficient use of power due to having fewer poseful aquatic tendencies of snakes are surprising. For
points of force application and dissipation of energy in example, Eastern Diamondback Rattlesnakes, Crotalus ada-
overcoming lateral resistance (see below). A point of force manteus, often enter marine waters voluntarily, and they are
application (from snake to a physical feature in the environ- regularly sighted as they swim between islands in the coastal
ment) is called a resistance site (fig. 3.4). Elongated tendons waters of Florida. Indeed, some of the more plentiful, re-
add length to a contractile unit while minimizing the muscle maining populations of this species are on the coastal keys of
involved, which has greater mass. Generally, studies have Florida’s Gulf coast or the East coast intracoastal waterway.
demonstrated that much of the variation in segmental Some rattlesnakes have been sighted more than 10 miles
length of the locomotor muscles is related to habitat, body from shore in the Gulf of Mexico. In Southern California,
form, and the manner of movement (see below). Red Diamond Rattlesnakes, Crotalus ruber, are occasionally
washed down rivers during periods of high rainfall. Subse-
quently, they can be seen swimming in offshore ocean waters
Locomotion: How Do Snakes Move? or crawling onto beaches. Unlike rattlesnakes in the eastern
A simple game that one can engage to illustrate the amazing United States, however, these are not likely to be in the ocean
locomotor adaptations of snakes is to lie on the floor with water out of choice.
arms held straight back against the side of the body and, All aquatic snakes swim by movements called undulation,
while holding this position, try to move forward without regardless of the type of locomotion their terrestrial rela-
using arms, hands, or feet. This sounds simple and prob- tives might have used on land. This is the most ubiquitous
ably silly, but after some while during serious attempts at form of swimming and occurs in representatives from all
moving without the use of arms or legs, one begins to re- classes of vertebrates except birds. Snakes undulate with
alize that appropriate forces are necessary and missing due lateral movements, in contrast with specialized marine
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Figure 3.3. Axial muscles of snakes, used in locomotion. The upper photograph illustrates a dissection of the axial muscles in a preserved rat
snake (Pantherophis obsoletus). The lower photograph illustrates fine dissection of a preserved Ahaetulla prasina, illustrating fused and
elongate tendons (arrows) associated with the anterior spinalis semispinalis muscles. Note the individual muscle units associated with each
tendon to the left of each respective element in the figure. This illustrates an unusual morphology located in the trunk near the head, and is not
typical. The scale bar at the lower left of this photograph equals 1 cm. Abbreviations: IC, iliocostalis; LD, longissimus dorsi; M, multifidus; SP,
spinalis; SSP, semispinalis. Dissections and photographs by Phil Nicodemo.
mammals, which undulate in a vertical plane. Undulatory segments of the entire body, water is “discharged” into a
locomotion can be illustrated by the swimming movements wake beyond the tip of the tail or body (fig. 3.5). These as-
of a sea snake. In smooth propulsive movements, the body pects of the locomotion may not be obvious to a casual ob-
is bent into a wave that travels backward along the body server who watches a snake swim rapidly across a pond or
(fig. 3.5). Each body segment moves from side to side as suc- a stream.
cessive waves move from head to tail. As each undulating The swimming behavior of Yellow-bellied Sea Snakes
wave travels backward, water is accelerated to the side and (Pelamis platurus) has been studied by a team of investiga-
toward the rear by the rear-facing segment of the body, tors led by Jeffrey Graham at the Scripps Institution of
which produces a propulsive force by pushing against the Oceanography. The swimming movements are very much
water. Almost immediately the water is acted on by the next like that of an eel (termed anguilliform swimming). During
propulsive segment of the wave. near-surface swimming there are four half-waves present
The amplitude of lateral movements and the tendency for along the body having amplitudes that increase toward the
undulating body segments to act more directly backward tail. Routine swimming velocities ranged up to 20 cm/s
(opposite to forward movement) with propulsive force when snakes were near or at the surface, while swimming
against the water tend to increase toward the tail. That is, the velocities were lower at 1–8 cm/s when snakes swam below
angle of the body relative to the overall direction of swim- the surface. During subsurface swimming the snake typi-
ming tends to increase and thereby accelerate the water rear- cally assumes a posture in which the tail is elevated—also
ward. Eventually, after being influenced by all the propulsive characteristic of other sea snakes—and the posterior part of
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Figure 3.4. A Cat-eyed Snake (Leptodeira annulata) crawling vertically up a rock face in Guanacaste, Costa Rica.
Points of force application, called resistance sites, are indicated by the solid black arrows. These are places where a
physical irregularity in the rock surface provides a “catch” where the snake’s body pushes and creates propulsive force
as an undulation passes the point. The summed reaction forces at these points provide the force vector that moves the
snake forward, or upward, on the rock face. The resistance site near the center of the photograph is shown with
enlargement to its left. The white “x” indicates the point where the body is pushing maximally against the resistance
site. Notice how the snake’s body is “tightened” at this point to exert force against the rock. At the lower right a
second snake (Leptodeira nigrofasciata) is shown crawling up a rock face. Here a prominent resistance site (x and arrow)
is illustrated where there is a distinct projection on the rock face. This feature is shown with magnification in the
projected enlargement (follow broken white arrowheads). Snakes were photographed in Guanacaste, Costa Rica: L.
annulata by Coleman Sheehy III; L. nigrofasciata by Shauna Lillywhite.
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Figure 3.5. A swimming Yellow-bellied Sea Snake (Pelamis platurus) near the Guanacaste coast of Costa Rica illustrates the forces that
contribute to its movement through water. The muscles of the snake create waves of undulation that move backward along the body,
progressing from the neck to the paddle-shaped tail. Each undulating wave presses against the water to produce a propulsive force. The water
in turn creates a reaction force, which acts in the opposite direction and produces forward thrust. The directions of the propulsive forces
generated by a hypothetical body segment (yellow) are indicated by arrows at the left, including component vectors that act laterally or
sideways at right angles to the direction of movement. The magnitude of each force is indicated by the length of the respective arrow. The
collective forces act more or less equally on each side of the body as waves progress from the head to tail. Therefore, the lateral force vectors
cancel and add nothing to the thrust that moves the snake forward. The vector components are further illustrated in the lower diagram to the
right of the snake, where the edge of a body segment is represented by the yellow curved line. Similarly, at the left-hand side of the snake one
sees that both the direction and magnitude of the propulsive forces change in relation to the curvature of the body, again represented by the
yellow curved line. Only a single force vector is illustrated in more detail to the right of the snake. The wavelets that are evident in the water
adjacent to the snake are produced by the undulating waves of the snake’s body pushing against the water. Note that these are greater and
broader near the tail end of the snake, where the larger components of thrust are produced by the tail, which can be seen in this photo to be
“pushing” more in the backward direction than sideward against the water. Photograph and labeling by the author.
the body assumes a nearly vertical orientation. Swimming in segments do not contribute equally to thrust. The more pos-
this posture involves torsional and rolling motions rather terior body segments move with greater amplitude; hence,
than simple undulations, and these may contribute to the posterior parts of the body move faster through greater
thrust. Swimming speeds measured in other species of both distances and “push” against the water with vectors of pro-
laticaudine and hydrophiine sea snakes by Richard Shine pulsive force that act more directly toward the tail. Therefore,
and his coworkers range between mean values of 23 and the greater forces are more nearly aligned with the direction
141 cm/s, with males swimming faster than females. Am- of movement. This principle is illustrated in fig. 3.5.
phibious sea snakes swim faster in water than they crawl The propulsive force depends on the mass of the water
when they are on land. affected by each propulsive segment, which depends, in
Thrust is the forward-acting force on the animal and turn, on body shape. The depth, or width, of the body in-
equals the sum of all contributions of the propulsive seg- creases the propulsive force. Because the more posterior
ments (imagine the length of the snake being divided up into parts of the body contribute more to thrust, forces are max-
as many segments as you like, each interacting against the imized when the greatest depth of the body is posterior.
surrounding water at variable angles). The various propulsive This is precisely the way the body is designed in many of the
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fully aquatic sea snakes (fig. 3.6). However, there are nearly buoyant, or has a tendency to sink in water, this decreases the
always exceptions to general rules in nature, and the Yel- total resistance when an animal is swimming toward the
low-bellied Sea Snake (Pelamis platurus) undulates its body bottom, and, conversely, it increases the resistance when
to move backward as well as forward. This species is pelagic the swimming is toward the surface. Fourth, if an animal is
and spends time floating on the surface of the sea, waiting turning, centrifugal acceleration adds to the resistance. This
to capture fishes that attempt to hide beneath objects in- force acts at right angles to the forces resisting forward move-
cluding the snake. Swimming backward seems to be a ma- ment. The relative magnitudes of the resistance forces vary
neuvering strategy, which might explain the more uniform with the type of swimming. When inertial forces dominate
body shape that characterizes this species (fig. 1.44). drag forces, then an object will usually continue to move for a
The swimming performance of an aquatic animal depends considerable distance after it stops producing thrust, as oc-
not only on thrust propelling it forward, but also on over- curs when boats shut off their engines.
coming forces that resist the forward motion. Such forces are, Of the forces mentioned, the drag force is the most
collectively or individually, referred to as resistance. The ori- complex. It arises primarily from viscous effects in the boun-
gins of resistance are complex but can be divided into several dary layer, which refers to a thin film of water that immediately
components. First is an inertial component due to mass of surrounds the moving snake. In physical terms, the boundary
the animal and the enveloping water around it. The inertial layer is the region of water adjacent to the animal’s surface
force predominates when an animal has large size and rela- where the velocity of water relative to the snake decreases
tively low velocity. Second is a drag force attributable to vis- from near zero (at the body surface) to that of surrounding,
cosity of the water, which is equivalent to friction. Third is a undisturbed water (called the “free stream” velocity) with in-
vertical force attributable to gravity. If an animal is negatively creasing distance away from the snake (fig. 3.7). In other words,
there is a gradient of velocity extending outward in water away
from the snake’s surface. Energy is dissipated in shearing
forces that resist a distortion of the adjacent “layers” of water.
Stated another way, there is frictional dissipation of energy as
adjacent layers of water try to “slide” past each other. Here fric-
tion is related to the “stickiness” of fluid in the adjacent inter-
acting layers of water. (In this description the reader must
imagine a layer of water to consist of a three-dimension sheet,
which includes all the water of a particular velocity and ex-
tends as a continuous envelope around the snake. The next
adjacent sheet, or layer, moves at a slightly different velocity,
as long as one is within the boundary layer, and so on.)
Figure 3.6. A Black-headed Sea Snake (Hydrophis melanocephalus)

photographed on a board to illustrate the overall body morphology
(left). Note that the body increases in depth toward its posterior end
where the tail terminates in a broad “paddle.” The smaller head and
neck are related to feeding habits that involve probing the head into
small holes or crevices in the sea floor or coral. This specimen was
photographed at Heron Island on the Great Barrier Reef of Australia.
The snake on the right is another species of Hydrophis (H. elegans) Figure 3.7. Illustration of a boundary layer of fluid next to a
collected near Weipa on the Gulf of Carpentaria. The two snakes hypothetical patch of skin. The length of the horizontal arrows
illustrate variability in the body form of these related species. Not all represents the velocity of the fluid, which increases with distance
sea snakes exhibit the extreme morphology of H. melanocephalus, away from the skin surface (*). The boundary layer ends where the
which is used here simply to illustrate some of the features that are velocity becomes constant with further distance, which is called the
discussed in the text. Photographs by the author. “free stream.” Drawing by the author.
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The magnitude of the drag force depends on the fric- mass consists largely of muscle. These combined features
tional properties of skin, the area that is in contact with appear to be present in the body design of a number of sea
water, and how the boundary layer interacts with the rest of snakes, illustrated by Hydrophis spp. (fig. 3.6). Considering
the flow around the animal. During high rates of accelera- all species of snakes, however, some experts will realize
tion, the boundary layer gradually increases in thickness. there are exceptions to these generalizations.
Initially, although acceleration is high, the speed or actual Sea snakes tend to flatten the entire body medially or
velocity of movement is low. Therefore, the frictional drag is vertically (midsaggital or vertical plane) when swimming,
small during fast starts, and the resistance to movement is which enlarges the area of contact with water to produce
dominated largely by inertial forces. This can be very impor- thrust (fig. 3.1). Such vertical flattening also is characteris-
tant, as we will see in the following discussion. tic of the extremely supple-bodied file snakes (Acrochordus
With respect to periodic or intermittent (stop-and-go) spp.) as well as some highly aquatic colubrid snakes while
swimming, it is advantageous for the propulsive segments to swimming. Some aquatic species also flatten the skin below
maximize thrust. Because the frictional drag is relatively the tips of the ribs to produce a ventral body keel (e.g.,
small during accelerations, a propulsive segment with large Pelamis platurus, figs. 3.1, 5.7). Moreover, the tail of sea
area has a relatively small penalty in terms of drag. The prin- snakes is laterally flattened into a paddle-like structure that
cipal source of resistance for intermittent swimming is the comprises most of the tissue posterior to the vent (fig. 3.8).
mass of the system, or more correctly the nonmuscular “dead Presumably, this feature increases the capacity for poste-
weight.” Adaptations of morphology that reduce the dead rior thrust when swimming, and more powerful swimmers
weight and increase the proportion of body represented by have larger “paddles” with greater area in the vertical plane,
force-producing muscle increase the capacity for accelera- in addition to greater muscle mass (fig. 3.8). Recent studies
tion. On the other hand, drag increases with the square of by Kate Sanders and her colleagues have demonstrated that
swimming speed and is the principle source of resistance for the fully aquatic hydrophiine sea snakes have evolved spe-
prolonged or sustained swimming at moderate speeds. cialized extensions of the caudal vertebrae that help to sup-
Both thrust and the theoretical “efficiency” of locomotion port the laterally compressed tail in these marine species.
can vary with the speed of swimming. Insofar as drag in- Considering this principle in broader terms, one may note
creases with swimming speed, thrust must also be increased that evolutionary shifts from terrestrial to aquatic habitats
to enable forward movement. This increase in thrust is has produced laterally compressed “paddles” on the feet,
achieved by an increase in either the frequency or the ampli- fins, or tails of a variety of vertebrates.
tude of undulations, or both. In a recent study of swimming Curious to investigate this phenomenon further, Fabien
in sea kraits (Laticauda spp.), a team of investigators led by Aubret and Richard Shine conducted studies in which artifi-
François Brischoux attached accelerometers to snakes and de- cial paddles were affixed to the tails of juvenile tiger snakes
termined that swimming speed was related to a combination (Notechis scutatus, a terrestrial species), and they demon-
of increase in frequency and amplitude of the sway undula- strated that relatively small paddles on the tail (35 percent
tions produced by the swimming muscles. These observations of tail length) increased swimming speeds by 25 percent,
confirmed previous studies that were based more strictly on but decreased crawling speed on land by 17 percent. Sur-
analysis of motion. These and previous data also confirm that prisingly, a larger paddle (84 percent of tail length) was less
the amplitude of the body undulation increases progressively than half as effective for increasing swimming speed as was
from head to tail, which implies that the speed of propagation the smaller paddle. Of course, these were artificial struc-
of the propulsive wave also increases from head to tail. tures that no doubt increased the stiffness of the tail. Evi-
The various factors affecting thrust and the resistance to dently, the larger paddles of sea snakes are only effective
motion during acceleration and turning can be summarized following adaptive modification of the musculoskeletal
in terms of a hypothetical optimal morphology, which can systems that generate propulsion (fig. 3.8). While swim-
be defined to maximize performance. These features are, ming is almost certainly the key adaptation of the paddle-
first, a relatively large body with area of body increasing to- shaped tail of sea snakes, other additional functions are
ward the tail. A second important feature is an appropriately also possible. On several occasions I have observed sea
flexible body so that the amplitude of swimming undula- kraits (Laticauda semifasciata) near the ocean surface slap
tions can be maximized. This is also a property of swimming the water violently with the tail just before diving to escape.
snakes. A third feature is a large ratio of muscle mass rela- Perhaps this is a behavior that communicates a threat to
tive to body mass. Power is proportional to the volume other snakes, or that acts to startle or confuse potential
(more strictly, cross-sectional area) of muscle, whereas drag predators. This statement is admittedly pure speculation,
is proportional to the area of the object that interacts with and the “slapping” might simply be the inadvertent result
water. Therefore, power increases relative to drag if the body of a snake attempting to dive rapidly.
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undulations increased from anterior to posterior along the
length of the body. Many of these parameters were quite
similar to those of swimming eels.
In another study, Fabien Aubret and coworkers investi-
gated locomotion in young tiger snakes (Notechis scutatus)
that they raised for five months in either an aquatic or ter-
restrial environment. The snakes raised in water were able
to swim 26 percent faster, but crawled 36 percent slower,
than did their siblings that were raised without water for
swimming. Thus, swimming performance can be phenotypi-
cally plastic in these snakes, which are closely related to sea
snakes. Some have suggested that such plasticity might
have accelerated large-scale evolutionary transitions like
those from terrestrial to aquatic or marine environments.
Terrestrial Locomotion: Moving over

Varied Landscapes
The movements of swimming snakes are also quite relevant to
terrestrial locomotion, but the lack of buoyancy and nature of
the substrate add variation to the principles that are involved.
Gravity pulls downward on the mass of the animal, and the
resulting inertial forces and frictional interaction with the sub-
strate must be overcome in order to achieve forward move-
ment. It is amazing how effortless this appears when snakes of
Figure 3.8. Paddle-shaped tails of three species of sea kraits having various species are observed while moving in their native hab-
different aquatic tendencies are shown in the upper photo. From top
itats. There are several fundamental patterns of movement
to bottom these are Laticauda semifasciata, highly aquatic; Laticauda
laticaudata, somewhat amphibious; Laticauda colubrina, amphibious, that are observed in snakes, referred to as “modes” of locomo-
but spending considerable time on land. Note that the more highly tion, and most species are capable of switching their manner
aquatic species (L. semifasciata) has a somewhat broader tail in the of movement depending on the particular features of the envi-
dorsoventral plane, and it appears more muscular, presumably to ronment or, sometimes, the speed required. The movements
power swimming (see chapter 1 for further description of habits). The
of snakes are complex and may involve more than one manner
arrows point to the vent (cloacal opening) of each snake. Photograph
was taken at Orchid Island, Taiwan, by Coleman M. Sheehy III. The
of movement in different circumstances, or sometimes simul-
lower photo illustrates a relatively broader tail in a fully aquatic sea taneously in different regions of the body. There is recent evi-
snake, Acalyptophis peronii, photographed by the author in Australia. dence that progression of speed with movement can involve
The sea kraits are partly terrestrial, whereas this latter species is a changes in the mode of movement, similarly to changes of gait
“true” sea snake and is entirely marine. The sea kraits and true sea in terrestrial vertebrates with limbs, notwithstanding the bio-
snakes represent two independent lineages, so the similar paddle-
mechanical differences.
shaped tails in the two groups represent a nice example of convergent
evolution (see reading by Sanders et al., 2012).
Lateral Undulation
The more commonly familiar form of serpentine locomo-
Bruce Jayne has compared swimming performance be- tion is termed lateral undulation or horizontal undulatory pro-
tween an amphibious, nonconstricting semiaquatic snake gression. Some might also refer to this mode of movement as
(Nerodia fasciata) and a constricting terrestrial snake (Ela- “slithering,” for the body of the snake moves continuously
phe, = Pantherophis, guttatus). This comparison is of interest relative to the ground or substrate. This behavior makes for
because of differences in habits, number of ribs (Elaphe has effective escape reactions and also adds fun and challenge to
50 percent more total vertebrae than Nerodia), and other an- the act of catching snakes!
atomical features. Both species swam with similar waveform During lateral undulation the mass of the animal is sup-
and maximum speed, which ranged from 103 to 155 cm/s in ported by forces that are transmitted by means of the ven-
the larger snakes. The maximum forward velocity increased tral and lateral body surfaces, which are continually in
positively with increasing length of a snake in both species. contact with the ground and associated objects. The propul-
Also in both species the amplitude and wavelength of lateral sive forces, however, are exerted via the sides of the trunk.
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Beginning at the head, a series of undulant or wavelike
curves passes from front to rear, and the backward facing
surfaces contact and push against irregularities in the
ground surface (fig. 3.4). Whenever a bend of the body con-
tacts a surface object such as a rock or small hillock of soil, it
deforms locally to fit more closely around it and exerts force
against it (fig. 3.4). If the surface over which a snake moves
lacks these irregularities and has extremely low friction, the
snake cannot move forward and simply thrashes back and
forth in vain! However, most natural surfaces contain irreg-
ularities, and even very small ones that may not be obvious
to human observers will work. The entire body of the snake
slides past these sites, and the resistance forces are exerted
at these points (fig. 3.4). These are variously called contact
zones, reaction sites, push points, or sites of resistance.
During lateral undulation the head of the snake pushes
off an uneven part of the ground, and each succeeding
body part follows where the head left off. Each part of the
body progressively follows the direction of the head. The
snake travels forward, each point along the body moving at
constant speed following a more or less sinusoidal path.
The snake produces thrust by bending continuously around
each point of contact, thereby shifting it to more posterior
segments of the body. The waves of bending are propa-
gated posteriorly such that they push laterally and poste-
riorly against the reaction sites on the surface of the
substrate. When a snake pushes against multiple reaction
sites simultaneously, the vectors of force that act laterally Figure 3.9. Schematic illustration of muscle activity (gray color)
cancel each other, and the resultant vector propels the during lateral undulation in snakes. The snake at the left is crawling on
snake forward. That is, the summation of these reactive a smooth surface with pegs provided for resistance sites (dark circles).
forces produces a net forward thrust (figs. 3.4, 3.9, 3.10). The snake to the right is swimming in water. The undulations are
traveling from head to tail, and the onset and offset of activity is
Each bend pushes against an object, and then slides out of
indicated by the posterior and anterior boundaries of the shaded areas,
contact with it. respectively. The drawings are based on information from
The lateral undulations are created by alternating waves of electromyography of major epaxial muscles. For both types of lateral
muscle contraction that progress from the neck toward the undulation, muscle activity is propagated posteriorly, and at a given
tail. Such movement requires precise neuromuscular coordi- longitudinal location muscle activity occurs only on one side of the body
in an alternating fashion between the left and right sides. For terrestrial
nation. The propulsive forces due to the snake pushing
locomotion, the muscle activity along the entire length of the snake
against the resistance sites are generated by the axial muscles begins at maximal convexity and ends at maximal concavity with
(fig. 3.3). Such forces pass perpendicular to the contact sur- respect to the side of the active muscle. By contrast, during swimming
faces. Because all of the body is in constant motion, frictional the timing of muscle activity relative to bending shifts along the length
forces at the resistance sites and the substratum induce of the snake because the speed of propagation of muscle activity
forces that oppose the forward motion. Therefore, progres- exceeds the speed of propagation of lateral bending (as also occurs in
the swimming of fishes). Drawings by Jason Bourque, Florida Museum
sion by means of lateral undulation is facilitated by low-fric-
of Natural History, after fig. 18 in B. C. Jayne, Muscular mechanisms of
tion surfaces so long as there are points for resistance snake locomotion: An electromyographic study of lateral undulation of
contact. The ventral scale surfaces are designed with a mor- the Florida Banded Water Snake (Nerodia fasciata) and the Yellow Rat
phology and orientation to reduce friction that opposes the Snake (Elaphe obsoleta), Journal of Morphology 197:159–181, 1988.
direction of forward movement (see figs. 5.9, 5.13). This as-
pect of a snake’s scale design is evident if one runs a hand
both forward and backward along the belly of a snake and As the animal moves, it senses irregularities while it is in
compares the frictional resistance with similar movements motion, and the curves of the body are forced into contact
over the back of the snake. The hand slides more easily in the with variously spaced resistance sites wherever they are en-
front-to-rear direction along the belly. countered. In many cases, the head of the snake is elevated
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peg and reverse its curvature anterior to it
(fig. 3.9). Most of the force that is directed
against a peg is produced by the muscles
in the bend of the body contacting the
peg, rather than by the muscles in distant
bends. The extent of bending around a
peg and the reversal of curvature anterior
to the peg determine the direction of
force exertion and the consequent move-
ment that results.
The mechanical features of the snake’s
body result in relatively low curvature
(that is, a long radius) of the vertebral col-
umn around each peg, while the body wall
exhibits greater (short radius) but asym-
Figure 3.10. Forces generated by snakes using variable numbers of pegs for lateral metric curvature around the peg. The sharp
undulation movement across a flat surface. Each arrow represents the reaction force bends around resistance sites involve
exerted by the peg against the body of the snake, which is equal and opposite to the complex movements produced largely by
force exerted by the body of the snake against the peg. The length of each arrow
the epaxial muscles. The higher curvature
indicates the relative magnitude of the reaction force. The sum of the reaction forces
has a net forward component that contributes to the forward progression of the snake.
of the body wall around the anterior
With increasing number of pegs, the energy lost to lateral forces increases. Longer surface of each resistance site appears to
snakes have a greater array of contact sites to utilize and should be able to contact involve a suite of factors including the ver-
three or more points more often than can shorter relatives. Hypothetically, there is likely tebral curvature, possibly axial torsion,
to be an optimal number of contact points for any particular size snake that maximizes and movements of the ribs and body wall.
the forward movement for any output of energy. Drawing by Jason Bourque, Florida
The forces exerted by a laterally undu-
Museum of Natural History, and after fig. 9.5 in J. L. Edwards, chapter 9 in M.
Hildebrand, D. M. Bramble, K. F. Liem and D. B. Wake (eds.), Functional Vertebrate lating snake must be sufficient to bend the
Morphology (Cambridge: Belknap Press of Harvard University Press, 1985). body laterally, push its sides against ver-
tical surfaces at reaction sites, and over-
come resistance due to lateral and ventral
and carried off the substrate as the body moves. Raising the sliding friction (roughly equal to the mass of
head involves a cantilevering action, and the axial muscula- the snake multiplied by the coefficient of friction). The term
ture shifts the weight of the elevated part toward the region sliding friction refers to a resistance to motion that is gener-
of the body that remains in contact with the ground. ated at a point (or area) of contact between two surfaces that
Studies of snake locomotion generally involve a combina- are in motion. The body curvature and the activity of muscle
tion of motion analysis (called kinematics) and measurements units increase in response to increased resistance to forward
of the electrical activity of muscles (called electromyography, motion that might be acting on a snake. Experimentally, the
abbreviated EMG). The latter is accomplished by means of addition of mass to a snake increases the resistance it must
placing electrodes in specific muscles and recording the timing overcome to move itself forward, and therefore increases the
and intensity of their activity. Most of these studies have in- force that is required for propulsion. The increased force that
volved snakes that are moving by means of lateral undulation. is exerted by the snake can be judged from the increased
In such movements, the epaxial muscles are activated sequen- muscle activities indicated by the EMG. One other feature of
tially along the body such that waves of muscle activity propa- muscle activity seems to be important. The axial muscles are
gate along the trunk in a posterior direction. The timing of activated immediately before, or when, they become stretched
such muscle activity is consistent with the shortening of to maximum, and they are deactivated when they reach either
muscle units and the formation of bends in the snake. resting length or maximal shortening.
Some studies of snake locomotion have employed snakes Early studies suggested that progression by lateral undu-
that are observed while moving over a flat, smooth surface lation is most stable with at least three contact points,
with vertical pegs that are provided as the sole resistance hence posteriorly directed vectors. More recent studies
sites (fig. 3.9). When snakes are moving among pegs, muscle have shown that the mechanism of propulsion by lateral un-
activity on the side of the animal opposite the point of con- dulation also works with one or more contact points, al-
tact pushes the snake’s body against the peg. The activity of though parts of the body can tend to slip sideways more
the muscles causes the vertebral column to bend around the when there is just a single contact point. Situations in which
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snakes cannot find one or more stable contact points cause I believe it is fair to conclude that the movements of un-
the snake to shift to a different mode of movement, such as dulating snakes in many habitats arise from a combination
sidewinding or concertina locomotion (see below). Increasing of features that are observed when a snake in the laboratory
the number of contact points increases both friction and moves among pegs or when it slithers over a featureless
the laterally directed forces relative to the forward directed terrain. Some functional morphologists also speculate that
forces. However, investigations involving snakes that are snakes might dynamically change their frictional interac-
crawling on a smooth surface having intermittent vertical tions with the surfaces over which they crawl by actively
pegs indicate there are two advantages associated with mul- adjusting the attitude or orientation of the belly scutes.
tiple points for propulsive contact. First, contact with mul- Lateral undulation is commonly employed by numerous
tiple pegs enables the cancellation of lateral force vectors terrestrial species of snakes and is often used in combination
over an extended length of the body, and this stabilizes the with other modes of locomotion. Undulating movements are
body against lateral slippage. Second, contact with multiple seen in the graceful and dramatic crawling of swiftly moving
pegs reduces the curvature around each individual peg (fig. species such as racers, whipsnakes, or brown snakes, and are
3.10). These two effects seem to facilitate higher speeds of also used by snakes such as mambas and vine snakes to climb
travel with less lateral slippage, but to a limit. When the over objects or to move in three-dimensional habitats of
contact points are very numerous, the lateral vectors be- bushes and trees. The slender appearance of many terrestrial
come relatively larger and the friction increases—which and arboreal species is well suited to undulatory progression,
means losses of energy and a reduction in speed. Fast- but this mode of movement likely becomes less efficient and
moving snakes such as racers and whipsnakes characteristi- more difficult in stouter and heavier species. While snakes
cally move with fewer long and shallow bends in the body, that are undulating appear to move very quickly and may
rather than numerous shorter and deeper bends. well escape someone who is in pursuit, the maximum veloc-
Recently, David Hu working with collaborators in mathe- ities measured in swiftly crawling snakes such as racers and
matics has investigated undulating locomotion (“slither- mambas are around 12–13 km/h (3.33 to 3.61 m/s) and some-
ing”) of snakes on strictly flat surfaces. The team used video, what less in other species such as garter snakes. Research
mathematical models, and measurements of the frictional investigations by Bruce Jayne and Albert Bennett have
properties of snake skin to evaluate the mechanics of slith- shown that rapid but usually brief locomotion (called
ering locomotion. When a snake is undulating over a “sprint”) increases in speed (m/s) with increasing body
smooth, flat surface, it dynamically distributes its weight so length of snakes, except for the larger snakes tested. These
that its belly presses against the substrate and periodically same investigators also demonstrated that the inherent
“loads” its weight at specific points of contact where the sprint speed of individual garter snakes is correlated with
ventral scutes press against the surface. These points of their survival in nature, except during the first year of life.
weight loading are where the body has zero curvature. The Lateral undulation in snakes appears to be highly special-
snake’s body may remain in contact with the substrate all ized and provides a unique propulsive system that uses
along its length, but the weight distribution is nonuniform. marvelous control of body muscles. Limbless lizards, in
During more rapid locomotion, segments of the body are al- comparison, cannot as effectively maintain contact with a
ternately lifted off and then onto the substrate. Whereas the push point or resistance site as the body travels forward sliding
body undulates from side to side, the center of the snake’s along a push point. Lizards often push against the resistance
mass moves constantly in the forward direction as sliding site for a short distance and then slip laterally out of contact
friction is used to generate propulsive forces and exceeds the with it, whereas snakes can keep the body in contact with, and
inertial forces by an order of magnitude. The inertial forces pushing against, the resistance site until they push off of it
attributable to the sideward undulations are balanced by the with the tail. The local adjustment of curvature around an
sum of sliding frictional forces in addition to the forces gen- object or point of contact represents exquisite sensory control
erated by the internal muscles of the body. One important of muscles and appears to be a unique characteristic of snakes.
property of ventral scales that Hu and his team discovered is
that friction, or resistance to movement, is highest when a Concertina Locomotion
snake is sliding sideways, rather than forward. The increased This mode of snake locomotion utilizes stationary body parts
sideways friction seems to be necessary for forward move- as anchors to push or pull the remaining body forward
ment across bare terrain that lacks rocks or other objects as (fig. 3.11). Static friction associated with the stationary part is
push points. Other biomechanical studies have demon- used as the reaction force to enable forward progression. This
strated that nanoscale geometric surface features of scales arrangement works so long as muscular-induced forces do
impart low friction for forward movement, but are an effec- not exceed the static friction force. Therefore, neuromuscular
tive stopper for backward motion (see also chapter 5). control during concertina locomotion is very important. The
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While moving forward, a snake using
concertina movement alternates an-
choring with folding, then anchoring
with extension, and so on. One part of the
body anchors against the substrate or
tunnel wall while a body segment immedi-
ately behind folds like an accordion to
“pull” that part of the snake forward. Once
forward, a part of the snake posterior to
the original anchor being considered then
again anchors the body and the segment
immediately in front extends the folded
body forward. These actions are repeated
along the length of the snake and alter-
nately in time. The snake alternately pulls
its body into bends and then straightens
out the body forward from the bends.
Some have compared this locomotion to
snakes taking steps. Mean velocities asso-
ciated with concertina locomotion are
Figure 3.11. Schematic representation of hypothetical snakes engaged in concertina around 0.1 km/h (2.78 cm/s) or less de-
locomotion, one inside a tube or burrow (left) and one moving over a flat surface (right). pending on the attributes of the environ-
In each case the snake progresses from right-to-left (anterior direction) by anchoring part ment (tunnel width relative to snake, etc.).
of the body against the interior of the burrow of against the ground surface, extending
Concertina movement can be used in
the body anterior to the anchored segment of snake, then anchoring the anterior part of
the body and pulling the posterior body toward the newly anchored segment. The
three dimensions and is often used by ar-
shaded part of each snake represents the anchored segment of body. Sequences are boreal snakes on tree limbs or branches, as
stopped in time progressively from bottom to top of each drawing (arrow). Progression of well as by fossorial or terrestrial species
the snake in the burrow involves bending of the internal axial skeleton. Drawings by moving in burrows. Having one part of the
Jason Bourque, Florida Museum of Natural History, after fig. 9.7 in J. L. Edwards, chapter body anchored can be a very advantageous
9 in M. Hildebrand, D. M. Bramble, K. F. Liem and D. B. Wake (eds.), Functional
thing when crawling over objects that
Vertebrate Morphology (Cambridge: Belknap Press of Harvard University Press, 1985).
are thin, capable of movement, and poten-
tially unstable. Also, the static friction
force of friction is related to the product of the friction coef- force can be increased by muscular effort as in constricting
ficient (characteristic of the properties of the substrate) mul- around branches (fig. 2.20). When crawling in burrows,
tiplied by the mass. Therefore, the mass of the snake must be snakes can use multiple sites for anchoring the body, and
sufficient to induce an adequate reaction force. On the other static friction can be employed by lateral as well as ventral
hand, as the body mass increases, so does the sliding friction surfaces of the snake. The confining space limits the ampli-
associated with the moving part of the snake, and so does the tude of flexions, and therefore a greater number of flexions
effort that is required to lift the body. When a snake is are typically used. This could be energetically more expen-
moving through an earthen tunnel, or burrow, the snake ac- sive and diminishes the endurance of the snake when crawl-
tively pushes against the sides of the tunnel to provide a ing distances through subterranean tunnels.
static anchor. Considerable muscular force might be gener- Both concertina and lateral undulation locomotion are
ated in anchoring the body against the walls of the burrow, so probably difficult for snakes that are both short and stout.
the energetics of concertina locomotion inside a burrow is In these cases, either rectilinear or sidewinding locomotion
likely to be different from that of a snake that is moving on a usually compensates for the disadvantages.
flat surface. Concertina locomotion on a flat surface outside
a burrow is often mentioned or illustrated in review articles Rectilinear Movement
and books, but in fact it is rarely observed. Recently, Mat- This term refers to straight-line motion, which in snakes in-
thew Edwards and the author uncovered a secretive blind volves comparatively slow forward progression powered by
snake (Leptotyphlops ater) beneath a stone in Guanacaste, muscles and movements of the belly scales. Such movement
Costa Rica. This small snake made repeated attempts to crawl relies on flexibility of the integument and the use of muscles
away using concertina movements. that are bilaterally symmetric (fig. 3.12). The belly scales are
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alternately lifted somewhat from the sub-
strate and pulled forward, then positioned
downward and pushed backward. When
the ventral scales are in static contact with
the substrate, the body is actually pulled
forward over them. The cycle repeats when
the body has moved far enough forward to
stretch the scales. Thus, groups of ventral
scales are alternately placed in static con-
tact with the ground followed by local ac-
tive stretching that extends the ventral
body wall somewhat like that of an inch-
worm. These movements occur simulta-
neously at several points along the body.
The dorsal surface of the snake progresses
at a constant velocity, and the continual
movement of mass conserves momentum.
But the movement is slow and typically
characteristic of heavy-bodied snakes such
as vipers, boas, and pythons, although
probably all snakes are capable of such pro-
gression. Instead of the body undulating
gracefully back and forth across the
ground, the snake moves in a nearly
straight line and appears to be powered by
some unseen force. The progression of the
animal can be very precise, quiet, and
rather amazing to watch. Figure 3.12. Schematic illustration of features in rectilinear locomotion by a
The principal muscles employed in rec- hypothetical snake. The costocutaneous muscles connect the ribs with skin and
tilinear locomotion involve the costocuta- impart forces involved in moving the snake forward from left to right in the figure. The
neous muscles that run between the ribs ventral costocutaneous muscles anchor the ventral scutes in contact with the ground,
and successive scutes are recruited in this manner to the region of ground contact
and the skin (fig. 3.12). One set of inferior
(upper to lower figure). These scutes provide a zone of resistance points against
muscles at a particular point along the which the muscles can act to move the snake forward. The ventral costocutaneous
body pulls on the ventral scales and an- muscles associated with the contact zone act to pull the ribs and vertebral column
chors them to the ground, thereby pro- forward, while the dorsal costocutaneous muscles act to lift the ventral scutes in
viding a pivot point against which other advance of the contact zone and to pull them forward. The actions of both sets of
muscles impart a continuous momentum to the vertebral column, and the dorsal
muscles can act. Similar muscles immedi-
body of the snake moves steadily forward. Several different ventral parts of the snake
ately posterior to this point pull the verte- alternately fix to the substrate, then lift out of contact and quickly accelerate
bral column forward and simultaneously forward to “catch up” with the dorsal part of the body. The ventral scutes are
add their affected ventral scales to the alternately lifted and pulled forward, then pulled downward and backward. The
pivot site. Another set of superior mus- flexibility of the skin is important to these actions. Drawing by Dan Dourson, modified
cles anterior to the pivot site acts simulta- from fig. 3.34 in C. Gans, Biomechanics. An Approach to Vertebrate Biology
(Philadelphia: J.B. Lippincott, 1974).
neously to lift the local scales off the
substrate and pulls them forward of the
pivot site. The result is that each of several pivot sites moves scales are alternately lifted and pulled forward, then pulled
posteriorly along the body of the snake. The sequential con- downward and backward. Flexibility of the skin is of para-
tractions of the muscles impart a continuous momentum mount importance here. As in the other modes of locomo-
to the vertebral column, imparting the steady forward tion, if one observes a snake crawling in this fashion—and
movement of the dorsal body of the snake. Simultaneously, especially a heavy snake—it can be seen that the ventral
the ventral part of the snake alternately fixes to the sub- scutes and segments of the snake respond to irregularities
strate, then lifts out of contact and quickly accelerates for- in the substrate such that the detailed pattern of the scute
ward to catch up with the dorsal side of the body. The belly movements is dynamic and variable.
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as its body pushes sand into a small ridge,
for example (fig. 3.14). Movement of the
snake creates vertical and posteriorly di-
rected pressure against the ground, which
produces the reaction force and moves the
snake forward without slippage or sliding.
Sidewinding movements utilize axial
muscle units in ways that are fundamen-
tally similar to those studied in lateral un-
dulation, except that some muscles are
activated bilaterally in the regions of
trunk that are lifted off the substrate.
A key aspect of sidewinding locomotion is
the ability of the snake to transfer the sup-
port of its mass to the body segments that
progressively contact the substrate. Such
actions depend on exquisite control of the
axial musculature. Compared with other
Figure 3.13. Schematic illustration of the progressive movements of a Sidewinder
snakes, species that specialize in side-
Rattlesnake (Crotalus cerastes), moving by sidewinding in a direction toward the top of
the illustration. The shaded portions of the body are in contact with the substrate winding (e.g., Crotalus cerastes) possess
(sand), and the open portions of the body are lifted above the substrate. At any fewer vertebrae and shorter segments of
moment, the snake typically has two parts of its body in contact with the substrate and axial musculature, and are relatively small
two parts lifted above the substrate. See text for further explanation. Drawing by Jason and moderately stout with short tails.
Bourque, Florida Museum of Natural History, after fig. 9.8 in J. L. Edwards, chapter 9 in
Because sidewinding involves lifted
M. Hildebrand, D. M. Bramble, K. F. Liem, and D.B. Wake (eds.), Functional Vertebrate
Morphology (Cambridge: Belknap Press of Harvard University Press, 1985).
segments of the body, the laterally di-
rected forces produced at each contact site
are unbalanced and the snake moves later-
Sidewinding ally as well as forward. Sidewinding
This form of locomotion is well known and has been some- snakes leave characteristic tracks that appear as a series of
what romanticized in context of western movies and various short separated impressions set at roughly 30° angles from
tales of life challenges in the desert. One immediately thinks the direction of movement. The ends of the individual im-
of the Sidewinder Rattlesnake (Crotalus cerastes), but other pressions consist of a “J” on one side, formed by the head and
desert vipers of Africa and Asia (as well as some other spe- neck, and a “T” on the other side, formed by the tail. The di-
cies) also employ sidewinding as a means of moving over rection of movement is indicated by the hook of the J, and
flat, smooth, or slippery surfaces. Homalopsid snakes, for fresh impressions allow one to easily follow the movements
example, might employ sidewinding to move over mudflats, of a snake (fig. 3.14).
and various diurnal snakes can behave similarly when lifting Studies by Bruce Jayne and Stephen Secor have confirmed
the body off of excessively warm ground. Various surfaces a long-held conjecture that sidewinding is mechanically
can be of either lesser or greater frictional resistance, and proficient and conserving of energy. Probably all midsized
sidewinding locomotion can still be employed. snakes are capable of sidewinding, but only desert vipers and
Sidewinding progression involves a snake lifting the certain homalopsid species appear to be specialized to rou-
head and moving the anterior body forward, placing it in tinely employ this mode of locomotion. Maximum speeds of
static contact with the substrate. While both head and tail sidewinding snakes are around 3.7 km/h (about one m/s).
are anchored in static contact with the ground, the middle
section of the body is lifted forward and essentially “rolls Slide-pushing
out” against the substrate from that point. The neck is then This is a mode of terrestrial locomotion that involves vigorous
curved, lifted, and moved forward again to repeat the action undulations and sliding of the body. It is functionally inter-
(fig. 3.13). During these movements the trunk of the snake mediate between lateral undulation and sidewinding, and is
may become bent in more than a single plane. The mecha- also similar to undulating motions of snakes when swimming
nism of movement involves static friction and irregularities in water. The term is attributable to Carl Gans, who described
in the substrate, which are either present as a passive fea- this as a separate mode of locomotion although it may well
ture of the physical environment or are created by the snake employ elements of the other two modes just mentioned. An
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Figure 3.14. Tracks in sand made by a Sidewinder Rattlesnake (Crotalus cerastes) that moved up a mound of sand in the direction of the
arrow. The snake was found coiled beneath a shrub at the top of the mound. These tracks are particularly deep as the snake had to exert
considerable force against the sand in order to sidewind uphill. This trackway was photographed by the author in the Anza-Borrego Desert
of Southern California.
alternative and very descriptive name for this movement is coefficient of friction and experience somewhat less slippage
slipping undulation. Picture a snake that is attempting to crawl at right angles to the longitudinal axis of the body. The resis-
either by lateral undulating movements or by sidewinding tance to slippage is proportional to the product of the fric-
movements, except that the substrate has very low friction tion coefficient and the mass, which are both usually greater
and the body of the snake slides backward as it attempts to at the posterior end of the snake. Slowly this moves the
push against reaction sites. What happens is the posterior snake forward over a low-friction surface, often at an angle
contact zones slide backward relative to the ground at several to the direction it is facing. The principal difference between
times the forward velocity. The snake does move forward, but this mode of movement and that of lateral undulation is
at a slow rate. The head and neck travel forward at a relatively that the posterior reaction zones are fixed in an “undulating
steady pace, while the head swings back and forth less so than snake,” but they move backward in the case of slide-pushing.
the trunk. Slide-pushing is comparatively inefficient, for it in-
The propulsive forces used in slide-pushing involve local volves many more undulating movements per unit of for-
force application by rapidly traveling waves of the snake’s ward progression than occurs in a lateral undulating
body. As the surfaces contact the ground, sliding friction is snake. Rather than considering this to be a specialized,
induced, but with an asymmetry. Anteriorly, the scales of evolved mode of movement, it should perhaps be regarded
the ventral body contact the ground. Posteriorly, there is simply as an exaggerated attempt at movement when
torsion of the body and the ground contact also involves the conditions of the substrate become poorly suitable for
sides of the trunk. The dorsolateral scales have a higher limbless locomotion. This mode of movement is used by
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various snakes when moving on slippery surfaces, or
during initial attempts to rapidly escape a potential
threat. An example might be the terrifying sight for some
people who might encounter a snake in their house, and
when disturbed the poor animal attempts to escape by
wriggling and slipping across a slick floor such as lino-
leum. Such a snake appears frantic and probably much
larger than it actually is when the story is told to a neigh-
bor. Or the misunderstood animal is interpreted as at-
tacking the resident, should the observer accidentally get
between the snake and the shelter it is seeking.
Other Specialized Behaviors in

Terrestrial Locomotion
Burrowing
Many snakes live in burrows or utilize subterranean tunnels
for refuge from weather and predators. A variety of cav-
ernous underground spaces are used for “denning” or over-
wintering when snakes seek refuge individually, or they
form social aggregations consisting of tens or hundreds of
individuals. In many cases, snakes share burrows with other
animals, or they construct their own. Snakes that truly
burrow usually exhibit a number of morphologic specializa-
tions including modified heads and rostral scales, shovel-
like snouts, and tails with roughened or spiked scales
(fig. 3.15; see also figs. 1.11–1.16, 1.20, 1.24, 1.49). Burrowing
is accomplished by “wiggling” or “plowing” through loose
Figure 3.15. The head of the Mexican Burrowing Python,
soil and sometimes scooping dirt laterally with the enlarged
Loxocemus bicolor, exhibits a strong, countersunk jaw (upper photo)
rostral scale. The rough tail is used to anchor the body that is used for burrowing in tunnels and animal burrows. The lower
during these movements, or to plug the burrow and prevent photo shows the snake with its head and neck in soil as it begins to
the entry of unwanted guests. Head modifications usually burrow. This species enters tunnels and nesting sites of iguanas
involve reinforced buttressed skulls to absorb the forces where it feeds on their eggs. Both snakes are different specimens that
that are generated during digging. were photographed by the author in Guanacaste, Costa Rica.
Certain snakes such as uropeltid and probably typhlopid

species employ a special type of concertina locomotion in
burrows and crevices only slightly larger in diameter than involves propulsion by means of reaction forces attributed
the body of the animal. These snakes bend the vertebral col- to all surfaces of the animal that might contact sand grains
umn separately from the outer parts of the body, which can during undulating movements, as in swimming. Snakes
be expanded to contact the wall of the burrow or crevice. that engage in this behavior with regularity possess valvu-
Such contact provides sites of stable support, allowing the lar nostrils to prevent the entry of particles when breathing,
axial core of the body to move forward (or backward) rela- and concave bellies that prevent the filling of spaces around
tive to the contact sites which, in turn, are repositioned to the snake so the body can expand and contract during lung
produce forward movement (fig. 3.11). inhalation and exhalation of air. Breathing by means of ver-
Snakes that occur in habitats with desert sands either tical movements is common in sand-swimming reptiles and
utilize burrows made by other animals (e.g., Sidewinder also in rock-dwelling forms. Kenneth Norris and Lee Kava-
Rattlesnakes use rodent burrows) or move beneath the nau investigated burrowing behaviors of the Western
sand in a manner that resembles swimming. Sand swim- Shovel-nosed Snake (Chionactis occipitalis) and observed
ming enables snakes to move through sand without form- that during active burrowing the head was bent slightly
ing a tunnel due to the loose nature of the collective sand downward, and the overhanging rostral scale created a
grains. This manner of movement is not well studied but cavity that was free of sand. This snake breathes while in
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Figure 3.16. A Sidewinder Rattlesnake (Crotalus cerastes) partially cratered in desert sand beneath a creosote bush at Borrego Valley,
California. Note the close camouflage match between the snake and the surrounding sand. The “horns” over the eyes keep them free of sand
when the snake is buried more deeply. This is a common “ambush” behavior of this species of snake, which feeds on rodents and lizards.
Photograph by the author.
sand by vertical movements of the gular region that is lo- defensive actions. The behavior is not common, as most
cated in this sand-free cavity near the head. snakes prefer to anchor the body when striking at prey or a
A modified mode of burrowing occurs in a behavior that potential predator. An actual “jump” involves a vigorous
has been termed “cratering.” Desert vipers will coil on the strike in which the momentum of the accelerated head and
surface of sand and, by continually moving the body while anterior trunk carry the attached body momentarily off the
remaining in a coiled posture, gradually displace the sand be- ground. Sometimes particularly agitated snakes will slide or
neath while the snake “sinks” gradually downward into the jump forward during strikes that occur while the animal is on
substrate. With enough effort such snakes can bury them- unstable or down-sloping substrate. Some species such as Af-
selves completely, but they usually leave the eyes exposed rican Horned Adders (Bitis caudalis) and jumping pit vipers
and may use the position as an advantage for ambushing (Atropoides spp.; fig. 1.36) characteristically spring forward
prey that might wander near unknowingly (fig. 3.16). Cot- into the air during vigorous strikes that comprise a defensive
tonmouths and probably other snakes sometimes crater strategy. In other cases, smaller snakes may catapult into
themselves deeply into leaves or other debris in response to the air during frantic strikes or escape behaviors, and some
cool or falling temperatures. arboreal species may purposely leave their substrate during
launches into aerial descents (see below).
Jumping A very interesting aspect of snake behavior is that some
Amazing as it sounds, although snakes are without limbs species and individuals may exhibit exaggerated aggression
some species or individuals can actually “jump” during certain if someone is in the way of a snake that is escaping from
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disturbance in a particular direction. Bruce Means has Many terrestrial snakes, and arboreal species in particular,
termed this “blocked-flight” aggression, during which a have a remarkable ability to cantilever, or to extend the
snake may raise its head, flatten its body, mouth-gape, anterior body horizontally without support. Some gracile
strike, and sometimes “jump” toward a person if he or she and arboreal species (e.g., vine snakes and the like, figs. 1.48,
is blocking the flight path of the animal. 1.51) are able to extend the body to more than 50 percent of
its length when bridging gaps in vegetation or substrate
(fig. 3.17). Amazingly, one of the recent observations from
Life in the Canopy: Climbing and Gliding Bruce Jayne’s laboratory is that some individual Brown Tree
Life and movement in arboreal habitats is challenging for a Snakes (Boiga irregularis) are able to support nearly 90 per-
variety of reasons. Probably the majority of snake species that cent of their snout-vent length in air above a supporting
are said to be arboreal also move on the ground during for- perch before making contact with a second destination perch
aging, nesting, dispersing, and other behaviors; therefore the directly above the supporting perch! Studies in Jayne’s labo-
presence in a canopy is transient or cyclic, but not permanent. ratory have shown recently that snakes are able to cross larger
However, some species of snakes are highly arboreal and are gaps when there is a vertical component of the gap distance
typically found (most of the time) above ground in shrubbery relative to strictly horizontal distance. When the gap has a
or trees. On the other hand, there are numerous snakes that vertical component (i.e., higher or lower than the level of the
are terrestrial and ground-dwelling, but readily climb into veg- snake’s starting perch), gravity acts over a relatively shorter
etation for a variety of reasons including basking, foraging, horizontal distance, and this enhances a snake’s ability to
escape from predators, and so on. In the New World, a variety produce sufficient muscular force to prevent buckling.
of whipsnakes, racers, and rat snakes readily take to trees and Juvenile snakes are able to cantilever better than can
can move swiftly through above-ground vegetation. Similarly, adults of the same species, presumably due to a lower mass
Old Word rat snakes, mambas, and some cobras perform sim- relative to the length of body. While features of muscle and
ilar feats. There are a number of snake species in which the
young are highly arboreal, but switch to a more ground-dwell-
ing existence as they grow older and longer. The switch could
be related to predator avoidance, prey-switching, or the fact
that vertical postures are less stressful on the cardiovascular
system if the body—hence blood column of the major arteries
and veins—is short rather than long (see chapter 6).
In terms of locomotion, movement through vegetation or
upon branches requires precise neuromuscular coordination
and the ability to sense whether smaller, unstable branches
can support the mass of the climbing snake. A variety of
movements is used, primarily lateral undulation in combina-
tion with concertina and, more rarely, rectilinear progression.
Currently, detailed investigations of climbing behavior and
mechanics in snakes are being carried out in the laboratory of
Bruce Jayne at the University of Cincinnati. Some of the new
findings indicate that Corn Snakes (Pantherophis guttatus)
and Boa Constrictors (Boa constrictor) characteristically per-
form a variant of concertina locomotion with periodic stop-
ping and gripping when moving horizontally or uphill on
cylindrical perches. If pegs are present on cylindrical perches,
the added resistance sites elicit lateral undulation and in-
creased speed of movement. Maximal speeds are greatest on
perches of intermediate diameter that approximate the width
of the snake. The forward velocity decreases when either the
incline or diameter of a perch increases, and the snakes are
not able to move, either uphill or downhill, when large-diam-
Figure 3.17. A Grenada Bank Tree Boa (Corallus grenadensis)
eter perches are experimentally inclined to 45° or 90°. These illustrating a dramatic extension of the body in air, while the posterior
studies indicate that balance, grip, and the “fit” to a perch all tail and body are anchored to a tree. Photographed in Grenada by
can limit the ease of climbing on perches. Richard Sajdak.
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skeletal features of a snake’s vertebral column are generally for longer periods of time. Overall, the arboreal snakes were
conserved in evolutionary terms, several modifications of superior to their terrestrial relatives in climbing abilities, but
vertebrae and associated epaxial muscles and their tendons the terrestrial species won out when it came to crawling
appear to be related to cantilever performance. Arboreal performance over horizontal ground. Rozar suggests that
snakes are generally slender with low relative mass and a there might be “trade-offs” in the proficiency of locomotion
compressed body form compared with strictly ground- in the two habitats related to the specialized morphology
dwelling relatives (figs. 1.31, 1.48). A large number of arbo- that is characteristic of many arboreal species of snakes.
real species are relatively short compared with nonarboreal
relatives, and the body exhibits lateral compression (fig. Straight Up and Down
1.51). Additionally, some arboreal boas and vipers possess Probably in most circumstances snakes climbing or moving
ribs that are directed downward rather than outward, through vegetation are nearly horizontal and use “switch-
thereby rendering the body to be narrow, yet deep, in cross- backs” (like roads coursing up a mountainside) to change
section. These features assist a snake to extend its body elevation. However, there are instances where snakes climb
horizontally without undue downward displacement of using a fully vertical posture. One example is the climbing
muscle to form a dorsally convex vertebral arc. by New World rat snakes straight up the trunks of pine
Aspects of arboreal locomotion have also been studied re- trees. These snakes might climb vertically to heights in the
cently by Ron Rozar at the University of Miami. He investi- tens of meters, and one reason for such ascent is to forage
gated movement behaviors and performance in eight pairs of for eggs or chicks in bird nests. The fully vertical position of
taxonomically related species having terrestrial and arboreal the snake challenges the blood circulation, and this is dis-
relatives. He demonstrated that the arboreal species were cussed further in chapter 6. Additionally, the snake must
generally superior in their abilities to bridge gaps and to trav- find irregularities on the tree surfaces where it can engage
erse narrow-diameter perches. The arboreal species were also resistance sites for production of thrust.
found to have greater climbing endurance than their terres- People have sometimes asked me how such climbing
trial relatives; that is, they could sustain climbing movement snakes come down from the tree. The answer to this question
Figure 3.18. A Yellow Rat Snake (Pantherophis obsoletus) clinging to a pine tree in central Florida. It is not clear whether snakes are able to
proficiently move downward on such a tree trunk, or whether they simply fall (purposely) to the ground. Photograph by Mac Stone.
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is not clear. It is possible for snakes to climb down trees
using the same features of the tree surfaces that are used in
upward movement, or sometimes snakes simply fall to the
ground (fig. 3.18). No one knows the intentions of snakes in
these circumstances, but purposeful “dropping” could have
been a behavioral precursor to the launches of gliding
snakes that are discussed next.
Gliding
Perhaps the most remarkable behavior of moving snakes is
that of gliding. While numerous cylindrical animals swim
through water, “flying” snakes of the genus Chrysopelea are
the only limbless animals that glide through air. Most an-
imal gliders, such as flying squirrels or tree frogs, use static
structures such as paired, outstretched “wings” to generate
lift during gliding, but snakes have no appendages to create
the wings or to assist with control during aerial movements.
Yet gliding that has been studied in the Paradise Tree Snake
(Chrysopelea paradisi) is on par with that of other gliders
and demonstrates remarkable control over the direction of
descent. This snake is a colubrid species that lives in tropical
forests of Southeast Asia. Evidently, it engages flight pri-
marily for escape, or to chase prey, or simply to glide from
tree to tree (fig. 3.19). Remarkably, Paradise Tree Snakes can
take off by jumping, maintain a stable glide path, maneuver
while in gliding flight, and land safely without injury.
The kinematics of this “flying snake” was investigated in
detail by John (“Jake”) Socha while he was a graduate stu-
dent at the University of Chicago. He determined the entire
three-dimensional gliding trajectory of wild-caught Chryso- Figure 3.19. Photographs of a Paradise Tree Snake (Chrysopelea
pelea that were videotaped when jumping from a horizontal paradisi) in various stages of gliding. The upper left photo shows a
branch at the top of a 10-meter-high tower in an open field dorsal view of a snake just after it has “launched” itself from an
arboreal perch. The other images illustrate the extremely flattened
at the Singapore Zoological Gardens. The snake prepares for
shape of the snake during gliding, both dorsal and ventral views.
“take-off ” by hanging from a branch with the anterior body Photographs are by Jake Socha.
looped into the shape of a J. It then jumps by accelerating
up and away from the branch; simultaneously it straightens
and flattens the body dorsoventrally. The body width nearly presumably requires neuromuscular control that is quite spe-
doubles, and the ventral surface becomes slightly concave cialized. John Socha has suggested that mobility and control
in shape. Dorsoventral flattening is one of the key features of rib movements that are necessary for holding body shape
of the gliding behavior of snakes (fig. 3.19). during undulation might have originated in relation to fine
As the snake pitches downward and increases in speed, grip control that is involved in climbing vegetation. The high
the head and tail are drawn laterally toward the midpoint amplitude undulations might serve to maximize the body
into the shape of an S, and the snake begins to undulate lat- length that is available for generating lift and might also
erally and to generate lift. In mid-glide, the anterior body ori- function to control instabilities related to pitch and roll.
ents parallel with the ground while the posterior body cycles A gliding Paradise Tree Snake is amazingly adept at ma-
up and down in the vertical plane. The aerial lateral undula- neuvering while in air. Unlike many fliers, the snake can turn
tion appears to be a modified form of typical terrestrial loco- sharply without banking. A turn is made by moving the ante-
motion, although the frequency of undulations is about rior body while the head is moving toward the direction of
one-third lower, while the amplitude is higher. The feat is the turn. One snake that was being filmed turned sharply to
probably more complex than terrestrial locomotion because avoid a tree during mid-glide. Typically, the flights of these
the snake maintains a ventrally concave shape while undu- snakes indicated the airspeed along the trajectory of glide av-
lating. The combination of movement and postural regulation eraged 8.1 m/s, or 29.2 km/h. The minimum glide angles of
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snakes averaged 28° and ranged from 13° to 46°. In more prac- unclear whether the reduced cost of sidewinding also is re-
tical terms, the gliding ability of these snakes is roughly lated to the specialized anatomical features that are found in
equivalent to that of other gliding vertebrates. proficient sidewinders such as Crotalus cerastes. Of course, the
energy cost of locomotion depends on the nature of the sub-
strate and the incline of the path of movement (see fig. 3.14).
The Energetic Costs of Snake Locomotion In spite of the differences in energy costs, the endurance
A limbless condition has evolved independently in several of locomotion is not very different between a laterally un-
groups of vertebrates, including salamanders, amphisbae- dulating racer and a sidewinding rattlesnake. The term en-
nians, and lizards, in addition to the snakes. Earlier specula- durance refers to how long a given level of locomotion effort
tions based solely on biomechanical considerations presumed can be sustained. If the two snakes mentioned above are
that the energetic cost of such locomotion was lower than moving at a speed of 0.6 km/h, the mean endurance is
that for vertebrates with limbs. Some of the arguments fa- about 73 minutes.
voring low energy expenditure during limbless locomotion
include no cost for vertically displacing the center of gravity
(as occurs in a walking or running human), no cost for acceler- Snakes as Robots
ating or decelerating limbs (there are none!), and a relatively Snakes have provided an interesting subject for robotics in
low cost for supporting the body. Subsequent investigations context of military, medical, and sundry other applications
have shown, however, that the actual energetic costs of where movement over complex terrain or narrow spaces is
locomotion in snakes can vary considerably depending on important. Robotic snakes have been made small enough to
the species and the mode of locomotion that it employs. maneuver around organs that are inside the human chest
Contrary to earlier expectation, the net energetic cost of cavity, while larger ones are able to carry a camera and
a racer (Coluber constrictor) moving by lateral undulation is transmit views from a treetop after crawling or swimming
equivalent to that of running in many limbed animals such to a tree and climbing it (fig. 3.20). Robotic snakes have
as lizards, arthropods, and mammals. Energy costs are often been called snakebots. Some of the advantages of snakebots
compared using a measure called the net cost of transport, over other types of robots include (1) ability to maneuver
which specifies the amount of energy that is used to trans- over rough terrain; (2) ability to climb steps; (3) ability to
port a given mass of an animal (say a gram) a given distance move over soft or thick materials; (4) ability to span gaps;
(for example, per kilometer). Such energy costs associated (5) ability to fit or squeeze into tight or narrow spaces; (6) a
with locomotion vary significantly with the mode of move- segmental structure in which similar segments can be re-
ment. Thus, it was found that the energetic cost of concer- placed easily; (7) ability to change body shape; and (8) ad-
tina locomotion is about seven times greater than is that for vantages in hostile environments in which exposed and
lateral undulation. The greater cost associated with the con- projecting surfaces such as limbs are easily damaged. Some
certina mode of locomotion possibly relates to the greater disadvantages of snakebots relate to control problems, lim-
frequency of movements, the smaller distance traveled per itations of transporting loads, temperature control, and op-
cycle of movement, and the summed contributions of both erating speeds that are slower than those of robot vehicles
sliding plus static frictional resistances. If the same snake is having wheels. The numerous advantages, however, render
moving by either mode, it travels less distance per cycle snakebots to be potentially quite useful.
during concertina locomotion compared with lateral undu- It is important to realize that no snakebot can accurately
lation, and the cost per cycle of movement is higher during or completely mimic the actual locomotion of live snakes,
concertina movement. The anchoring aspect of concertina but these robots can be made in various shapes and sizes
locomotion requires that part of the trunk must be at rest, and perform a large variety of tasks that would be difficult
so acceleration of body segments alternates with decelera- otherwise. One example of a very clever use of snakebots is
tion during the movement cycles. Theoretically, such loss of an application in animal control. A snakebot can pursue
momentum with each cycle of progression costs energy. dangerous or invasive animals (a rabid raccoon, for example)
In contrast, a Sidewinder Rattlesnake (Crotalus cerastes) and assist with their capture. Many such animals will attack
that is moving by sidewinding exhibits a net cost of transport a snakebot when it comes close, and the potential contact
that is somewhat less than half that of a racer (Coluber con- will result in the snakebot emitting an electrical shock that
strictor) that is moving by lateral undulation. It appears that paralyzes the aggressive animal. Snakebots are currently
the lifting of the body during sidewinding movements is ener- being developed for search and rescue applications at a
getically more economical than is the combined work that is Biorobotics Laboratory at Carnegie Mellon University, and
involved in overcoming the ventral and lateral sliding fric- are being investigated as a new type of interplanetary probe
tional forces that are inherent in lateral undulation. It is by engineers at the NASA Ames Research Center. Thumbs
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Figure 3.20. Robotic snakes, or “snakebots,” illustrated crawling over various surfaces, and climbing a tree. Each snakebot has a camera
mounted in front. Photos are courtesy of Howie Choset, a professor at Carnegie Mellon University’s Robotics Institute who was named as one
of the top 100 innovators in the world under the age of 35.
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up for real snakes being the inspiration for such innovative Banded Water Snake (Nerodia fasciata) and the Yellow Rat
research! Snake (Elaphe obsoleta). Journal of Morphology 197:159–181.
Jayne, B. C. 1988. Muscular mechanisms of snake locomotion: An
electromyographic study of the sidewinding and concertina
Additional Reading modes of Crotalus cerastes, Nerodia fasciata and Elaphe obsoleta.
Aubret, F., and R. Shine. 2008. The origin of evolutionary innova- Journal of Experimental Biology 140:1–33.
tions: Locomotor consequences of tail shape in aquatic snakes. Jayne, B. C., and A. F. Bennett. 1990. Selection on locomotor per-
Functional Ecology 22:317–322. formance capacity in a natural population of garter snakes.
Aubret, F., X. Bonnet, and R. Shine. 2007. The role of adaptive plas- Evolution 44:1204–1229.
ticity in a major evolutionary transition: Early aquatic Jayne, B. C., and A. F. Bennett. 1990. Scaling of speed and endur-
experience affects locomotor performance of terrestrial ance of garter snakes: A comparison of cross-sectional and
snakes. Functional Ecology 21:1154–1161. longitudinal allometries. Journal of Zoology (London)
Brisçhoux, F., A. Kato, Y. Ropert-Coudert, and R. Shine. 2010. Swim- 220:257–277.
ming speed variation in swimming sea snakes (Laticaudinae): Jayne, B. C., and J. D. Davis. 1991. Kinematics and performance
A search for underlying mechanisms. Journal of Experimental capacity for the concertina locomotion of a snake (Coluber
Marine Biology and Ecology 394:116–122. constrictor). Journal of Experimental Biology 156:539–556.
Byrnes, G., and B. C. Jayne. 2010. Substrate diameter and compliance Johnson, R. G. 1955. The adaptive and phylogenetic significance of
affect the gripping strategies and locomotor mode of climbing vertebral form in snakes. Evolution 9:367–388.
boa constrictors. Journal of Experimental Biology 213:4249–4256. Kelley, K. C., S. J. Arnold, and J. Gladstone. 1997. The effects of
Cundall, D. 1987. Functional morphology. In R. A. Seigel, J. T. Col- substrate and vertebral number on locomotion in the garter
lins, and S. S. Novak (eds.), Snakes: Ecology and Evolutionary snake Thamnophis elegans. Functional Ecology 11:189–198.
Biology. New York: McGraw-Hill, pp. 106–140. Lillywhite, H. B., J. R. LaFrentz, Y. C. Lin, and M.-C. Tu. 2000. The
Dial, B. E., R. E. Gatten Jr., and S. Kamel. 1987. Energetics of con- cantilever abilities of snakes. Journal of Herpetology 34:523–528.
certina locomotion in Bipes biporus (Reptilia: Amphisbaenia). Lindell, L. E. 1994. The evolution of vertebral number and body
Copeia 1987:470–477. size in snakes. Functional Ecology 8:708–719.
Gans, C. 1974. Biomechanics: An Approach to Vertebrate Biology. New Means, D. B. 2010. Blocked-flight aggressive behavior in snakes.
York: Lippincott. IRCF Reptiles and Amphibians 17:76–78.
Gans, C. 1984. Slide-pushing: A transitional locomotor method of Moon, B. R., and C. Gans. 1998. Kinematics, muscular activity and
elongate squamates. Symposium of the Zoological Society of propulsion in gopher snakes. Journal of Experimental Biology
London 52:12–26. 201:2669–2684.
Gasc, J.-P., D. Cattaert, C. Chasserat, and F. Clarac. 1989. Propul- Norris, K. S., and J. L. Kavanau. 1966. The burrowing of the West-
sive action of a snake pushing against a single site: It’s com- ern Shovel-nosed Snake, Chionactis occipitalis Hallowell, and
bined analysis. Journal of Morphology 201:315–329. the undersand environment. Copeia 1966:650–664.
Graham, J. B., W. R. Lowell, I. Rubinoff, and J. Motta. 1987. Surface Ruben, J. A. 1977. Morphological correlates of predatory modes in
and subsurface swimming of the sea snake Pelamis platurus. the coachwhip (Masticophis flagellum) and rosy boa (Lichanura
Journal of Experimental Biology 127:27–44. roseofusca). Herpetologica 33:1–6.
Gray, J. 1946. The mechanism of locomotion in snakes. Journal of Sanders, K. L., A. R. Rasmussen, and J. Elmberg. 2012. Indepen-
Experimental Biology 23:101–120. dent innovation of paddle-shaped tails in viviparous sea snakes
Hazel, J., M. Stone, M. S. Grace, and V. V. Tsukruk. 1999. Nanoscale (Elapidae: Hydrophiinae). Integrative and Comparative Biology
design of snake skin for reptation locomotions via friction an- 52:311–320.
isotropy. Journal of Biomechanics 32:477–484. Secor, S. M., B. C. Jayne, and A. F. Bennett. 1992. Locomotor per-
Hirose, S. 1993. Biologically Inspired Robots: Snake-Like Locomotors formance and energetic cost of sidewinding by the snake
and Manipulators. Oxford: Oxford University Press. Crotalus cerastes. Journal of Experimental Biology 163:1–14.
Hu, D. L., J. Nirody, T. Scott, and M. J. Shelley. 2009. The me- Shine, R., H. G. Cogger, R. N. Reed, S. Shetty, and X. Bonnet. 2003.
chanics of slithering locomotion. Proceedings of the National Aquatic and terrestrial locomotor speeds of amphibious sea-
Academy of Sciences (USA) 106:10081–10085. snakes (Serpentes, Laticaudidae). Journal of Zoology (London)
Jayne, B. C. 1982. Comparative morphology of the semispinalis- 259:261–268.
spinalis muscle of snakes and correlations with locomotion Shine, R., and S. Shetty. 2001. Moving in two worlds: Aquatic and
and constriction. Journal of Morphology 172:83–96. terrestrial locomotion in sea snakes (Laticauda colubrina, Lati-
Jayne, B. C. 1985. Swimming in constricting (Elaphe g. guttata) and caudidae). Journal of Evolutionary Biology 14:338–346.
nonconstricting (Nerodia fasciata pictiventris) colubrid snakes. Socha, J. J. 2002. Gliding flight in the paradise tree snake. Nature
Copeia 1985:195–208. 418:603–604.
Jayne, B. C. 1986. Kinematics of terrestrial snake locomotion. Socha, J. J. 2011. Gliding flight in Chrysopelea: Turning a snake
Copeia 1986:915–927. into a wing. Integrative and Comparative Biology 51:969–982.
Jayne, B. C. 1988. Muscular mechanisms of snake locomotion: An Walton, M., B. C. Jayne, and A. F. Bennett. 1990. The energetic cost
electromyographic study of lateral undulation of the Florida of limbless locomotion. Science 249:524–527.
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TE MPERATU R E AND E C T OT H E RM Y
Of the hundreds of variables that can shape the phenotype of an organism,

temperature has undoubtedly captured more than its share of attention.
—Michael J. Angilletta Jr., Thermal Adaptation: A Theoretical and Empirical

Synthesis (2009), p. 1
4
Heat Exchange with Long Bodies and The attenuate and limbless body form of snakes has im-
No Limbs portant consequences with respect to the manner in which
Like most other reptiles, snakes are exemplary of these animals are influenced by their physical environment
ectotherms—animals that rely on the external environ- and the behaviors by which they interact with it (fig. 4.1).
ment for sources of heat to elevate the body temperature. First, an elongated body has a relatively large surface-to-
This condition is fundamentally different from the physi- mass ratio and does not accumulate and store heat as easily
ology of birds and mammals, which generate internal heat as is the case for a more spherical shape and centrally posi-
production by means of relatively high rates of metabolism tioned mass. Of course, this limitation can be offset tempo-
(energy expenditure attributed to all the living processes rarily when the length of a snake is drawn into a tight coil,
within cells). The condition in birds and mammals is as shown in fig. 4.1. But when moving, the mass of the
termed endothermy, in contrast to that of snakes, which is snake exchanges heat with the environment along its
termed ectothermy. The higher rates of metabolism of en- length, and there is less “thermal inertia” in a snake than
dotherms confer relatively more freedom from the varia- there is in, say, an armadillo of similar mass. Furthermore,
tion of external conditions related to geography and the long body is subject to more regional variation of body
climate, but it comes with a cost. Endotherms must take in temperature and heat exchange than would be the case for
more energy as food in order to run their heat-generating a more compact body form.
machines, whereas ectotherms require less energy per Second, because snakes have no limbs, their body is in
time, in many cases approaching a full order of magnitude continuous contact with the ground or other surfaces upon
less than what is required by an endotherm. Thus, endo- which it crawls. Therefore, the exchange of heat is influ-
therms—especially smaller animals such as hummingbirds enced strongly by conduction to and from the substrate, in
and rodents—must eat on a daily or even hourly basis, contrast with, let’s say, a lizard that can erect its limbs and
whereas some snakes have survived more than a year with- stilt its trunk off the ground (fig. 4.2). Both animals are sub-
out food. Considering ecological communities, Harvey ject to radiative and convective heat exchange due to wind
Pough of Cornell University estimated that reptiles can or air movement, but the snake is relatively more influ-
produce as much biomass annually as do the resident birds enced by conductive exchange of heat with the ground
and mammals, even though they consume a much smaller upon which it crawls. When a desert lizard runs across hot
fraction of the net primary production in their environ- sandy surfaces (sometimes bipedally!), only the hands or
ment. The comparatively low rates of metabolism of snakes feet have minimal and intermittent contact with the
conserves energy relative to that expended by birds and ground, whereas a crawling snake on the same hot sub-
mammals, but it does not produce sufficient heat to elevate strate conducts heat into its body over a much larger area of
the body temperature significantly. Thus, if a snake is to contact.
warm itself, it must seek sunlight or warmer parts of the I was very surprised on two separate occasions to find
microenvironment in order to elevate its body tempera- snakes that were moving at midday in full summer sun
ture (but see below). across an open field. The setting was a field of dried grass in
| 103
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Figure 4.1. Heat exchanges between a South American Rattlesnake (Crotalus durissus) and its environment. Streams of thermal energy
radiating to the snake include direct solar radiation, indirect long-wave radiation from sky and surrounding objects, and possibly conduction
from the ground. The snake, in turn, radiates long-wave radiation to the environment, may conduct heat to the substrate, and loses heat by
convection and evaporation of water. Pathways (or modes) of heat transfer represented by red arrows indicate heat transfer from the
environment to the rattlesnake (plus metabolic heat production); pathways of heat transfer represented by blue arrows indicate heat transfer
from the rattlesnake to the environment; and pathways of heat transfer represented by brown arrows indicate bidirectional heat exchange to or
from the environment depending on which object is warmer. If it is a very warm day with air temperatures greater than the snake’s surface
temperature, the snake might gain heat by convection. The direction of net heat exchange depends on the difference in absolute temperature
between the snake, the ground, and other objects in the snake’s environment. All objects having a temperature above absolute zero radiate
long-wave infrared radiation, and the net exchange of such radiation between the snake and any object in its environment depends on the
difference in temperature. The snake’s body temperature depends on the balance between input and output of the various streams of energy
flow. This snake was photographed in Belize by Dan Dourson.
the Laguna Mountains of San Diego County, California. have met its death in the open field. These were two events
These snakes were likely moving from one area of chaparral that stimulated my thinking about the ease of overheating
or shaded oak woodland to another, but each was traversing in snakes that find themselves on heated ground surfaces
an open field that was in between. I captured each of these during very warm days (fig. 4.3).
snakes on the two occasions—one a Southern Pacific Rat- Lawrence Klauber during the 1930s recognized that tem-
tlesnake and the other a San Diego Gopher Snake—and perature limited the activity of snakes, and soon thereafter
took the body temperature of each, which felt warm to my both Walter Mosauer and Raymond Cowles became influen-
hands. The body temperature of the rattlesnake was 39.5°C, tial in promoting further thoughts about body temperature
and that of the gopher snake was very near the same value. and its control in squamate reptiles. Studies by these two
Both temperatures were quite close to the upper lethal limit herpetologists, and by Charles Bogert, established that both
of temperature tolerance. If either snake had not found a lizards and snakes have rather specific preferences for body
hole or shelter, or had not been captured by me, it might temperature. These early investigations stimulated what
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Figure 4.3. A Dusky Pygmy Rattlesnake, Sistrurus miliarius
barbouri, will potentially overheat if it remains too long in open, sunlit
sand during hot days in northern Florida. Photo by Dan Dourson.
(then called a Schultheis thermometer, named after its man-

ufacturer) or an electronic thermometer using either a
thermistor or thermocouple as a sensor (fig. 4.4). Herpeto-
logical humorists have referred to this as “grab and stab”
because investigators enthusiastic to obtain body tempera-
tures of animals in the wild would catch an animal (espe-
cially lizards) and quickly obtain a cloacal temperature
Figure 4.2. A Red-sided Garter Snake (Thamnophis sirtalis
parietalis) basks with its body flattened, remaining largely in contact
using one of the devices shown in fig. 4.4. It was relatively
with the substrate on which it lies (upper photo). The body easy to obtain field data in this way. People eventually real-
temperature therefore is influenced to a large extent by the ized, however, that interpretations of such data had limita-
temperature of the ground or objects on which it lies. In contrast, a tions if there was inadequate information provided about
Collared Lizard (Crotaphytus collaris) (lower photo) can minimize the the thermal environment of a snake. Additional limitations
influence of the substrate by raising its body off the ground or above
related to (1) reporting single instead of repeated measure-
the object on which it rests. Many lizards do this when the substrate
becomes too warm, whereas the snake must crawl to a cooler ments from an individual, (2) having a limited number of
substrate if it is threatened by an excess rise in its body temperature. measurements from conspecific individuals, and (3) intro-
The snake was photographed in Kansas, and the lizard was ducing a bias due to the time of day that individuals col-
photographed in Nevada by the author. lected measurements according to their own schedule.
Thus, the evaluation of thermoregulation and the variation
and causes of temperature selection in snakes has been in-
later became a long-lasting interest in behavioral thermoregu- adequate until the more recent adoption of more sophi-
lation and the importance of temperature in the ecology and sticated approaches. These have included continuous or
life history of reptiles. Lizards have been the principal sub- repeated measurements of body temperatures from free-
jects of these studies, but snakes have provided important ranging snakes using radio telemetry (fig. 4.5), and the corre-
additional insights and are uniquely suitable animals for in- lation of behaviors and physiology with body temperatures
vestigating many interesting facets of this subject. The word of snakes during experimental studies in the laboratory.
“thermoregulation” is a shortened form of “temperature reg-
ulation” and is commonly used in literature on this subject.
During the several decades following the early studies of Behavioral Thermoregulation
Ray Cowles and Charles Bogert, scientists have reported With a few exceptions (see below), ectothermic vertebrates
data for body temperatures measured in more than 100 depend on behavioral interactions with their environment in
species of snakes representing more than 10 different fam- order to regulate body temperature because there is insuffi-
ilies. Many of the early measurements were obtained op- cient heat production from metabolism to maintain a warm
portunistically using a rapid-registering glass thermometer body temperature continuously in variable environments.
Temperature and Ectothermy | 105
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Figure 4.4. Various devices that have been used to measure body temperatures of snakes and other small vertebrates, and the temperatures of
their environment. Progressing clockwise from the upper left: (A) A Wescor two-channel Digital TC Thermometer, which measures temperature
by means of a thermocouple at the termination of two small wires attached to the posts on the instrument. Each channel can utilize a separate
thermocouple wire, and the output can be recorded on a computer. (B) A Yellow Springs Intruments Co., Inc. 12-channel Tele-thermometer,
which measures temperature by means of a thermistor embedded at the end of various cables or leads that are attached to the instrument. The
one shown here is a flat disc that is designed to measure temperatures of flat surfaces, or can be used to indicate the temperature of a fully
absorbing “black body” if painted black and used to intercept solar radiation. Each of 12 channels can accommodate a separate thermistor
probe, and the various outputs can be recorded on a computer. (C) A Holohil Systems Ltd. implantable radio transmitter with an attached aerial.
This unit can be implanted into the body cavity of a snake, and temperature-dependent signals can be picked up from a distance using an
antenna and a calibrated recording device. (D) An Omega noncontact Infrared Thermometer, which detects the infrared energy emitted by any
material (e.g., an animal surface) and converts the energy factor into a temperature reading. The temperature of the emitting surface must be
above absolute zero (0º Kelvin). This instrument enables temperature measurements from a distance without contacting the object that is being
measured. (E) A Schultheis rapid-registering thermometer is shown lying next to a metal protective carrying case. This small thermometer has a
reduced bulb and can rapidly measure temperatures from 0 to 50 ºCelsius. The early models of these thermometers were manufactured by
Schultheis and Sons of Brooklyn, New York, but are available now from Miller and Weber of Queens, New York. These thermometers are easily
carried in the field and have been used to quantify field temperatures for more than 50 years. Photograph by the author.
Endotherms such as birds and mammals can do so primarily heat production does contribute to the animal’s heat load at
due to their high rate of metabolism, combined with insula- any given time, and there are physiological attributes such
tion (fur, feathers, or blubber in the case of aquatic forms) as variations of blood flow that can help to control the rates
that sequesters the metabolic heat within the body and re- of heating or cooling. However, behavior is overridingly im-
tards the losses of heat to cooler surroundings. Snakes, portant because it is used to adjust the net rate of heat flux
lacking insulation and having an attenuate body form, dis- to and from the physical environment, which determines
sipate heat rather rapidly and thus seek out direct solar ra- the rate and direction of body temperature change (fig. 4.1).
diation and warm microenvironments in order to elevate There are two aspects of behavior that are of primary im-
body temperature (fig. 4.2). The modest rate of metabolic portance to thermoregulation in snakes. The first is sometimes
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Figure 4.5. Dhiraj Bhaisare radio-tracks a King Cobra (Ophiophagus hannah) in the rainforest of the Western Ghats, India. Radio signals allow
the tracking antenna and receiver (not shown) to locate the snake, which is some distance away and shown here in the inset. A radio
transmitter has been surgically implanted into the body cavity of the snake. Such transmitters can be configured to transmit temperature as well
as other physiological information (e.g., heart rate), in addition to the location of a free-ranging animal. Photographs by Thimappa, a local tracker.
termed shuttling and refers to movements back and forth be-

tween warmer or cooler parts of the environment, depending
on the need of the animal. Numerous species of snakes living
in temperate climates flatten the body to absorb solar radia-
tion following their morning emergence in the spring prior to
engaging in movement and activity (fig. 4.2). During hotter
periods of the day these same snakes will seek shaded environ-
ments to avoid overheating (fig. 4.6). Retreating to subterra-
nean shelters or beneath leaf litter sometimes can retard heat
loss and can be important in limiting nocturnal cooling. On
the other hand, boa constrictors in tropical climates were
shown by investigations of Samuel McGinnis and Robert
Moore to maintain body temperature as much as 7°C below
shaded ground temperatures by seeking out subterranean en- Figure 4.6. A Southern Pacific Rattlesnake (Crotalus oreganus
helleri) seeks a shaded shelter during midday when environmental
vironments that were cooler.
temperatures have warmed considerably and the radiant energy from
The elongate body form of snakes presents a relatively direct sun is relatively intense. This animal was photographed by the
large surface area to the environment, especially if the author in the Laguna Mountains of Southern California, where the
snake is flattened and fully outstretched. However, when species is largely diurnal but restricts much of its activity to nighttime
the body is tightly coiled (as in fig. 4.1) the surface-to-mass in the middle of the summer.
ratio is greatly reduced and in some species can approach
the minimum possible ratio exemplified by a sphere. Such increases the likelihood of controlling body temperature
coiling minimizes heat exchange with the environment and by means of cardiovascular adjustments or metabolic heat
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production. In large constrictors such as boas and pythons,
rates of heat loss to the environment are reduced by as
much as one-half, although this factor varies with the envi-
ronment. Social aggregations of snakes can also further
modify the environment-body surface interactions. Large
overwinter aggregations of snakes tend to occur at north-
ern latitudes, where James Gillingham and Charles Carpen-
ter discovered that the tendency of snakes to form tight
aggregations within a den is temperature-dependent. The
snakes increasingly aggregate as the temperature falls (fig.
4.7). On the other hand, many snakes with ranges in lati-
tudes having more moderate climates tend to overwinter
singly rather than in large aggregations.
Opportunities for active thermoregulation can be some-
what limited in fossorial habitats, aquatic environments,
and even some terrestrial environments in the tropics. Thus,
some snakes might behave “passively” and merely conform
to their thermal environment. Aquatic snakes living in fresh-
water or marine environments live essentially at ambient
water temperature, which might be thermally uniform or
variable depending on the particular habitat. However, Rich-
ard Shine and Robert Lambeck studied aquatic file snakes
(Acrochordus arafurae) in northern Australia and found that
the variability of body temperature is significantly less than
that of the surrounding water in which they live. Much of the
year, the body temperature varies by no more than a few de-
grees Celsius owing to the stability of water temperature and
the selection of microhabitats on the part of the file snakes.
Snakes living in ponds or streams can alter their body tem-
perature by moving between warmed shallow edge waters Figure 4.7. Hundreds of Red-sided Garter Snakes (Thamnophis
sirtalis parietalis) amass together outside the entrance to a den where
and the deeper waters that are nearer midstream (fig. 4.8).
these snakes overwinter in southern Manitoba, Canada. Large
The second aspect of behavior important to thermoregula- aggregations of snakes are typical at many denning sites in temperate
tion involves postural adjustments such as flattening, tilting, regions having cold winters. Photograph by Tracy Langkilde.
coiling, or extending the body. Such behaviors alter the expo-
sure and contour of body surfaces, thereby adjusting the
regional exchanges of heat between the snake and its environ-
ment. Postural adjustments are a way in which a snake “fine-
tunes” the direction, rate, and location of heat flows to and
from the body. On cold mornings, Australian Red-bellied
Blacksnakes (Pseudechis porphyriacus) flatten the body broadly,
somewhat akin to a cobra but including the entire body, and
then tilt up on edge so the broad surface is exposed at right
angles to the early morning sun. Harold Heatwole and Clifford
Ray Johnson studied blacksnakes that were implanted with
thermocouples and demonstrated that postural adjustments
over a narrow range of body temperature abruptly alter the
thermal gradients within the body.
Snakes are long creatures, so there is clearly a likelihood
of thermal variation along the length of the body in various
circumstances. When snakes are observed to thermoregulate Figure 4.8. A Florida Green Water Snake (Nerodia floridana) rests
behaviorally in the laboratory using a finite heat source such at the edge of a pond where the water has been warmed by the sun.
as heat lamp, there is a pronounced tendency for at least This snake was photographed in Levy County, Florida, by Dan Dourson.
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Figure 4.9. Schematic illustration of a recorded sequence of body
positions, noted at 10-minute intervals, for an adult Red-bellied Black
Snake (Pseudechis porphyriacus) basking beneath an infrared heat
lamp. The “x” represents the center of irradiance from the lamp, and
the circle indicates roughly the isotherm where irradiance falls off to Figure 4.10. A gravid female Burmese Python (Python molurus
50 percent of maximum. The numbers indicate the time and core bivittatus) lying in an “upside-down” position with much of the
body temperature of the snake (measured by radiotelemetry). Drawing ventral body upright. This snake also features an unusual color morph
by Jason Bourque, Florida Museum of Natural History, based on fig. 2 of this species. Photograph by David Barker.
in H. B. Lillywhite, Behavioral thermoregulation in Australian elapid
snakes, Copeia 1980:452–458, 1980.
Thermal Preferences
The tendency for snakes to maintain their body temperature
some individuals to adjust their position such that different within a narrow range or at a particular level has been de-
parts of the body alternate location beneath the heat lamp. scribed by various words. The more commonly used terms
These behaviors suggest the snake is altering the regional are preferred body temperature, thermal preferendum, mean se-
heat input through time so as to maintain a more uniform lected temperature, or sometimes preferred range. For sake of
body temperature throughout its length. I discovered this convenience in this chapter I will use the term preferred
phenomenon while studying the thermoregulatory behav- body temperature (PBT) to indicate the mean of body tem-
iors of Australian elapid snakes (fig. 4.9). During early obser- peratures that are measured either in active snakes in the
vations, I found myself saying simply “Yes, the snake is still wild, or as the mean of body temperatures that are recorded
under the heat lamp.” But upon closer inspection I came to when snakes are allowed to exploit a gradient or mosaic of
realize that individual snakes were making subtle adjust- temperatures in the laboratory. When given a choice of envi-
ments in their position. The result was very crudely analo- ronments with adequate thermal opportunities, many spe-
gous to grilling meat or kabobs on a barbecue: various parts cies of snakes select a PBT generally within the range of 29 to
of the meat or vegetables (body of the snake) must be turned 34°C, and usually very close to 30°C. Measurements for nu-
regularly with respect to the heat source if one wishes to merous species have been summarized in various publica-
cook (warm) the object evenly. tions that are listed at the end of this chapter. Diurnal species
A number of species of pythons have been reported to inhabiting relatively open habitat may regulate body tem-
bask “upside down” by inverting the normal body position perature at levels in excess of 30°C, whereas lower tempera-
such that the ventral side is facing up. Such body inversion tures are characteristic of snakes that are nocturnal, fossorial,
is usually limited to the posterior half of the snake, while or occupants of shaded habitats. Some species that have
the head and anterior body remain with a more normal been investigated carefully are capable of regulating body
upright posture (fig. 4.10). Such inverted basking postures temperature with a very high degree of precision, sometimes
are more prevalent when a female snake is gravid, possibly varying no more than 1–2°C when a heat source is available.
functioning to distribute heat to the reproductive tract Charles Peterson of Idaho State University studied garter
and incubating embryos. On the other hand, David Barker snakes (Thamnophis elegans) using radio telemetry and dem-
suggested to me that the position might be related more onstrated a typical triphasic pattern of thermoregulation.
to the comfort of the female when the body is heavy with This consisted of (1) a rapid heating phase in the morning
young, much as position becomes important to the com- when relatively cool snakes emerged and basked in direct
fort of a pregnant woman. Basking positions and postures sunlight, (2) an extended “plateau” phase while snakes ther-
of various snakes also are thought to maximize body tem- moregulated during the day, and (3) a long cooling phase
perature of the gut when a recently taken meal is being during the late afternoon and night when snakes were se-
digested. cluded in nocturnal retreats (fig. 4.11). Raymond Huey and a
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Whether physiological mechanisms ex-
plain the maintenance of regional body
temperature differences in snakes is not
known (see below).
The preferred body temperatures of
snakes may undergo seasonal changes and
can be modified by changes in physiological
factors or the physical environment. The
term acclimation refers to a reversible
change in a character (including measures
of performance such as the speed of loco-
Figure 4.11. Hypothetical but characteristic plot of the daily changes in body motion) that results from a prolonged
temperature of a snake that (1) emerges in the morning and heats rapidly during exposure
change in the environment, especially tem-
to full sunlight, (2) behaviorally regulates body temperature during an extended “plateau”
phase when the thermal environment is appropriate, and (3) cools slowly when the sun perature. Thus, if an animal that is, let’s say,
sets and the snake seeks shelter from the cooling environment. Drawing by the author. adapted to low temperature experiences
warm temperatures for a prolonged period
of some days or weeks, a physiological per-
team of collaborators studied these snakes at Eagle Lake in formance curve (see below) might gradually
northeastern California and found that they retreated be- shift upscale so that the function is improved to better match
neath rocks of intermediate thickness, which offered the the temperature. Such physiological changes usually involve
snakes an appropriate variety of thermoregulatory oppor- alterations in the quality and quantity of enzymes that are re-
tunities relative to thinner or thicker rocks. Snakes beneath lated to alterations of genetic expression induced by the
the selected rocks were protected from overheating, but change of temperature. By definition, these changes are re-
they could achieve their preferred body temperature for versible, and of course they have limitations. In scientific liter-
long periods—longer times than if they remained on the ature, the term acclimation generally refers to such changes
ground surface or if they moved up and down within a when they are induced in the laboratory, whereas the term
burrow. One female snake, for example, maintained a body acclimatization is used to describe such changes that go for-
temperature between 27.6 ° and 31.6 °C for 14 hours (the ward naturally in a wild animal’s environment.
mean or “average” = 30.3°C), and for an entire 24 hours the Studies of acclimation that occurs when snakes are sub-
body temperature never decreased below 23.6°C. jected to different temperatures in the laboratory demon-
A number of herpetologists have found that temperatures strate an inverse relationship between the PBT and the
of a snake’s head are maintained within more narrow limits acclimation temperature. Such acclimation responses have
than are body temperatures measured elsewhere in the various interpretations, but they indicate a resetting of
snake, suggesting that relatively more precise regulation of thermoregulatory “set points” during prolonged exposure
head temperature above that of body temperature might to the temperature changes. A variety of factors in addition
help to optimize functioning of the central nervous system. to environmental temperature potentially influence PBT
Some diurnal lizards and snakes have been observed to warm set points, including illumination, reproductive condition,
the head before they fully emerge from nighttime retreats. feeding, skin shedding, endogenous seasonal or circadian
In a very interesting study of Northern Rubber Boas (Cha- rhythms, age, and sex. Much work remains to be conducted
rina bottae), Michael Dorcas and Charles Peterson found that in order to understand the variation of body temperature,
diurnally active snakes maintained a warmer head at temper- both within and between species, and the genetic determi-
atures below their thermal preference, but they maintained nants of the PBT in relation to interactions with forces of
warmer bodies when temperatures were above their thermal natural selection in a species’ environment.
preference. In other words, rubber boas regulate their head
temperature more precisely than their body temperature
during the daytime. Furthermore, rubber boas were shown to Physiological Thermoregulation
exhibit significantly higher head temperatures than body tem-
peratures during the night. The active maintenance of head- Internal Thermogenesis and Endothermy
body temperature differences (about 2 °C) can be attributed Although the majority of snakes are likely to be strict ecto-
either to behavioral mechanisms such as preferential head therms nearly all of the time, we know of documented cir-
warming, or to physiological mechanisms involving blood cumstances in which internal heat production is capable of
shunts or countercurrent heat exchangers (see chapter 6). elevating body temperature above that of the immediate
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within the general range of 31 to 33°C over an ambient range
of at least 10°C. The heat that is generated by the snake
maintains the temperature of her brooding eggs close to
30°C when air temperatures range between 23 and 30°C.
Thus, brooding female pythons can elevate the tempera-
tures of developing eggs by some 7°C above the temperature
of the nest outside the brooding female. These snakes
are not only capable of endothermy, but they use it to regu-
late body temperature and, indirectly, the temperature of
the incubating eggs. This brooding behavior is advantageous
in pythons whose geographic range extends to mountains
where air temperatures can fall to levels that might slow the
development and hatching of the species’ eggs. Some other
pythons (e.g., Water Pythons, Liasis fuscus) show facultative
Figure 4.12. A Ringed Python (Bothrochilus boa) brooding her
maternal brooding behavior, with the genesis of body heat
clutch of eggs. The egg temperatures are regulated by spasmodic
muscle twitches of the female snake, which is similar to muscle being used to warm the clutch. Richard Shine and others
“shivering” in humans. Photograph by David Barker. have therefore suggested that a female python’s “decision”
where to locate her eggs and whether to remain and brood
them can have important consequences for the subsequent
environment. The most dramatic and well-known example is development and success of the offspring. These are won-
in connection with the brooding behavior of female pythons. derfully “hot” topics in snake biology!
Female pythons gather their eggs into a heap around which Surprisingly, there are other very interesting examples
the snake coils tightly and encloses the clutch in the center of endothermy in snakes. One is a condition that I discov-
of the coils (fig. 4.12). The female generates heat for transfer ered recently in newly hatched California King Snakes. The
to the eggs by means of twitching her body muscles. The hatchlings are born with a large amount of yolk that is still
means of heat generation is very similar to what occurs present in their digestive tract. For periods up to two weeks,
when mammals—including humans—shiver to produce the skin temperature of hatchlings averages 0.6°C above the
body heat in response to cold exposure. Skeletal muscles are ambient temperature. This small but significant elevation
activated by nerves, but not in a coordinated way to produce of body temperature is thought to result from the active ab-
movement. Rather, the muscles twitch sporadically and gen- sorption and metabolism of the yolk and is therefore analo-
erate tension without shortening to produce movement. The gous to what is called postprandial thermogenesis (specific
spasmodic twitching of muscles in the python thus gener- dynamic action; see chapter 2). A group of scientists led by
ates heat, which warms the body of the female and transfers Glenn Tattersall have carefully investigated South Ameri-
heat to the eggs that are located between the body coils. can Rattlesnakes (Crotalus durissus) and demonstrated that
The controlled production of body heat with significant postfeeding elevation of body temperatures can result from
transfer to elevate the temperature of a brooded clutch of internal thermogenesis related to metabolic responses to
eggs has been shown convincingly in three species of py- feeding. The body surfaces of fed rattlesnakes have been
thons, but many others might be incapable of significant shown to elevate 0.9–1.2°C by thermal imaging, so the mag-
heat production. Isometric muscle contractions have also nitude of associated changes in deep core temperatures
been noted in rat snakes (Pantherophis obsoletus) and Bull- could well be even more pronounced (fig. 4.13). This degree
snakes (Pituophis melanoleucus) when exposed to low tem- of thermogenesis is sufficient to enhance digestion signifi-
peratures (10°C and 8°C, respectively). The contribution of cantly. More important, however, are voluntary seeking of
such muscle activity to body temperature in these circum- warmer environments or increased basking to elevate body
stances is not known, however. temperature following feeding. For example, David Slip and
The phenomenon of heat generation during brooding by Richard Shine found that Australian Diamond Pythons
pythons is known as facultative endothermy (and in mam- (Morelia spilota) select temperatures that are several de-
mals shivering thermogenesis). The phenomenon has been grees higher after feeding in order to speed up the digestion
studied most completely in Burmese Pythons (Python molu- of food. Not all snakes, however, elevate their body temper-
rus) and was first investigated by Lodewyk H. S. Van Mierop ature following feeding.
and Susan Barnard. Brooding female Burmese Pythons gen- Larger snakes, by virtue of their mass, can retain heat
erate muscular heat when ambient temperatures fall below longer than can smaller individuals and thus have greater
about 31°C, and the elevated body temperature remains thermal inertia, especially when the body is drawn into a
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snakes in aggregated situations appear
very capable of controlling their rates of
heat loss to some extent, there is no evi-
dence that metabolic heat production is
actively engaged in thermoregulation as
in the brooding female pythons.
Respiratory Heat Transfer Mechanisms

When snakes are exposed to stressfully
higher body temperatures, they may in-
crease the rate of lung ventilation and
breathe with the mouth open. Evapora-
tion from moist membranes lining the
mouth, trachea, and lung cools these sur-
faces and potentially removes heat from
the body. Such evaporative cooling can be
important to thermoregulation in endo-
thermic birds and mammals, and can
stabilize brain temperatures of desert
Chuckwalla lizards some 3ºC below air
temperatures. However, such cooling
probably has marginal influence in the
body’s heat balance of snakes. Thermo-
graphic images of temperature differences
between the head and body of rattle-
snakes have revealed regions of cooling
around the mouth and nasal capsule, sug-
gesting that heat loss occurs by means of
evaporative cooling in the ventilatory pas-
sageways (fig. 4.13). A research team lead
by Brendan Borrell demonstrated that the
Figure 4.13. Thermal images illustrating postfeeding thermogenesis in a South differences in temperature between the
American Rattlesnake (Crotalus durissus). The upper photo shows a rattlesnake prior
head and body increase from about 2ºC to
to feeding on a live mouse that can be seen nearby. Note the warm body temperature of
the endothermic mouse relative to that of the rattlesnake. The lower photo shows the about 3ºC when rattlesnakes begin rat-
rattlesnake again, 24 hours after it has eaten the mouse. The elevated body tling. These and other studies suggest that
temperature of the rattlesnake is due to metabolic heat production related to an behavioral activities such as locomotion
up-regulation of metabolism associated with digestion of the mouse. The “cold” spot at and rattling might change breathing rate
the head of the snake is attributable to respiratory evaporative cooling of the nasal
and thereby influence cooling of the head
passages associated with breathing. The vertical numerical scales to the right of each
photo indicate how surface temperature varies according to the colors in the image.
relative to the body. How these mecha-
Note these scales are different for each image. Photographs by Glenn J. Tattersall. nisms might be activated during heat
stress has not been evaluated.
Whether or not snakes actively pant
tight coil. The possibility of endothermic elevation of body to remove body heat is not well studied
temperature is increased further when snakes aggregate in (see also chapter 6). The phenomenon is documented in a
large numbers. Theoretical calculations by Fred White and number of lizards, yet no snake is known to effectively
Robert Lasiewski have suggested that a hypothetical aggre- pant. Perhaps panting is less effective in snakes because of
gate of 150 denning rattlesnakes could maintain an aggre- the long shape of the body with its heat content being more
gate body temperature about 15°C above the ambient den removed from the region of cooling (at or near the head)
site temperature. This level of endothermy is attributable to than is the case in lizards. The hypothalamus of the brain is
metabolic heat production relative to an aggregate “effec- an important center for regulating thermoregulatory re-
tive” surface area that is 40 percent of the summed surface sponses, including behavior, in both mammals and lizards.
areas of individual snakes if they were in isolation. While This is likely to be true in snakes as well.
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Why Do Snakes Thermoregulate? studied and best characterized in several species of frogs
Snakes regulate their body temperature for basically two and turtles. Garter snakes (Thamnophis sirtalis) and boreal
reasons: (1) to avoid thermal extremes that threaten their vipers (Vipera berus) can endure brief exposures to freezing
existence, and (2) to maximize or optimize bodily functions. temperatures, but they die when temperatures fall below
At the low end of the temperature scale, snakes and other about −2 to −3°C for more than a few hours. Some periph-
animals must avoid freezing to death. At the high end, tem- eral freezing of skin and muscle tissue is probably tolerated,
perature disrupts the structure of proteins and can be es- but the penetration of ice to core vital organs such as the
pecially injurious to enzymes, causing denaturation that heart is not.
impairs the ability of molecules to maintain proper struc- The process of freezing has been studied in frogs and in
ture and therefore function. One immediate consequence is turtles. Formation of ice crystals is initiated at a peripheral
that coordinated systems such as nerves and muscles lose site such as the skin, and is propagated inward in a direc-
orchestration and therefore their integrity of response. The tional manner through the body. Ice forms first in spaces
result is death as movement, breathing, blood circulation, outside the organs, such as the abdominal space; then even-
and other vital activities become disrupted or impaired. tually the organs freeze. During thawing, melting occurs
uniformly throughout the body core, and the organs melt
Tolerance Limits to Cold before the ice that surrounds them.
The temperature at which a cooling snake loses coordina- In amphibians and some reptiles other than snakes, so-
tion and movement is potentially lethal if the animal called “antifreeze” proteins inhibit the formation of ice crys-
cannot escape from that condition. Laboratory determina- tals in body fluids, and “ice-nucleating” proteins may initiate
tions of such a temperature is termed the critical thermal and control the formation of ice in the extracellular fluids.
minimum (CTMin), representing the temperature at which A common adaptation is for low molecular weight metabo-
long-term survival is not possible unless the snake escapes lites such as glucose to accumulate seasonally during cold
from this or lower temperatures. Critical thermal minima weather and to provide resistance to freezing of intracellular
have been determined for perhaps about a dozen species fluids and the whole body. Studies of turtles have shown
and are generally in the range of one to two or several de- that genes responsive to cold produce proteins that help to
grees Celsius above freezing. Freezing temperatures are protect cells from the injurious effects of reduced blood flow
threatening because of the potential damage that occurs to and oxygen that results from the freezing of blood plasma
cells from ice crystals that form in the cellular or extracel- during exposure to extreme cold. However, these physiolog-
lular fluids and physically disrupt or destroy the cellular ical and biochemical aspects of freeze tolerance have not yet
membranes and other structures. Freezing of body fluids been demonstrated in snakes.
also increases the osmotic concentration of fluids that re-
sult when water is withdrawn from solutes during the for- Tolerance Limits to Heat
mation of ice crystals. This reduces the solvent relative to Temperatures that are high-end counterparts to critical
solutes, and the resulting osmotic concentrations in the re- thermal minima are termed critical thermal maxima (CT-
maining fluids disturb cellular function and the distribution Max). These also have been measured in about a dozen spe-
of body fluids in the various body compartments. The effect cies of snakes and typically range from 37 to 44°C with a
is very similar to dehydration. mean around 40°C. Death ensues if the body temperature
Many reptiles and some snakes have the ability to escape increases just a few degrees higher than this point. Like
the lethal effects of freezing temperatures by “supercooling” many other vertebrates, the operational body temperature
the entire body to temperatures that are below the normal of snakes is much closer to the upper lethal limit than it is
freezing point without the formation of ice crystals. Several to the lower lethal limit. At least, this is true if the animal is
colubrid, elapid, and viperid species of snakes have been given a choice and has the means to achieve its preferred
shown by Charles Lowe and his colleagues to supercool to body temperature. Again, snakes must be very careful to
temperatures ranging roughly from −4 to −7°C. Survival fol- avoid overheating because they crawl with the ventral body
lowing supercooling without the formation of internal ice is surfaces in contact with the substrate. This imposes great
widespread among ectothermic vertebrates and is probably difficulty for regulating body temperature if the environ-
quite common among snakes, especially those that manage mental temperatures are hot. Therefore, the principal
to survive at high latitudes and high mountains. defense of snakes against overheating is the behavioral
Numerous animals living in seasonally cold environ- avoidance of microenvironments that might transfer exces-
ments also have the ability to endure the freezing of extra- sive heat to a snake. Such avoidance explains why one does
cellular body fluids (cells must be protected from freezing). not see snakes crawling around during the hotter daylight
This phenomenon is termed “freeze tolerance” and has been hours in open, hot environments such as a low-latitude
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desert. The snakes are secluded down holes or beneath
rocks and other objects where the extreme temperatures of
more open environments are avoided.
Thermal Sensitivity, Performance Curves,

and Trade-offs
Anyone familiar with chemistry and physics knows that
fundamental physical and chemical processes are acceler-
ated by temperature, and that biochemical reaction rates
increase with increasing temperature up to some max-
imum. Therefore, life processes that depend on underlying
biochemistry—respiration, digestion, growth, and so on—
are sensitive to changing temperatures. This means also Figure 4.14. Hypothetical performance curves depicting how a
that coordinated systems—composed of many parts but chosen variable (digestion, for example) changes with temperature.
acting as a whole—alter in performance with changes in The breadth of each performance curve is indicated by the horizontal
temperature. Most persons familiar with snakes or other arrows, which describe the limits of temperature within which a large
percentage of the functional range is expressed (say, 95 percent).
ectothermic reptiles have observed comparatively slow
Curve A depicts a hypothetical performance curve in a species of
movements during locomotion or tongue flicking when the snake that is adapted to living at low temperatures (e.g., at high
animal is cold, whereas at higher temperatures all the action altitude or latitude) and is subjected to colder environmental
speeds up considerably. temperatures than is the species represented by curve B, which
So-called “performance curves” usually refer to the ther- features a performance curve for a species adapted to living at higher
mal sensitivity of key tasks or functions, which are quanti- temperatures (a warm-environment species). The variation or shifts of
the function depicted at curve B (dashed line) represents hypothetical
fied in some manner and plotted as a function of temperature.
changes that are related to acclimation or acclimatization. That is, if
Examples are illustrated in figure 4.14. The concept has be- the animal is subjected to changing temperatures in the environment,
come widely used in comparative biology, particularly in con- the performance shifts upscale (in response to warmer temperatures)
text of linking phenotypic traits, performance, and fitness. or downscale (in response to cooler temperatures) if the environmental
There is, of course, tremendous variation of performance change is prolonged. The horizontal dashed line represents the total
increase in performance breadth that is attributable to thermal
curves, and they can be expected to vary with species as well
acclimation. These changes in the physiology or performance of the
as individual acclimation history related to previous thermal animal in response to environmental variation are called phenotypic
exposure. Each performance curve predicts the thermal opti- plasticity. Drawing by the author.
mum, or temperature of maximum value, and the perfor-
mance breadth of a given function, which is some measure of
the thermal range over which performance has some subjec- terms relate to the inherent ability (genetic capacity) of a
tive value to the organism. species to alter its structure, function, and behavior for im-
Regardless of the underlying mechanism or causation of proved survival in response to changing aspects of the
the thermal sensitivity, adaptation for performance at low dynamic environments in which a species lives.
temperatures (e.g., locomotion in cold-climate European vi- The sensitivity of life processes to temperature, as well as
pers) usually involves a trade-off with performance at high other resources such as availability of water, limits the activ-
temperatures, and vice versa (e.g., locomotion in warm- ities of snakes both in time and in space. Hence, many snakes
environment tropical file snakes). Put in other words, a ge- that live in temperate climates are active at different times of
notype or phenotype that performs well at low temperatures the day depending on the season and how daily changes in
usually performs poorly at high temperatures and vice versa. the thermal environment influence the ability of a snake to
Hence, there are constraints on performance depending on achieve appropriate body temperatures. A dramatic example
the environment and the adaptive specialization of the an- of such seasonal change is the switch in behavior of snakes
imal. However, some “escape” from these constraints is pos- that are diurnal during early spring and become nocturnal
sible owing to acclimation (fig. 4.14). during the hotter periods of summer (fig. 4.15).
Another word that is commonly used to express the var- The variation of body temperature has potentially many
iation of a phenotype attributable to environmental influ- consequences for snakes, just as for other ectotherms that also
ence is phenotypic plasticity. And the range of phenotypes have variable body temperatures. Rates of resting metabolism
that are expressed by a given genotype operating under a generally increase exponentially with temperature so that en-
range of environmental conditions common to an animal’s ergy requirements are increased at higher temperatures but
habitat is called reaction norm. Fundamentally, all such with the advantage of enhanced muscle performance, foraging
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An interesting example of how temperatures that are se-
lected by snakes influence important functions is the behav-
ioral choice of temperature that increases the chemical
energy that might be gained following the ingestion of a
meal. Using empirical models related to digestion in Chinese
Green Tree Vipers (Trimeresurus s. stejnegeri), Tien-Shun
Tsai and his collaborators demonstrated that selection of el-
evated body temperatures (about 28ºC) for a brief period
following eating (see chapter 2) consistently maximized the
amount of energy that was gained from the meal.
Herpetologists have recognized that there are costs as
well as benefits to thermoregulation in ectotherms such
as snakes. The idea has been championed by Raymond
Huey and holds that a snake that maintains a high body
temperature—by sun exposure for example—might also
be more exposed to predators than if it was more reclusive
in its behavior. Equally or more important, higher temper-
atures increase the rate of metabolism so that snakes use
more energy when the body temperature is high. This sit-
uation is all right provided the foraging success compen-
sates, but if prey items are in short supply it might be a
better strategy to conserve energy by spending less time
at the higher temperatures. This subject of “trade-offs” be-
comes even more complicated when one considers the in-
teractions of temperature with evaporative water losses,
Figure 4.15. Bar graph illustrating the percentage of Black Tiger skin shedding, reproduction, immune responses, and nu-
Snakes, Notechis ater niger, that are active in two different seasons, merous other living processes. There is evidence that some
based on studies at the Franklin Islands, South Australia. Note that snakes adjust their thermoregulatory strategy according
snakes are more active during midday in winter when the season is
to the status of energy and water balance, reproduction,
cooler, but during the hotter summer the activity shifts to early morning
or late afternoon and evening hours. Data are redrawn by the author, and other factors. More detailed studies are needed, how-
from T. D. Schwaner, A field study of thermoregulation in Black Tiger ever, before models of cost-benefit analyses can be gener-
Snakes (Notechis ater niger: Elapidae) on the Franklin Islands, South alized. As with many things in nature, we can take
Australia, Herpetologica 45:393–401, 1989. satisfaction in knowing that behaviors of snakes are un-
doubtedly far more complex and interesting than we
usually give credit.
success, and so on—up to some limits, of course. Some snakes
exhibit a “plateau” of the rate of metabolism at temperatures
corresponding to the activity range of the species, suggesting
Additional Reading
there is adaptation to stabilize performance related to energy Avery, R. A. 1982. Field studies of body temperatures and thermo-
use at those temperatures that are most favorable for the ani- regulation. In C. Gans and F. H. Pough (eds.)., Biology of the
mal’s activity. Temperature also affects growth and develop- Reptilia, vol. 12. New York: Academic Press, pp. 93–166.
ment, but there have been surprisingly few studies of these Bennett, A. F. 1984. Thermal dependence of muscle function.
American Journal of Physiology 247:217–229.
phenomena in snakes. The advantage of higher temperatures
Borrell, B. J., T. J. LaDuc, and R. Dudley. 2005. Respiratory cooling
for growth is related in part to increased muscle performance, in rattlesnakes. Comparative Biochemistry and Physiology A
foraging success, and rapid digestion and absorption of in- 140:471–476.
gested food items. In ecological terms, temperature can affect Cowles, R. B. 1939. Possible implications of reptilian thermal toler-
the frequency of feeding, the manner in which snakes forage, ance. Science 90:465–466.
the time spent foraging, success of prey capture, processing of Cowles, R. B., and C. M. Bogert. 1944. A preliminary study of the
thermal requirements of desert reptiles. Bulletin of the Ameri-
ingested energy, reproduction, avoidance of predators, and sur-
can Museum of Natural History 83:261–296.
vivorship. Nocturnal behaviors of snakes during summers, for Dorcas, M. E., and C. R. Peterson. 1997. Head-body temperature
example, can reduce the exposure of active snakes and there- differences in free-ranging rubber boas. Journal of Herpetology
fore the risk of capture by diurnal predators such as hawks. 31:87–93.
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Gillingham, J. C., and C. C. Carpenter. 1978. Snake hibernation: Naulleau, G. 1983. The effects of temperature on digestion in
Construction of and observations on a man-made hibernacu- Vipera aspis. Journal of Herpetology 17:166–170.
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Graham, J. B. 1974. Body temperatures of the sea snake Pelamis free-ranging garter snakes. Ecology 68:160–169.
platurus. Copeia 1974:531–533. Porter, W. P., and C. R. Tracy. 1974. Modeling the effects of tem-
Gregory, P. T. 1990. Temperature differences between head and perature changes on the ecology of the garter snake and
body in garter snakes (Thamnophis) at a den in central British leopard frog. In J. W. Gibbons and R. R. Sharitz (eds.), Ther-
Columbia. Journal of Herpetology 24:241–245. mal Ecology AEC Conference 730505. Oak Ridge, Tennessee,
Hammerson, G. A. 1977. Head-body temperature differences mon- pp. 595–609.
itored by telemetry in the snake Masticophis flagellum piceus. Pough, F. H. 1983. Amphibians and reptiles as low-energy systems.
Comparative Biochemistry and Physiology 57:399–402. In W. P. Aspey and S. I. Lustick (eds.), Behavioral Energetics: The
Heatwole, H., and C. R. Johnson. 1979. Thermoregulation in the Cost of Survival in Vertebrates. Columbus: Ohio State University
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Zoological Journal of the Linnean Society 65:83–101. Scott, J. R., and D. Pettus. 1979. Effects of seasonal acclimation on
Heatwole, H., and J. A. Taylor. 1987. Ecology of Reptiles. 2nd edi- the preferred body temperature of Thamnophis elegans vagrans.
tion. Chipping Norton, New South Wales, Australia: Surrey Journal of Thermal Biology 4:307–309.
Beatty & Sons,. Shine, R., and R. Lambeck. 1985. A radiotelemetric study of move-
Huey, R. B. 1982. Temperature, physiology, and the ecology of rep- ments, thermoregulation, and habitat utilization of Arafura file-
tiles. In C. Gans and F. H. Pough (eds.), Biology of the Reptilia, snakes (Serpentes: Acrochordidae). Herpetologica 41:351–361.
Vol. 12. New York: Academic Press, pp. 76–98. Shine, R., T. R. L. Madsen, M. J. Elphick, and P. S. Harlow. 1997.
Huey, R. B., C. R. Peterson, S. J. Arnold, and W. P. Porter. 1989. Hot The influence of nest temperatures and maternal brooding on
rocks and not-so-hot rocks: Retreat-site selection by garter hatchling phenotypes in water pythons. Ecology 78:1713–1721.
snakes and its thermal consequences. Ecology 70:931–944. Slip, D. J., and R. Shine. 1988. Thermoregulation of free-ranging
Huey, R. B., and M. Slatkin. 1976. Costs and benefits of lizard ther- diamond pythons, Morelia spilota (Serpentes, Boidae). Copeia
moregulation. Quarterly Review of Biology 51:363–384. 1988:984–995.
Klauber, L. M. 1939. Studies of reptile life in the arid Southwest. Tattersall, G. J., W. K. Milsom, A. S. Abe, S. P. Brito, and D. V. An-
Bulletin of the Zoological Society of San Diego 14:1–100. drade. 2004. The thermogenesis of digestion in rattlesnakes.
Landreth, H. F. 1972. Physiological responses of Elaphe obsoleta Journal of Experimental Biology 207:579–585.
and Pituophis melanoleucus to lowered ambient temperature. Tsai, T. S., H. J. Lee, and M.-C. Tu. 2009. Bioenergetic modeling
Herpetologica 28:376–380. reveals that Chinese green tree vipers select postprandial tem-
Lillywhite, H. B. 1980. Behavioral thermoregulation in Australian peratures in laboratory thermal gradients that maximize net
elapid snakes. Copeia 1980:452–458. energy intake. Comparative Biochemistry and Physiology A
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Snakes, Ecology and Evolutionary Biology. New York: Macmillan, Postnatal ecdysis establishes the permeability barrier in snake
pp. 422–477. skin: New insights into lipid permeability barrier structures.
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Physiology 39A:125–135. in a brooding female Python molurus bivittatus (Serpentes: Boi-
McGinnis, S. M., and R. G. Moore. 1969. Thermoregulation in the dae). Copeia 1976:398–401.
Boa Constrictor Boa constrictor. Herpetologica 25:38–45. White, F. N., and R. C. Lasiewski. 1971. Rattlesnake denning: The-
Mosauer, W. 1936. The toleration of solar heat in desert reptiles. oretical considerations on winter temperatures. Journal of The-
Ecology 17:56–66. oretical Biology 30:553–557.
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S T RUC T U R E AND F U NC T I ON
O F SKIN
He who does not find core or substance in any of the realms of being, like
flowers which are vainly sought in fig trees that bear none,—such a monk
gives up the here and the beyond, just as a serpent sheds its worn-out skin.
5
—The Worn-out Skin: Reflections on the Uraga Sutta, translated by
Nyanaponika Thera (Kandy: Buddhist Publication Society, 1989)
Where Body Meets the Outside World leather or jewelry (fig. 5.2). But let us return to a consider-
The skin of snakes is a very important organ and one that can ation of skin that is based in structural features and func-
be incredibly beautiful, adorned by natural selection with ex- tions that are more relevant to the snake itself.
quisite colors and patterns. The color pattern of the skin, and First and foremost, the integument of any animal pro-
its sleek appearance, is for many persons the foremost at- vides a barrier between the internal environment and the
tribute that focuses our attraction to the animal. The word outside world. It is a mechanical barrier that protects the
integument refers to the covering of an animal, which is the underlying muscles, blood vessels, and internal organs
skin and its derivatives such as scales, feathers, fur, or “horns” from abrasion and physical injury. It also functions as a
of various kinds. It is in this broader context that I will use physiological barrier and prevents the excess losses or gains
the term “skin” in this book. As such, the skin of a snake is of water, ions, and other components of the body fluids.
usually the largest organ of its body, at least in terms of mass. The skin acts to prevent things from getting in as well as
It is also of extreme importance, having multiple functions out. Therefore, the skin acts to prevent the entry of un-
and interactions with the environment. We humans take wanted chemicals, especially microbes and toxins.
comfort in the fact that beauty is more than skin deep, but We see that the skin acts as a barrier, but the barrier is
for snakes the beauty we see is virtually all in the skin. not absolute. Thus, the skin acts to regulate the exchange of
The interest of humans in the skin of snakes, and specu- some things but does not prevent their passage entirely. For
lations about the functions of reptilian skin, has had a long example, respiratory gases—oxygen and carbon dioxide—
history. The disciples of Aesculapius, the Greek god of heal- are exchanged to some extent in aquatic snakes that bre-
ing, revered snakes and interpreted their periodic skin- athe, in part, across the skin. Simultaneously, skin that is
shedding as a symbol of rebirth and renovation (fig. 5.1). permeable to the respiratory gases must also regulate the
Aristotle was interested in the abilities of Old World cha- exchange of water, ions, and toxins. This is a complicated
meleons to change colors. More recently the idea that rep- subject that will be revisited elsewhere in this book. The
tiles first “conquered” dry land because of their cornified skin also is a transducing surface, absorbing solar radiation
integument has been implied in general textbooks, and that is converted to heat and very often used to warm the
some folks still believe that squamate reptiles are essen- body. (A transducer is something that changes the form of
tially waterproof owing to the presence of “scales” on the energy that impinges on it. See chapter 7 for further discus-
skin. Herpetoculturists have become fascinated with the sion.) Another example is when mechanical vibrations are
many unusual color patterns that are expressed within a sensed by nerves in the skin, which convert the mechanical
species, and they have selected for particular genetic lines energy into bioelectric energy that is used to transmit nerve
that are popular with pet enthusiasts. Unfortunately, many signals from the skin to the brain. Solar energy impinging
snakes have been killed in various parts of the world and on the skin also is used to initiate chemical reactions that
their skins have been tanned to adorn various products of lead to the synthesis of Vitamin D.
| 117
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Figure 5.1. Stone carvings depicting various items of snake worship, located on a Hindu temple ground in south India. The stone at the far
right resembles a caduceus, or “herald’s staff” carried by Hermes in Greek mythology. The same staff was also borne by heralds in general and
consists of a staff entwined by two snakes. This symbol was used in astrology and alchemy, and also became recognized as a symbol of
commerce. The caduceus is sometimes confused with the traditional medical symbol, which has only a single snake and represents the rod of
Asclepius (inset). The photograph is courtesy of Romulus Whitaker, and the inset was drawn by Shauna Lillywhite.
As we can judge from this discussion, the skin is an organ Structure of the Dermis and Epidermis
having many functions. And there are others. Shedding of Much of what people know about skin is based in clinical,
skin releases substances that communicate chemical sig- pharmaceutical, and cosmetic contexts related to human
nals between snakes. As an example, female garter snakes skin, which for most practical purposes is fairly homoge-
of various species shed their skin soon after they emerge neous (although it is a composite organ). In contrast, the
from dens or overwintering sites. The new skin bears a sub- skin of snakes is very heterogeneous and consists of a
stance identified as a methyl ketone, which acts as a chemi- system of layered membranes. The more complex, outer
cal attractant for male snakes of the same species. Such a part of the skin is the epidermis, separated from the dermis
chemical is called a pheromone, defined as a chemical sub- below it by a basement membrane (fig. 5.3). The innermost
stance produced by an individual organism and released dermis consists largely of fibrous connective tissue com-
into the environment for the purpose of signaling a social posed mostly of collagen fibers, and is separated from un-
response from other individuals of the same species. The derlying body muscles by looser connective tissue and fat.
pheromone of the garter snake adheres to the ground where For reasons not entirely understood, the dermis of some
they crawl, and males locate the females by trailing them. species is applied very tightly to the underlying muscle,
Thus, the skin mediates communication between individ- whereas in others it is considerably looser. Persons who
uals by means of releasing pheromones onto trails (see also have skinned snakes are probably aware of these differ-
chapter 9). ences. In other reptiles (e.g., crocodilians, turtles, and some
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Figure 5.2. Hundreds of tanned snake skins in a warehouse of the Bharat Leather Corporation in Chennai (formerly Madras), India. This was a
clearinghouse for snake skins that was established after the ban on snake skin trade was enacted in the 1970s, the idea being to clear existing
stocks of snake skins once and for all. Presently there is no legal snake skin industry in India. Photograph by Romulus Whitaker.
lizards) the dermis gives rise to bony plates and other struc- The more rigid layers of β-keratin overlie the less rigid
tures that are lacking in snakes. The dermis in snakes adds layers of α-keratin beneath. The outermost keratin is derived
mechanical strength and thickness, and it is an important from a single layer of β-cells and is termed oberhautchen. This
underlying support for the epidermis above it. is a unique constituent of the epidermis of lepidosaurs and
The epidermis of snakes consists of a layered structure gives rise to the sculptured patterns that adorn the surfaces
including both dead and living cells. Two principal types of of scales (see below). Beneath the oberhautchen are several
keratin are present, each adding strength and rigidity to the more cell layers of β-keratin. Evidently, the function of the
scaled surfaces. Keratins are fibrous proteins that are entire β-layer is largely mechanical. The presence of this
formed when living cells—keratinocytes—die as they ma- stiffer type of keratin serves to maintain the shape of a scale
ture and synthesize protein fibers. The resulting matrix of (see below) by acting in equilibrium with forces that are gen-
keratin fibers is simply called keratin, a word that is also syn- erated by the complex arrangement of horizontal struts and
onymous with corneous or cornified layers. Whereas mam- vertical columns of collagen fibers within the dermis.
malian skin has only one type of keratin, α-keratin—which The β-keratin is separated from the α-keratin layers
gives rise to nails, claws, and hair—the skin of snakes con- deeper below by a thin layer of strand-like keratin known as
sists of both α-keratins and β-keratins. The latter resemble the mesos layer. The mesos layer is a highly specialized re-
the very stiff keratins that are characteristic of bird feathers. gion that is rich in lipids and comprises the barrier to water
These two classes of keratins occur in separate horizontal movement, thus serving as a check against excessive losses
layers that are arranged vertically in snake skin. All of the of water to the environment. A complex mixture of lipids is
keratinized layers of the epidermis—termed the stratum secreted from specialized organelles into extracellular
corneum—are derived from living cells that proliferate from spaces where they become organized into flattened layers
a basal layer lying above the dermis (figs. 5.3, 5.4). that envelope, and alternate with, layers of keratin. Several
Structure and Function of Skin | 119
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Figure 5.3. Schematic illustration of the generalized skin structure in snakes. Two generations of epidermis are shown, representing the outer
generation (OG) of tissue that will be sloughed from the body during skin shedding, and the inner generation (IG), which is new epidermis that
is formed before the older OG is shed. The outermost thin layer of beta (β) keratin is termed oberhautchen and bears the microsculpturing that
is discussed elsewhere in the text. The mature α- and β-keratin layers collectively comprise the stratum corneum, and are derived from the
living layer of stratum germinativum cells below. The stratum germinativum cells lie against a basement membrane, which separates the
epidermis from the dermis with its blood capillaries below it. The mesos layer is a layer of specialized cells that separates the β- and α-keratin
and contains lipids that comprise the water permeability barrier. Another zone of specialized cells (not labeled) separates the inner and outer
generations, which split apart in this region during shedding of the OG. Drawing by Dan Dourson, after fig. 1 in H. B. Lillywhite, Water relations
of tetrapod integument, Journal of Experimental Biology 209:202–226, 2006.
layers of α-keratin occur immediately below the mesos The size, geometry, and gross structure of scales also
layer, followed by living immature α-cells yet to undergo ke- vary from species to species, and regionally on the body.
ratinization. These α-cells differentiate from the basal layer Generally, the ventral scales (termed scutes) are broad and
that marks the inner boundary of the epidermis (fig. 5.4). extend from side to side as one single structure (fig. 5.6; see
also fig. 1.6). There are exceptions to this morphology, how-
Scales ever, and the ventral scales are much smaller or equivalent
The layered distribution of cell types occurs over the entire to dorsal body scales in file snakes (Acrochordus spp.), many
body surface, but regional differences of thickness are re- sea snakes, and species in some other taxonomic groups
lated to the structure of scales. The skin of snakes and (fig. 5.7; see also fig. 3.1). The scales on the remainder of the
other squamates develops within the embryo as a surface trunk tend to be rather uniform but variable among species
that becomes folded into scales. Each fold, or scale, has an (figs. 5.8, 5.9). The scales on the head also vary considerably
outer and inner surface creating a region known as a hinge. depending on the species of snake.
The hinge regions are more flexible than either the outer or Scales in various taxa have evolved to be small and gran-
inner scale surfaces and enable the epidermis to be de- ular (e.g., as in file snakes, Acrochordus spp., and some other
formed when the snake moves. They also permit consider- marine species), large and flattened (as in boas and pythons,
able stretching when a swallowed prey item expands the various elapids and colubrids), or thickened with cornified
skin. Indeed, when a snake is engorged with a large prey keels, projections, or other structures (various vipers and pit
item it has eaten, the area of exposed hinge tissue may ex- vipers). Scales having a relatively smooth and usually flat-
ceed that of the scales that occur in between (figs. 2.19, tened surfaces are termed smooth in contrast to scales having
2.31, 2.32). The epidermal covering of the hinge region is a visibly roughened appearance attributable to a small spine
usually thinner than that of the other scale surfaces. More- or a central longitudinal ridge, which are termed keeled (figs.
over, the β-layer is relatively thin on both the hinge and 5.8, 5.9; see also figs. 1.16, 1.26–1.29, 1.33, 1.46–1.48). This ter-
inner scale surfaces compared with the outer scale surfaces minology refers strictly to the external appearances of scales
(fig. 5.5). when these are viewed with the naked eye.
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Figure 5.4. Photomicrographs featuring
histological features of the skin of Dumeril’s Ground
Boa (Acrantophis dumerili). The upper image
illustrates cell layers in skin during the resting
stage prior to epidermal renewal of a shedding
cycle. The alpha (α) and beta (β) keratin layers are
separated by the mesos layer, which tends to split
as an artifact of preparation due to the presence of
lipids that form the permeability barrier against
water loss. The stratum germinativum (sg) is a
living layer of cells that gives rise to all the
keratinized cells above it. The basement
membrane of the sg separates the epidermis from
the dermis below. The middle image features an
early stage of epidermal renewal. The α- and
β-keratin layers of the outer (o) and inner (i)
generation of epidermis are separated by a clear
layer that becomes a zone of separation when the
old outer epidermis separates from the new inner
generation epidermis. The oberhautchen layer
(Obi) of cells forming in association with the inner,
renewing epidermis is seen just below the clear
layer. It will keratinize to become the thin,
outermost surface layer of the β-keratin to become
the new epidermis. Immature cells that will
contribute to the β- and α-keratin of the new
generation are seen between the stratum
germinativum and the newly keratinizing β-layer of
the inner generation (βi). The lower image shows
a biopsied scale in the late renewal phase
approximately two days before shedding of the
outer epidermis. Lacunar tissue can be seen just
above the region of epidermal separation (clear
layer), and the oberhautchen, remaining β-layer,
and much of the α-layers of keratin have completed
maturation in the inner epidermal generation, so
that only a few immature cells can be seen above
the stratum germinativum. Photomicrographs by
Elliott Jacobson.
The outermost (oberhautchen) surfaces of snake scales features to the lives of snakes that exhibit various sculp-
bear microscopic patterns of sculpturing, referred to by tured patterns.
various names such as microornamentation, microdermato- Patterns of microsculpturing seem likely to influence the
glyphics, microstructure, microarchitecture, and other terms. exchange of radiant energy, heat, and evaporation of water,
The patterns of microsculpture have been revealed by but these possibilities have not yet been rigorously investi-
scanning electron microscopy (SEM), which produces en- gated. There is strong circumstantial evidence that the mi-
larged images of minute structures on the surfaces of croscopic surface morphology of some burrowing species
objects. Scanning electron micrographs have shown that acts to prevent the adhesion of dirt, and the scale surfaces
the scale surfaces of various snakes are sculptured in of many snakes are hydrophobic and repel water (fig. 5.11).
complex patterns of minute ridges, spines, and other pro- The prevention of wetting at the surfaces of snake epider-
tuberances (fig. 5.10). Specific patterns of microsculptur- mis may well be important with respect to the potential
ing are characteristic of particular taxa of snakes, and problem of swelling, which results from hydration of kerati-
these characters have been proposed for use as diagnostic nous tissue. Such swelling might physically disrupt the me-
characters. Less is known about the significance of these sos layer and thereby impair the permeability properties of
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Figure 5.5. Photomicrograph of a histological section through the skin of Dumeril’s Ground Boa (Acrantophis
dumerili). The section illustrates both the outer and inner regions of the scale during the resting phase when one
generation of the epidermis is present. The beta (β) keratin is thicker on the outer scale surface and is represented
only by the thin oberhautchen on the inner scale surface. The mesos layer can be seen as strand-like material
between the β- and α-keratin, an artifact of separation especially at the right end of the scale. The cells with bluish
nuclei comprise the stratum germinativum. Section was stained with H & E. Photomicrograph by Elliott Jacobson.
or that live in areas of high rainfall. Moreover, some natri-

cine species of snakes are known to overwinter in circum-
stances where they are entirely immersed in water at the
blind ends of burrows. The hydrophobic properties of the
outer scale surfaces thus might function partly to prevent
the inward diffusion of unwanted water that otherwise
contacts the skin.
The shape, orientation, and pigmentation of scales
might also influence rates of radiative heat exchange and
consequently the temperature and evaporation characteris-
tics of the skin. It need not be inferred, however, that the
water or thermal relations of snakes are necessarily signifi-
cant selective forces that have shaped the topography of the
Figure 5.6. A Chinese Green Tree Viper (Trimeresurus stejnegeri)
integument. On the other hand, nor do the characteristic
rests on a branch, revealing the width of the belly scutes in
comparison with the dorsal and lateral body scales. This photo
microsculptured patterns appear to be simply a by-product
features a Taiwanese specimen and is courtesy of Ming-Chung Tu. of the splitting of the corneous layers of old from new epi-
dermis during skin shedding, an idea that has been a sub-
ject of some discussion. My own observations have revealed
the skin. Numerous snakes are exposed to water for signifi- that the outer keratinous surface of the spectacle covering
cant periods, especially species that are aquatic or semiaquatic, the eye is not sculptured like the other scale surfaces, but
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Figure 5.7. Underwater view of a Yellow-bellied Sea Snake (Pelamis platurus) illustrating the single row of ventral scales. Broad ventral scutes
are simply absent. This is no doubt an adaptation for swimming because the snake flattens its body in the dorsoventral plane, and the
lowermost aspect (belly) becomes a flattened keel with rows of scales not greatly different from the rest of the body. The inset shows the ventral
keel in more detail. This snake was photographed in Costa Rica by Joseph Pfaller.
rather is comparatively smooth to permit the unobstructed roughness of scale surfaces is more common in marine than
entry of light. Therefore, given the regional variation, the in terrestrial snakes, that the condition is more pronounced
microsculpturing patterns on various scale surfaces cannot in male snakes, and that roughness of scale surfaces might
be a simple nonadaptive product of skin shedding. assist the positioning of males during courtship. The ro-
There is one feature of the epidermis that appears, how- ugher surfaces that are characterized by spines or pro-
ever, to be a physical coincidence of the structure. The outer truding structures are more highly innervated and likely to
skin of a newly shed snake may be colorful with iridescence be sensitive to tactile cues, and they also enhance friction
that results from the physical interaction of visible-spectrum between male and female when the bodies are in contact.
radiation with the sculptured surfaces. The patterns of mi- The surface structures might also play a hydrodynamic role
crosculpturing act as a diffraction grating and project colors in modifying water flow over the body. The authors demon-
of the spectrum when light is reflected in specific patterns strated that the rougher scale surfaces reduce the boundary
from the opaque edges of the sculpture pattern (fig. 5.12). layer over the body and create more turbulent flow, which
These appear to be incidental structural colors that are unre- they suggest might enhance the cutaneous exchange of re-
lated to any adaptive meaning or significance. The brilliance spiratory gases during activities such as courtship.
of these colors is most intense just after shedding and fades The nanoscale structures of microsculpturing on scale
as time passes, probably due to the gradual wear or the accu- surfaces also have important implications for locomotion.
mulation of minute debris upon the oberhautchen surfaces. The surfaces of ventral scales exhibit highly organized ar-
In at least some species, it has been shown that the sculp- rays of microfibrilar projections or “micro-hairs” that point
turing of scale surfaces differs between the sexes. This sub- in the posterior or caudal direction and are separated by
ject has been studied in some detail for sea snakes by Carla sharp grooves (fig. 5.13). Each microfibril is from one to a
Avolio, Richard Shine, and Adele Pile at the University of few hundred nanometers in diameter, based on measure-
Sydney. They have suggested that sexual differences in the ments in boid snakes. These create an asymmetry with
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respect to the frictional properties of the scales, which ex-
hibit low friction for forward motion relative to backward
motion (see also chapter 3).
Finally, there have also been observed systems of micro-
pores penetrating the oberhautchen surfaces. These are
speculated to be a possible delivery system for lipids that
might provide surface lubrication, enhance resistance to
water loss, or expel chemical attractants related to courtship
(see chapter 9). The real function of such pits has not been
demonstrated, however, and requires further research.
Ecdysis: The Shedding of Skin

Snakes periodically shed their skin, a phenomenon that oc-
curs in all lepidosaurs and is usually referred to as shedding,
sloughing, or ecdysis. Skin shedding was well known to the
ancients, and there is considerable mythology and folklore
related to the subject. Snakes shedding skins have become
powerful symbols of rebirth and renewal (fig. 5.14).
It is generally well known that snakes initiate the act by
rubbing the snout or head against an object, which loosens
the skin and breaks it away from the new skin beneath
(fig. 7.4). As the snake crawls forward, it literally crawls out
of the old skin, which turns inside out and is left behind in
the process. There are certainly subtle variations on this
theme, but the procedure is generally similar in all species,
and in normal circumstances the old skin is left behind as
one entire piece rather than being shed in patches. Some
aquatic species of snakes living where rough objects are not
generally present to assist skin shedding may tie themselves
into loose knots and use their own body to push or pull the
old epidermis backward and off the trunk or tail. This be-
havior has been observed in pelagic sea snakes (Pelamis pla-
turus) and in file snakes (Acrochordus granulatus) (fig. 5.15).
The shed skin is soft and moist at first, but it soon dries
to become relatively brittle. It appears whitish in color and
translucent, being quite thin upon careful inspection; for it
is only a mature generation of epidermis that is shed, and
not the next immature generation of epidermis or the
thicker dermis that lies beneath.
Paul Maderson first described in detail the cellular
changes that take place in the skin of a snake throughout
Figure 5.8. Photos featuring the body scales of three species
of snakes. The upper photo shows a Florida specimen of Eastern
the shedding cycle. Many subsequent studies have empha-
or Black Racer (Coluber constrictor), which has smooth scales. sized the wonderful complexity of the cycle especially in the
The middle photo reveals the keeled scales of a Florida Green context of the interaction between intrinsic and environ-
Water Snake (Nerodia floridana). In the lower photo a male mental factors in its control. The entire shedding cycle is
and female Rough-scaled Bush Viper (Atheris squamiger) surprisingly complex, and the controlling influences are
are seen resting together. These snakes have very rough
still very much a mystery. Here we shall explore only a brief
scales with prominent central ridges and spiny tips, especially
prominent in the male (at left). The upper and middle photographs overview of the relevant morphological changes that occur.
are by Dan Dourson, and the lower photograph is by Elliott A mature generation of epidermis (epidermal generation:
Jacobson. figs. 5.3, 5.4) consists of a keratinized layer of β-keratin, with
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Figure 5.9. Photographs of skin surfaces of a Yellow-bellied Sea
Snake (Pelamis platurus) (upper photo), Shaw’s Sea Snake (Lapemis
curtus) (middle photo), and an Eastern Diamondback Rattlesnake
(Crotalus adamanteus) (lower photo). The scales of Pelamis are
tuberculate and well separated with flattened surfaces. Note there are
small spinules or spots in the middle of the scale surfaces (arrows).
These are almost certainly sensory structures, but they have not been
studied in detail morphologically or physiologically (see chapter 7).
Prominent keels with central spines (arrow) are seen on the lateral
scales of Lapemis, which is a male and develops such scale roughness
during the mating period. The scales of the rattlesnake are keeled,
and each dorsal scale has a central ridge, or “keel,” running its length.
The belly scutes are shown in the lower part of the figure. Note that
there are transitional scales between the ventral scutes and dorsal
scales that do not have ridges. The direction of orientation with
respect to the snake is head-to-tail from left-to-right. The sea snakes
were photographed in Costa Rica (Pelamis) and Australia (Lapemis).
The rattlesnake was photographed in Florida. All snakes were living
specimens photographed by the author.
sandwiched between alternating layers of lamellar lipids as

described above. Keratinized α-keratin occurs beneath the
mesos layer, formed from multiple cell layers similarly to the
β-layer. Below the α-keratin there is a transitional region
wherein mature keratin merges with immature α-cells that
are in various stages of keratinization (fig. 5.4). All of the
living cells that contributed to these described layers are
derived from the stratum germinativum at the innermost
base of the epidermis, overlying the dermis beneath.
Immediately following ecdysis, the new generation of
epidermis is more or less in the state just described, and it
may remain that way for some time that is known as the
“resting stage.” After some while, which can vary from weeks
to months, the skin enters a “renewal stage” in which a new
inner generation of epidermis begins to form beneath the
older, mature outer generation of epidermis (fig. 5.4). Essen-
tially what happens is that cells proliferate from the basal
germinal layer and begin to keratinize as they accumulate
between the outer generation and the stratum germinativum.
Progressive keratinization of these newly proliferated cells
produces a new generation of epidermis that is nearly ma-
ture by the time of shedding. Thus, at ecdysis there is a ma-
ture outer generation of epidermis that overlies a newly
formed, but not quite mature, inner generation of epidermis.
The extent of development of the new, inner generation α-
layer varies considerably at the time of ecdysis.
One further detail regarding these tissues requires com-
ment. Prior to formation of the new β-layer belonging to
the inner generation, several layers of unusual cells form at
the microsculptured oberhautchen forming the outermost the base of the outer generation. These cells separate the
surface contacting the environment. The entire β-layer is two generations of epidermis, although technically they are
derived from multiple cell layers. Beneath the β-layer is the part of the older outer generation because they disappear at
mesos layer, consisting of several thin layers of keratin the time of shedding. These cells are called “lacunar cells,”
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The process of shedding is aided evidently by fluids that
penetrate these tissues at the time of shedding, but the na-
ture and control of such fluids are not well understood. The
“fluid” may contain water and/or lipids and accounts for the
generally damp nature of the shed generation of epidermis
immediately after it is shed from the snake’s body. Enzymes
that degrade some of the clear layer and lacunar tissue are
also present at the time of shedding.
Periodic shedding occurs in all snakes, and it seems that
the general features of epidermal renewal are similar in all
species. Characteristically, the renewal and shedding of the
epidermis is a synchronized cycle of events that occur
simultaneously over the entire body, rather than in patches.
The periodicity of shedding, however, varies. Some snakes
may shed their skins only once or twice per year, whereas
others shed more frequently (sea snakes, for example).
Because the keratin in the scales of snakes is a rigid mate-
rial, shedding is required to permit growth. Thus, shedding
can be expected to relate generally to the growth of snakes,
and those snakes with the higher inputs of food might be
expected to shed more frequently than others, assuming
that all other factors are equal.
Other factors, however, can also influence the frequency
of shedding, independently of growth per se. Sea snakes
shed their skin relatively frequently, sometimes at two- to
six-week intervals. One of the reasons is thought to relate
to removal of fouling organisms that can tend to grow on
the outer surfaces of these snakes. Barnacles, bryozoans,
Figure 5.10. Scanning electronmicrographs illustrating and algae have all been found growing on the skin of sea
microsculpturing on the surfaces of snake scales. The upper photo
snakes (fig. 5.16). It is also thought that shedding is impor-
shows part of the dorsal scale from an African Stripe-bellied Sand
Snake, Psammophis subtaeniatus. The surface oberhautchen in this tant to renew epidermis that might become damaged over
species illustrates a pattern of ridges separated by shallow crevices time, likely involving minute breaks or fractures in the per-
sculptured with tertiary spaces and ridges. The rear (or caudal) end of meability barrier. Thus, an important function of shedding
the scale (and snake) is toward the right side of the micrograph. The might also relate to renewal or possibly improvement of the
lower photo features the rear part of the dorsal scale from a Russell’s
permeability barrier in relation to environmental influ-
Viper, Daboia russelii. The oberhautchen scale surfaces in this species
consist of elevated knobs or projections, each having a honeycombed
ences on water balance.
surface and being increasingly elevated in the central part of the Many snakes shed their skin within a few days following
scale, which forms a “keel.” The rear of the scale (and snake) is toward birth or hatching. Working in my laboratory at the Univer-
the bottom of the micrograph. Each black scale bar is 10 μm, and the sity of Florida, Ming-Chung Tu and I discovered that in
lower micrograph is at a higher magnification than the upper one. California King Snakes (Lampropeltis californiae) this initial
Micrographs are by the author.
ecdysis results in a doubling of the skin resistance to evap-
orative water loss, and the resistance increases still further
and the single layer of cells overlying the oberhautchen of following the second ecdysis. These phenomena might ex-
the new inner generation is called the “clear layer.” The plain some behaviors of newborn snakes, which often re-
tissue of the clear layer interdigitates with the sculptured main either with a parent in some viviparous species (e.g.,
surfaces of the inner (new) generation of oberhautchen and certain pit vipers) or at the site of hatching from eggs until
essentially “unzips” from it during the actual process of the first ecdysis, after which the young snakes disperse
shedding when the two generations of epidermis separate. away from the site of birth. Remaining more reclusive right
Thus, the shed “skin” that is lost from the snake at ecdysis after birth might conserve evaporative losses of body water
consists of the outer generation β-layer (including ober- during the period before the first ecdysis when evidently
hautchen) and α-layers of keratin, including the lacunar the permeability barrier to water loss has not yet been es-
cells and clear layer. tablished (see chapters 2 and 9).
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Skin Color: Causes, Patterns,
Significance
Colors are wonderful, and without them
snakes would be far less interesting. Ima-
gine if every snake you encountered or
saw featured in a film was the same drab
color of pink or gray. Boring? But, in fact,
snakes have myriad colors and patterns
of color in their skin, not all of which is
genetically determined by the expression
of pigments. First, we shall examine the
physical basis of coloration, and then
turn to some interesting topics related to
its significance.
The Physical Basis of Color

What we call “color” results from the vi-
sual perception of specific wavelengths
of electromagnetic radiation. Radiation
wavelengths between 400 nm and 750
Figure 5.11. Water droplets are shown beaded on the surface of a Fer-de-Lance
nm comprise what is called the “visible
(Bothrops asper) photographed in Belize by Dan Dourson (upper photo). A higher
spectrum” of light, with reference to the magnification of the phenomenon is illustrated on the shed epidermis from a sea krait,
visual capabilities of the human eye. Laticauda semifasciata, photographed by the author (lower photo). The scale surfaces
Other animals, including some snakes, are hydrophobic and repel water; thus the surface tension forces cause the water
can perceive wavelengths somewhat droplet to assume a near-spherical shape instead of spreading to form a flatter film.
outside this range. The colors we see are
attributable to wavelengths of light that is reflected back
from an object (say, skin) to enter our eyes, where it ex- species of blind snake (Leptotyphlops humilis), but the sug-
cites visual receptors that are categorically different de- gestion is anecdotal.
pending on which wavelengths they are “tuned.” This Most of the color we see in snake skin, however, is attribut-
excitation of visual receptors is passed on to the parts of able to the presence and pattern of chemical compounds we
the brain responsible for interpreting visual sensation by call pigments. Most of the pigments involved are fixed within
means of nerve signals that pass along the appropriate the skin, but the lighter skin regions of some snakes may turn
pathway of interconnected neurons (single nerve cells). from pinkish to white depending on the amount of blood that
Wavelengths of light that are either absorbed by the skin is flowing through the skin. In this case, the pink or reddish
or transmitted through it do not contribute to the colors coloration is attributable in large part to reflectance of light
we see. We see only the components of light that are re- from hemoglobin within the red blood cells. Hemoglobin is a
flected back to our eyes. respiratory pigment and carries oxygen around the body (see
Skin color results from complex interactions among the chapter 6). Nevertheless, it is called a pigment because of its
chemical and physical properties of the tissue. What is light-reflecting properties that impart color to it.
known as structural color is that component of coloration Pigments that are fixed within the skin are synthesized
which is attributable to physical features of the skin other within cells called chromatophores. There are four principal
than pigments. For example, the microsculpturing pat- groups of chromatophores that contribute to the coloration
terns on the surfaces of scales create patterns of wave- of snakes. The more common, widespread, and better kn-
length interference that produce iridescent colors, own of these is the melanophore, an irregular-shaped cell
especially prominent right after skin shedding, when the that contains the pigment melanin. Melanin is a dark pig-
skin surfaces are new and clean (fig. 5.12). The physical ment derived from the oxidation products of tyrosine and
properties and geometry of keratin organization in the dihydroxyphenol compounds. The color can vary from dark
skin can determine what wavelengths of light are selec- red to dark brown or black. Melanins are present in the skin
tively absorbed, refracted, or reflected. Fluorescence—the and are also found associated with some of the internal
emission of light from a surface after it has absorbed radi- organs of an animal. There are two kinds of melanophores
ation from an outside source—might possibly occur in a in the skin. Dermal melanophores are broad, flat cells that
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Figure 5.13. Microstructural projections on the surface of a ventral
scute from the African Stripe-bellied Sand Snake, Psammophis
subtaeniatus. The head-to-tail direction of the projections is from top
to bottom in the photograph. The black scale bar at the bottom of the
photograph equals 5 μm. Minute pores can be seen in the regions
between the elevated projections running parallel with the length of
the snake (arrows). Scanning electron micrograph by the author.
termed erythrophores contain oil with heterocyclic com-

pounds called pteridines, and are reddish in color. Some
consider the erythrophores to be a type of xanthophore
that is reddish in color, in contrast to the other xantho-
Figure 5.12. Photos of a Cross-barred Tree Snake (Dipsadaboa phores that are yellow in color. Silvery chromatophores
flavida) (upper photo) and a Rainbow Boa (Epicrates cenchria) termed iridophores do not contain true pigments but con-
(lower photo) illustrating iridescent scale colors attributable to tain crystals of guanine. Guanine is a purine that reflects
structural features of the epidermal surfaces (not pigments). Note the light and imparts a noniridescent bluish or silvery white
blue and green colors on the edges of the scales and head plates,
color. The color varies depending on the scattering of light
which are due to reflected light patterns dependent on the direction
of lighting. Such structural colors are most vivid just after a snake has
and the surrounding pigments in the skin. They may also
shed its skin. These are captive snakes owned by Ron Rozar and contain derivatives of other purines, and the combination
photographed by the author. of different crystals determines the variety of hues that
are produced by diffraction, scattering, and reflection of
light. The colors are structural and not attributable to true
occur in the dermis, whereas epidermal melanophores (also pigments. The different kinds of chromatophores may as-
called melanocytes) are thin, elongated cells that contribute sociate in the skin to produce various colors by virtue of
pigment to regions of the epidermis. Once pigment is pro- their reflectance of light and their collective interference
duced within melanocytes, it is “packaged” in a sense and with reflected light.
transferred to epidermal cells (keratinocytes) that will pro- In preserved snakes such as those in museum col-
duce keratin. Whether pigments are transferred between lections, the pigments contained in xanthophores and
the dermis and epidermis is an entirely unresolved issue. erythrophores are soluble in formalin or alcohol and thus
Pigment cells termed xanthophores contain oil-filled slowly leach from the skin. Melanins are insoluble, so
vesicles with suspended pigments called carotenes that over time the colors of preserved snakes fade except for
are yellowish or orange in hue. The carotenes are taken up the patterns that are attributable to the distribution of
from the diet and are related to vitamin A. Pigment cells melanins.
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Figure 5.14. Part of the Mayan-Toltec ruins at Chichen Itza, Mexico. This wall is covered with iconography depicting many snakes, the larger
one at the top representing the Mayan snake deity Kukulkan, or “Plumed Serpent.” Feathers, or plumes, can be seen to decorate the stones at
the top of the wall and just beneath it. Many of the other snakes represented in this stone structure clearly represent rattlesnakes. The white
arrows point to some of the rattles at the tails of these stone serpents. Photograph by Ming-Chung Tu.
The Functions of Color Pattern that influences body temperature. Investigations by Har-
Anyone familiar with even a modest sampling of the diver- vey Pough, James Jackson, and their coworkers suggest
sity of snakes knows that they come in a variety of colors there is a correlation between the dorsal color pattern of
and patterns of color, which to the novice might not make snakes and the manner in which they respond to preda-
much sense in terms of understanding reasons for the vari- tors. Snakes with uniform colors or disruptive patterns of
ation. Some snakes such as desert vipers appear quite well blotches, spots, or irregular crossbands tend to rely on
camouflaged against a background of sand (fig. 3.16), and crypsis, or concealment, to avoid being seen by potential
thus we might suppose that diffuse, buff colors fit that predators. Some excellent examples are blotchy or speck-
purpose. Others seem brilliantly colored with amazing led vipers that blend with their background when viewed
patterns of rings, bands, or blotches, and these are not nec- upon rocky or course soils (fig. 1.25, 3.16); green or brown
essarily cryptic (camouflaged). Still other snakes might ap- tree snakes that are concealed in green foliage or twigs
pear dull when viewed from above, but the underside is a and branches, respectively; and blotched or banded
brilliant color that is obvious when presented by turning snakes when viewed among leaves (figs. 1.28, 1.29, 1.33,
over or curling the tail (figs. 1.48, 1.50). Considering all that 3.16, 5.17). Many of these species also defend themselves
is known about these various color patterns reveals some with aggressive behaviors when the concealment fails.
generalizations regarding their function. Thus, many viperid species will coil and strike when dis-
We begin by regarding color patterns to be phenotypic covered by a human or other animal, rather than fleeing
traits, which in some manner “fit” a snake to its environ- to escape. This behavior also tends to correlate with a
ment. The contexts of “purpose” usually have to do with lesser ability to crawl rapidly. These are generalizations,
antipredator behaviors, social interactions, or the physical however, and there are many exceptions involving indi-
environment—for example, the relative heat absorption viduals or even species.
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Figure 5.15. Left: Knotting behavior in a pelagic Yellow-bellied Sea Snake (Pelamis platurus) photographed in Costa Rica. The knotting
behaviors of sea snakes are thought to be employed to remove debris and potentially settling ectoparasites (barnacles for example) as well as to
remove old epidermis during skin shedding. The specimen shown in this photograph is not shedding its skin. Right: A Little File Snake
(Acrochordus granulatus) photographed in the Philippines. The snake is outside of water to illustrate a “knot” that was being used to remove old
epidermis during skin shedding. The arrows point to the location on the body where a tight coil (above arrowheads) is being used to push
against part of the body where the old epidermis is sliding toward the tail and off the snake (below arrowheads). The old epidermis can also be
seen as the wrinkled skin in the lower part of the photo. The greenish color is attributable to the presence of algae. The anterior part of the
snake from which the skin has been removed is evident in the upper part of the photo. The photograph of Pelamis is by Joseph Pfaller, and that
of the Acrochordus is by the author.
On the other hand, snakes that possess colors forming velocity of an object depends on the color pattern of the
stripes or more uniform patterns than those discussed object and its surrounding field on which it moves. Striped
above tend to be more active and rely on rapid escape by snakes appear to be stationary when crawling slowly, and
fleeing away from potential predators. Herpetologist Ed- they can appear to be moving more slowly than they actu-
mund Brodie III found this to be true even within a species ally are. It is difficult for the eye of the predator to “fix” on a
when he investigated color patterns of individuals of the particular point on the fleeing snake and follow it, so the
Northwestern Garter Snake, Thamnophis ordinoides. Indi- result can be that the stripe is seen momentarily but then
viduals of this species have colors that vary from distinct suddenly the tail appears in a flash and the striped object
stripes to patterns of spots. When Brodie measured the vanishes! This optical illusion clearly has advantages for the
tendencies of snakes to flee following provocation, he found escaping snake and suggests the striped pattern may be
that striped snakes tended to crawl away from the ag- more effective in permitting escape than does some other
gressor, whereas snakes with more blotched patterns were color patterns when fleeing is involved. The striped pattern
more likely to flee a short distance and then suddenly stop becomes more apparent with increasing size of garter
and assume a motionless position. Such behaviors are snakes, and the tendency to flee from threats intensifies in
termed “reversals” and reflect a behavioral component of older striped individuals of Thamnophis ordinoides.
crypsis that is employed following the initial detection of Ed Brodie III also studied natural selection for combina-
an animal by a predator. It is a defensive tactic that does not tions of color pattern and escape behavior in a population
rely greatly on speed. The behavior confuses a predator of T. ordinoides. Newborn snakes that were scored for be-
when a fleeing animal that is being followed rapidly and havior and color pattern in the laboratory were released
suddenly “disappears” (when it stops). into the wild, and their survival was followed by mark and
Optical illusions can be created by moving color patterns recapture techniques. Snakes with the highest probability
and their effects on visually foraging predators. Studies of survival performed uninterrupted flight if striped, but
have found that the ability to perceive motion and the tended to flee evasively by performing reversals if they were
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Figure 5.16. Barnacles encrusting into the skin atop the head of an
Olive-headed Sea Snake, Disteria major. The lower photo shows a
closer-up view of two such barnacles. Photographs by Sara E. Murphy.
spotted or nonstriped. The covariation of color pattern and

behavior help to explain the variation of color pattern that
is seen in natural populations of this species.
Another important function of snake colors is that of
a warning signal to predators. The warning function is
termed aposematism and is probably best known in coral
snakes of the genera Micrurus and Micruroides. These
Figure 5.17. An Eastern Diamondback Rattlesnake (Crotalus
snakes are conspicuously colored with usually red, yellow, adamanteus) resting on a sand dune at Sapelo Island, Georgia. From
and black bands, which function as a warning signal to a distance (upper photo) the snake (arrow) is almost completely
avian predators. Aposematic colors are most effective cryptic and difficult to see. At reasonably close range (middle photo)
when they contrast strongly with that of the animal’s the snake remains cryptic. Only if the observer is right upon the snake
background, and the warning colors tend to be avoided by does it become conspicuous (lower photo). Photographs by James
Nifong.
would-be predators. Such contrasting colors have also
been shown, or suspected, to be aposematic in other spe-
cies of snakes including some sea snakes, other elapids,
colubrids, and viperids (figs. 1.14, 1.41, 1.52 and below). function (fig. 1.25). The dorsal colors can reduce the detec-
A very interesting example of an aposematic color pat- tion by avian predators while the snake is coiled motionless,
tern occurs in European Vipers, Vipera berus, which have a but change into a highly conspicuous and characteristic sig-
dorsal zigzag pattern that has been shown to be aposematic. nal once the snake has been seen. Moreover, the pattern can
The zigzag pattern of European vipers is not very conspic- create a “flicker-fusion” illusion during movement, which
uous and could also have both a cryptic and aposematic makes it difficult for a predator to focus on a moving snake
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and thereby increases the chances for escape. Many snakes
are brightly banded, and during rapid crawling movement
the bands create a similar effect, or they blur to produce a
seemingly uniform color that also enhances escape by
fleeing. A similar effect occurs in swimming sea snakes,
many of which have banded coloration (figs. 1.43, 1.45).
Numerous venomous snakes possess potent venom and
irritable defensive behaviors, but are cryptically colored
and not conspicuously marked like the European vipers.
The use of such weak color signals combined with strong
defenses is a common phenomenon (see writings by John
Endler). Many snakes are preyed upon largely by birds, and
a number of these birds are specialists that feed primarily
on snakes. If some predators avoid venomous snakes be-
cause of their coloration, while others do not, it makes
sense to employ a color strategy that involves crypsis to
avoid being seen by predators, while also having an apose-
matic function once an individual is seen.
Other examples of warning coloration include tail
curling or exposure of ventral surfaces, which are brightly
colored in various species of snakes (figs. 1.48, 1.50). The
arboreal Red-tailed Rat Snake (Gonyosoma oxycephalum) of
Southeast Asia presents blue colors to predators when it
Figure 5.18. The upper photo shows the open mouth of a Brown
is in a defensive attitude, and similar defenses have also (or Mexican) Vine Snake (Oxybelis aeneus) and reveals dark blue
evolved in other arboreal species. The blue colors are some- coloration that is displayed within. In the lower photo one sees the
times revealed when body scales are spread apart by neck blue colors that decorate the tongue of a Red-tailed Rat Snake
inflation, or when the mouth is opened or the tongue is (Gonyosoma oxycephalum). This species also displays a dark blue
flicked (fig. 5.18; see also fig. 6.19). spot on the inside of the mouth when it is opened in a threatening
defensive display. The vine snake was photographed by Dan Dourson
in Belize; the rat snake was photographed by the author.
Mimicry
The term mimicry refers to the phenomenon where organ-
isms resemble one another in context of gaining an advan- insects appears to mimic snakes, and the sophistication of
tage in the avoidance of predators. Studies of coral snakes, the resemblance can be indeed remarkable (fig. 5.21). Trop-
in particular, have demonstrated the existence of mimicry ical millipedes with ringed patterns might also gain some
systems in which harmless snakes resemble or “mimic” advantage in resembling ringed patterns of snakes, but this
coral snakes in color pattern and thereby gain the benefit is simply speculation at present.
of signaling avoidance to avian predators (fig. 5.19; see also
figs. 1.14, 1.52). Field studies by Ed Brodie III have provided Melanism
direct evidence that avian predators avoid banded patterns Melanism refers to excessive pigmentation or blackening
of model snakes. Thus, there appears to be a generalized of the skin, usually determined by genetics and having
avoidance by free-ranging avian predators of ring patterns evolutionary origin. In some cases, melanism is deter-
resembling those of coral snakes. Other plausible but less mined by recessive homozygotes at a single gene locus.
tested systems might involve mimicry of viperid body form The significance of melanism has attracted the attention
and coloration by snakes such as American hognose snakes of biologists since the 19th century. As in other reptiles,
(Heterodon spp.; see fig. 1.49), or spreading the neck in a birds and mammals, melanism is quite common in snakes.
cobra-like fashion among various colubrid species of In some circumstances, the melanism in individuals may
snakes. Many such displays occur in snakes that are not be partial, and populations may reflect a mixture of me-
sympatric with an appropriate model species, however, lanistic and normally colored individuals representing
and are likely to represent convergent evolution of defen- either rare or well-established polymorphism. There are
sive tactics (fig. 5.20). several plausible advantages for melanistic individuals,
Mimicry involving snakes might also extend to other depending on the environment, ecology, and behavior of a
kinds of organisms. For example, coloration of some tropical species.
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Figure 5.19. Coral snakes and coral snake mimics. The upper left photo is an Eastern Coral Snake (Micrurus fulvius), paired with a sympatric
mimic (upper right), a Scarlet King Snake (Lampropeltis elapsoides). The middle left photo is a Central American Coral Snake (Micrurus
nigrocinctus), paired with a sympatric mimic (middle right), a Black Milk Snake (Lampropeltis triangulum gaigeae). The lower left photo
features a Brazilian Coral Snake (Micrurus decoratus), and the lower right photo features a Terrestrial Snail Sucker (Tropidodipsas sartorii) that
is common throughout much of Central America. Note the variation of banding and ring patterns, all of which can have a generalized advantage
of being avoided by avian predators. The Micrurus fulvius was photographed in Florida by Dan Dourson. The other snakes were photographed
by the author: Lampropeltis elapsoides in south Florida; Lampropeltis triangulum, Micrurus nigrocinctus, and Tropidodipsas in Costa Rica; and
Micrurus decoratus in Itatiaia National Park, Brazil.
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Figure 5.20. A Red Coffee Snake (Nina sebae) with threatening
display. This snake is normally secretive and when uncovered it
typically remains motionless (a behavior that has earned it the name
“dormiloma,” meaning “sleepyhead,” in parts of Mexico). However,
when startled or disturbed the snake may dorsoventrally flatten its
neck and part of its body, crawl forward, and elevate its head. The
snake also thrashes or moves its body jerkily to keep its red-colored
back facing toward a potential predator. Such a head and neck display
is relatively rare in snakes that are this small (maximum length 40 cm)
and probably serves to make the snake look larger or more
threatening. This snake was photographed in Belize by Dan Dourson.
One advantage clearly is cryptic in cases where black or

very dark individuals match a dark background (figs. 5.22,
5.23). Examples are darkly colored specimens of the South-
western Speckled Rattlesnake, Crotalus mitchellii pyrrhus, Figure 5.21. A Brazilian Hawkmoth caterpillar (Hemeroplanes
which occur on dark lava rock flows, as mentioned earlier, ornatus, = Leucorampha ornatus) inflates itself to resemble a snake
and the Arizona Black Rattlesnake, C. cerberus, which has a when it is frightened by a potential predator. The resemblance is
amazing, and the caterpillar sways from side to side in effort to
limited range in the vicinity of black lava outflows from an
improve the resemblance. The would-be predator might even think
ancient volcano (fig. 5.22). Another context for crypsis is a the false snake is striking! Photograph by Lincoln Brower.
match of dark skin color against charred backgrounds or
objects that result from wildfires. From personal experi-
ence, I know that Southern Pacific Rattlesnakes (C. oreganus
helleri, fig. 4.6) tend to be very dark in regions of Southern
California that have had a history of frequent fires. Al-
though wildfires are an ephemeral event, selection is very
intense for perhaps one to three or four years afterward be-
cause of increased appearance of aerial predators that tend
to forage in the open habitat. Moreover, charred stalks
from shrubs tend to remain dark in color for many years,
and the author has often confused these momentarily for
snakes while walking through recently burned habitats.
Another adaptive context for melanism is a presumptive
advantage for more rapid warming and thermoregulation in
relatively cool environments. This has been shown to play an
important role in a number of lizard species, as well as in
Figure 5.22. An Arizona Black Rattlesnake (Crotalus cerberus)
garter snakes and melanistic color morphs of the European
illustrating the predominantly black color that renders this snake
Adder, Vipera berus. Ralph Gibson, Bruce Falls, Tonya Bittner, cryptic when seen against dark rocks that are part of an ancient lava
and others have demonstrated that melanistic adult garter flow associated with its range. Photograph by William B. Montgomery.
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for melanistic color morphs in an island population of Vipera
berus by Claes Andrén and Göran Nilson.
Another function of dark pigmentation is protection of
reproductive and other critical organs from harmful ultra-
violet radiation. In various species, and particularly in those
inhabiting open habitats with intense sunlight, dense
layers of melanin can be found in the internal thin membra-
nous tissues that surround the gut (called peritoneum), re-
productive organs, and venom glands of venomous snakes.
These internal melanins, in addition to those present in the
skin, are thought to protect sensitive internal organs from
the harmful effects of penetrating UV radiation. Changes in
the amount of melanin and its dispersion throughout the
skin significantly affect the amount of radiation that pene-
trates the body wall. Studies of color-labile desert lizards by
Warren Porter and Kenneth Norris have demonstrated that
lightening of the skin color doubles the amount of UV and
visible radiation that penetrates the body wall to the perito-
neum and is potentially mutagenic judged by effects on
bacteria. Hence, the so-called “black peritoneum” is an im-
portant shield that guards against incoming radiation.
Changes of Color Pattern

The color patterns of snakes are generally fixed, and the la-
bility (especially short-term variation) of color change in
Figure 5.23. The upper photo features a Southwestern Speckled
any individual is not as pronounced as what occurs in some
Rattlesnake (Crotalus mitchellii pyrrhus) that has emerged from a
granite rock outcrop that was blackened by a recent wildfire. The
other taxa such as frogs, lizards, and fishes. However, it is
charred rocks in this habitat are typically pinkish-orange in color, fairly common for snakes to exhibit significant change of
which matches the color of the snake. The lower photo illustrates color pattern during development, with juveniles exhibit-
the normal pink color of rocks in the vicinity (before the fire). The ing blotched or banded patterns that transform to uni-
snake to the left is another Southwestern Speckled Rattlesnake formly colored or striped patterns in adults. In some cases,
(C. m. pyrrhus), and that to the right is a Southern Pacific Rattlesnake
the changes in color pattern correspond with changes in
(C. oreganus helleri). This photograph was taken in the early morning,
and shadows unintentionally exaggerate the dark colors. The speckled behavior and appear to be related to crypsis or escape
rattlesnake matches the rock more closely after it warms up and its strategies. For example, juvenile Cottonmouths (Agkistro-
colors lighten akin to the one in the upper photograph. The Southern don piscivorus) are orange or brownish in color with pat-
Pacific Rattlesnake, on the other hand, is naturally quite black. It is an terns of blotches and crossbands, whereas the adults are
obvious mismatch of color with the pink rock, but it is relatively
more uniformly colored brown or black (fig. 1.32 cf. fig.
camouflaged on the blackened substrate following a fire. These
snakes were photographed by the author in the southern Laguna
2.28). The colors of the juveniles tend to provide crypsis re-
Mountains of San Diego County, California. lated to a tendency of young snakes to spend more time
immobile in situations where there are leaves or other
ground vegetation in contrast to adults, which forage noc-
snakes (Thamnophis sirtalis) maintain significantly higher turnally in shallow water or muddy banks of ponds and
body temperatures (by about 1.3°C) during the colder periods streams. Put another way, the color pattern of juvenile cot-
of the day when compared with normally colored morphs of tonmouths resemble somewhat closely the color pattern of
this species. The higher body temperatures can influence the related Copperhead (Agkistrodon contortix), which is
rates of metabolism and growth of individuals, leading to very inconspicuous when coiled amid the leaf litter of a
increased reproductive success. Black morphs might also be hardwood forest (fig. 1.32). Unfortunately, there are no
active for somewhat longer periods of a year. However, mela- quantitative data to confirm the tendency of juvenile cot-
nistic individuals of a species may occur at particular loca- tonmouths to coil among leaf litter in comparison with the
tions, or at moderate to relatively low frequencies in a behaviors of adults.
population, due to being conspicuous and subject to increased Studies of the racer Coluber constrictor by Douglas Creer
predation. The increased predation risk was demonstrated demonstrated that newborn and juvenile racers were more
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likely than adults to exhibit aggressive behavior in con- in color pattern. Specimens that are captured on or near
trast to fleeing that is more characteristic of adults. The lava flows in the Mojave Desert appear nearly slate gray in
young snakes have a blotched color pattern in contrast color, whereas individuals captured on nearby areas of sand
with adults, which develop a more uniform color ranging or light substrate can be a peppered whitish color in appear-
from blue or brown to black. Generally, however, the sig- ance. The author has also seen specimens of variable colors
nificance of ontogenetic color changes in snakes is not well that generally match the predominant soils or rocks with
understood. which they associate, ranging from darker gray or bluish
The changes of color that occur during ontogeny in- tones through lighter, usually pinkish colors. Moreover,
volve fixed pigment patterns that do not vary substan- these snakes appear capable of changing their dorsal color
tially from day to day, and the transformation from pattern to match not only the basic ground color but also
juvenile to adult patterns is an example of what is called the speckled appearance of granite rocks in their habitat.
morphological color change. These take place over the life- Nonetheless, the fundamental ground color of these snakes
time of an individual, or might describe evolutionary appears to become “fixed” sometime during early ontogeny
changes in which the color pattern of a species changes (fig. 5.23).
over relatively long periods of evolutionary time. On the
other hand, shorter-term changes can occur over periods Acquisition of Color Directly from Environment
of minutes to hours in individuals experiencing hormonal Genetically based color patterns can also be affected by the
or nervous stimulation of chromatophores, termed physi- adherence of dirt or mud particles that a snake contacts
ological color change. While common in some other ani- directly in its environment. Generally, the skin of snakes is
mals, such changes are comparatively rare in snakes, kept exceptionally clean due, in part, to the hydrophobic
but they do occur. The distinction is that physiological nature of the microstructural properties of the epidermis.
changes involve the movement of pigment (usually mel- However, snakes that frequent muddy environments such
anin) into or out of dermal melanophore processes (to as stream banks, or which occur in dry habitats with wind-
cause darkening or lightening, respectively) whereas mor- blown dirt or sand, can accumulate a thin layer of debris
phological color changes involve increases or decreases in that alters the normal skin color. One example is the ad-
the absolute numbers of melanophores that are present in herence of mud to the skin of Cottonmouth snakes that
the skin. crawl over muddy surfaces associated with stream banks or
Physiological color change has been documented in sev- ponds (fig. 5.24).
eral families of snakes including viperids, boids, tropidophi-
ids, bolyeriids, and colubrids. In many cases it seems to be Genetics of Snake Coloration
cyclical and related to activity or 24-hour light cycles. In The genetics of skin color is not well studied in snakes, and
other cases, colors may vary seasonally and might be diffi- much knowledge of genetic systems and expression related
cult to detect by human visual systems. Scott Boback and to coloration has been derived from investigations of other
Lynn Siefferman studied such phenomena in Boa Constric- animals. Investigations of snake colors arise, however, in
tors and suggested that physiological color changes can be relation to two principal interests. First, evolutionary biol-
related to underlying hormone cycles involving melatonin ogists interested in coloration, evolutionary principles, or
and melanophore stimulating hormone (or MSH). The pat- natural selection recognize that snakes offer a diversity of
terns of color changes in snakes have probably evolved in fascinating color systems and are subject to selection pres-
relation to crypsis, thermoregulation, and sexual signaling sures that provide useful experimental systems for under-
in various species. standing the underlying genetic mechanisms related to
Some rattlesnakes tend to lighten with increased tem- certain patterns or variation. Second, herpetoculturists
perature or activity, and hormonal control of the relative are interested in breeding various mutant lines of color
state of melanin dispersion has been suggested to con- variants that have become popular in the pet trade. Var-
stitute the mechanism for controlling these changes. ious private and commercial breeding programs have
Early studies by Hermann Rahn revealed that high tem- yielded information about fundamental Mendelian ge-
peratures contracted melanophores in rattlesnakes, and netics of color in various strains or subspecies of interest
the state of lightening resembled that seen in response to buyers. Much of the knowledge related to these breeding
to surgical removal of the pituitary gland, which elimi- programs has not been published in the scientific litera-
nates the melanophore dispersing actions of pituitary ture, but is available from various individuals who are in-
hormones. volved (fig. 5.25).
The Speckled Rattlesnake, Crotalus mitchellii, of the Skin color in snakes and in other vertebrates can be sub-
southwestern United States seems to be particularly labile ject to relatively rapid natural selection and expressed by
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Figure 5.25. A working scene at Vida Preciosa International, Inc.,
better known as VPI. This is a commercial enterprise owned and
operated by David and Tracy Barker near San Antonio, Texas. VPI is
Figure 5.24. Florida Cottonmouths (Agkistrodon piscivorus conanti)
best known for its collection and captive breeding of pythons. Here
with skin colored by a superficial layer of dried mud that occurs in
Tracy is shown preparing eggs from the cage of a Red Blood Python
the snake’s natural habitat (Lower Suwannee National Wildlife
(Python brongersmai) for artificial incubation. Successful captive
Refuge). In the upper photo, two juvenile snakes are shown before
breeding of various python species at VPI has produced numerous
(left) and after (right) shedding the skin. In the lower photo, an older
color variants, many of which are related to natural taxonomic and
individual from the same region is shown with part of the old
geographic variation. Photograph by David Barker.
epidermis removed just prior to skin shedding. The older, outer
generation of epidermis is covered with a layer of dry mud from the
animal’s habitat, whereas the new skin revealed beneath is an entirely
different color before it becomes covered with adhering mud particles. pattern is inherited differently from melanin that is scat-
Photographs by the author. tered more diffusely throughout the skin.
A number of snake species become melanistic or vari-
ously darkened with age. Examples are the Northern Black
comparatively simple genetic mechanisms. The production Racer (Coluber c. constrictor), which is very black as an adult,
of melanin in snakes is controlled by a single pair of genes, the Eastern Hognose Snake (Heterodon p. platyrhinos), in
which when recessive can result in albinism. Unlike mam- which melanistic individuals are normal color variants, and
mals, however, an albino snake has normal amounts of red insular Florida Cottonmouths (Agkistrodon piscivorus co-
and yellow in the skin so the condition is more appropri- nanti), which darken to nearly uniform black color earlier in
ately referred to as amelanistic partial albinism. Additionally, life than do conspecifics on the mainland (see color of the
there are probably a number of genetic defects that are ca- adult snake in the upper part of fig. 1.32). Some Eastern
pable of producing amelanistic partial albinism. There is Garter Snakes (Thamnophis s. sirtalis) from nearshores of
great variation in the quantity of black that is present in the the Great Lakes are born jet black, and early breeding ex-
skin, and the quantity can also be controlled by multiple periments suggested this to be attributable to a single pair
alleles (alternate forms of a specific gene). There is a clear of recessive genes. Subsequent work, however, has put this
suggestion in some species that melanin related to color supposition into doubt. Richard Zweifel suggested that
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and pattern dimorphism or polymorphism within a spe-
cies. Color anomalies are noted by herpetologists from time
to time in wild-caught snakes, and various abnormal pat-
terns likely reflect genetic mutations or abnormal changes
in genetic expression. A classical example of pattern dimor-
phism is seen in the California King Snake, Lampropeltis
californiae. The usual color pattern consists of alternating
black and white (or brown and yellow) bands, but an alter-
nate pattern consists of a white stripe running lengthwise
along the center of the back (fig. 5.26). The majority of
snakes throughout the range of this species exhibit the
banded pattern, but in the vicinity of San Diego about 40
percent of specimens exhibit the longitudinally striped pat-
tern. Both patterns occur in snakes from the same litter
and represent a natural dimorphism, the striped pattern
having originated as a genetic mutation.
Finally, an interesting example of color polymorphism
involves the Yellow-bellied Sea Snake (Pelamis platurus).
This pelagic species has the largest range of any snake spe-
cies and exhibits extensive variation of color and pattern.
Most individuals have black or brown coloration largely re-
stricted to the dorsal surface, mixed with spots, stripes,
bands, or mottling of yellow, which predominates on the
ventral surface (fig. 1.44). The tail is usually a mottled com-
bination of black and yellow or white. All-yellow individuals
have been reported from certain localities in Costa Rica and
Panama. In particular, there appears to be a localized popu-
lation of all-yellow individuals in the Golfo Dulce of south-
ern Costa Rica (fig. 5.27). Alejandro Solórzano suggests that
this population is relatively isolated within the gulf because
of circulation patterns of surface currents within and out-
side the gulf. Preliminary evidence suggests that such isola-
tion by currents might restrict gene flow between oceanic
and gulf populations and contribute to what appears to be
population differentiation.
Conclusions concerning Color Polymorphisms

The variability of snake coloration includes variation within
Figure 5.26. Three different color phases of the California King
Snake (Lampropeltus californiae). The banded phase (top) is the more
populations and species, and this likely reflects, in large
common form of this snake in the wild. The striped form (center) is part, interactions with the environment and especially
less common but occurs somewhat commonly in the vicinity of San threats of predation. Snakes are very attractive prey to
Diego. The spotted form (bottom) is quite rare but illustrates further birds, and avian predation pressures can be very signifi-
variation of pattern in this species. These photos also illustrate cant. To the extent that intraspecific color variation reflects
variation of the ground color that ranges from brown to black.
polymorphisms, ecological and evolutionary consequences
Photographs by the author.
promote color “ecomorphs” involving coadapted complexes
of genes. Recent comparative analysis of Australian squa-
melanism in this species may depend not only on genetic mates by Anders Forsman and Viktor Åberg demonstrates
constitution but also on environmental influence, for ex- that species with variable color patterns have larger ranges,
ample, cold temperature. utilize a greater diversity of habitats, and are less likely to
There is much normal variation in color pattern in spe- be threatened with extinction. These findings likely reflect
cies and populations of snakes, related to individual varia- theoretical predictions that variable color patterns, or color
tion, ontogenetic changes, regional geographic differences, polymorphisms, enable a species to increase the efficiency
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Bittner, T. D., R. B. King, and J. M. Kerfin. 2002. Effects of body
size and melanism on the thermal biology of garter snakes
(Thamnophis sirtalis). Copeia 2002:477–482.
Boback, S. M., and L. M. Siefferman. 2010. Variation in color and
color change in island and mainland boas (Boa constrictor).
Journal of Herpetology 44:506–515.
Brodie, E. D., III. 1989. Genetic correlations between morphology
and antipredator behavior in natural populations of the garter
snake Thamnophis ordinoides. Nature 342:542–543.
Brodie, E.D., III. 1990. Genetics of the garter’s getaway. Natural
History 99:44–50.
Brodie, E. D., III. 1992. Correlational selection for color pattern
and antipredator behavior in the garter snake Thamnophis
ordinoides. Evolution 46:1284–1298.
Brodie, E. D., III. 1993. Differential avoidance of coral snake banded
patterns by free-ranging avian predators in Costa Rica. Evolu-
tion 47:227–235.
Brodie, E. D., III, and F. J. Janzen. 1995. Experimental studies of coral
snake mimicry: Generalized avoidance of ringed snake patterns
by free-ranging avian predators. Functional Ecology 9:186–190.
Creer, D. A. 2005. Correlations between ontogenetic change in
color pattern and antipredator behavior in the racer, Coluber
constrictor. Ethology 111:287–300.
Endler, J. A., and J. Mappes. 2004. Predator mixes and the conspic-
uousness of aposematic signals. American Naturalist 163:532–547.
Forsman, A., and V. Åberg. 2008. Associations of variable colora-
tion with niche breadth and conservation status among Aus-
tralian reptiles. Ecology 89:1201–1207.
Gibson, A. R., and J. B. Falls. 1979. Thermal biology of the common
Figure 5.27. Yellow-bellied Sea Snakes (pelamis platurus) captured garter snake Thamnophis sirtalis (L.). II. The effects of mela-
from a population of yellow color morphs at Golfo Dulce, Puntarenas, nism. Oecologia 43:99–109.
Costa Rica, and photographed by the author. Most of the snakes in this Hedges, S. B., C. A. Hass, and T. K. Maugel. 1989. Physiological
population are completely yellow, but a more “normal” bicolored snake is color change in snakes. Journal of Herpetology 23:450–455.
shown in the lower photograph for contrast with the yellow specimens Hulse, A. C. 1971. Fluorescence in Leptotyphlops humilis (Serpen-
as well as a snake that has diffuse black mottling on its dorsal surface. tes: Leptotyphlopidae). Southwestern Naturalist 16:123–124.
Jackson, J. F., W. Ingram III, and H. W. Campbell. 1976. The dorsal
pigmentation pattern of snakes as an antipredator strategy:
A multivariate approach. American Naturalist 110:1029–1053.
with which it exploits resources of the environment Lillywhite, H. B. 2006. Water relations of tetrapod integument.
through increased ability to utilize varied environments Journal of Experimental Biology 209:202–226.
and to extend its range. Thus, snakes provide excellent Lillywhite, H. B., and P. F. A. Maderson. 1982. Skin structure and
permeability. In C. Gans and F. H. Pough (eds.), Biology of the
model systems in which studies of coloration can reveal im-
Reptilia, vol. 12, Physiology C, Physiological Ecology. New York:
portant principles related to population and evolutionary Academic Press, pp. 379–442.
processes. On the other hand, snakes are fundamentally Maderson, P. F. A. 1965. Histological changes in the epidermis of
exquisitely colorful animals, and one does not need addi- snakes during the sloughing cycle. Journal of Zoology (London)
tional justification to enjoy the beauty that stimulates our 146:98–113.
Maderson, P. F. A. 1984. The squamate epidermis: New light has been
raw emotions.
shed. Symposium of the Zoological Society of London 52:111–126.
Maderson, P. F. A. 1985. Some developmental problems of the rep-
tilian integument. In C. Gans, F. Billett, and P. F. A. Maderson
Additional Reading (eds.), Biology of the Reptilia, vol. 14, Development A. New York:
Andrén, C., and G. Nilson. 1981. Reproductive success and risk of John Wiley & Sons, pp. 523–598.
predation in normal and melanistic colour morphs of the Maderson, P. F. A., K. W. Chiu, and J. G. Phillips. 1070. Endocrine-
adder, Vipera berus. Biological Journal of the Linnean Society epidermal relationships in squamate reptiles. Memoirs of the
15:235–246. Society for Endocrinology 18:259–284.
Avolio, C., R. Shine, and A. J. Pyle. 2006. The adaptive significance Maderson, P. F. A., T. Rabinowitz, B. Tandler, and L. Alibardi. 1998.
of sexually dimorphic scale rugosity in sea snakes. American Ultrastructural contributions to an understanding of the cellu-
Naturalist 167:728–738. lar mechanisms in lizard skin shedding with comments on the
Bechtel, H. B. 1995. Reptile and Amphibian Variants: Colors, Patterns function and evolution of a unique lepidosaurian phenome-
and Scales. Malabar, FL: Krieger Publishing non. Journal of Morphology 236:1–24.
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Niskanen, M., and J. Mappes. 2005. Significance of the dorsal zig- Yellow-bellied Sea Snake, Pelamis platurus. Integrative and
zag pattern of Vipera latastei gaditana against avian predators. Comparative Biology 52:321–330.
Journal of Animal Ecology 74:1091–1101. Solórzano, A. 2011. Variación de color de la serpiente marina Pela-
Porter, W. P., and K. S. Norris. 1969. Lizard reflectivity change and mis platura (Serpentes: Elapidae) en el Golfo Dulce, Puntare-
its effect on light transmission through body wall. Science nas, Costa Rica. Cuadernos de Investigación UNED 3:89–96.
163:482–484. Tu, M.-C., H. B. Lillywhite, J. G. Menon, and G. K. Menon. 2002.
Pough, F. H. 1976. Multiple cryptic effects of cross-banded and Postnatal ecdysis establishes the permeability barrier in snake
ringed patterns of snakes. Copeia 1976:834–836. skin: New insights into lipid barrier structures. Journal of Ex-
Rahn, H. 1942. Effect of temperature on color change in the rattle- perimental Biology 205:3019–3030.
snake. Copeia 1942:178. Zweifel, R. G. 1998. Apparent non-Mendelian inheritance of mela-
Sheehy, C. M., III, A. Solórzano, J. B. Pfaller, and H. B. Lillywhite. nism in the garter snake Thamnophis sirtalis. Herpetologica
2012. Preliminary insights into the phylogeography of the 54:83–87.
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IN TE R NAL TR ANSP ORT
Circulation and Respiration
As is well-known, snakes have a tendency to secrete themselves in very

confining quarters and they are capable of passing through relatively small
apertures and channels. It was noted earlier that the air sac reduces the
6
changes in diameter necessary for ventilation. Possibly of greater importance in
the present context is the fact that if one region of the body is entirely
immobilized ventilation can be maintained by regions that are free. In attempting
to record breathing movements by means of mechanical levers and cuff
pneumographs it was found that most snakes are very sensitive to pressure on
their ribs. Almost invariably the region in contact with the cuff ceases movement
and ventilation is taken up elsewhere. It is reasonable to suppose that a similar
reaction occurs in nature when a snake passes through a narrow passage.
—Harry S. McDonald, Herpetologica 15 (1959): 195
The Need for Oxygen some aquatic species can supplement pulmonary exchange
Just like any other vertebrate, a snake requires oxygen in (meaning “lung” exchange) with some intake of O2 and
order to remain alive. Oxygen is required for cellular respi- losses of CO2 across the skin. Internally, the oxygen is trans-
ration, which in the strictest sense refers to the intracel- ported throughout the body by means of the blood circula-
lular oxidation of organic substrates by molecular oxygen, tion, which also transports CO2 from the various body
coupled in turn to the generation of usable energy that tissues back to the lung and skin (fig. 6.1).
becomes trapped in the molecular form of ATP. The organic
substrates consist of macromolecules that are derived
from the processes of digestion and absorption of the food Diffusion versus Convection: The Need
that snakes eat. The well-known by-products of respiration for a Pump
are CO2 and H2O. The latter is called metabolic water and The movement of gaseous molecules such as O2 and CO2 is
actually makes a small, but sometimes significant, contri- by diffusion across the internal lung surfaces and from
bution to the water input of an animal (see chapter 2). In blood capillaries to the mitochondria of cells where the
more popular and lay usage, the term “respiration” is often oxidation processes involving oxygen occur. The term diffu-
used (inaccurately) as a name for the process of exchange sion refers to the movement of molecules by random mo-
of O2 and CO2 between the animal and its environment. tion that depends on the temperature and a gradient of
The term external respiration is sometimes used in refer- concentration difference. The net movement occurs from
ence to breathing, which more accurately should be called higher to lower concentration (or, in the case of gases, par-
ventilation. tial pressure). Diffusion is a slow process, however, and in
Oxygen is acquired from the environment, while CO2 a moderate size snake—say, a boa that is 3 or 4 meters
escapes the body and dissipates to the environment. Both long—it would require literally a few years for oxygen to
processes are fundamentally essential to life. Collectively, diffuse through tissues from the lung at the anterior quar-
these are referred to as gas exchange, and any organ that ter of the animal to the tissues in its tail! Thus, animals
evolves specifically for this task is called a gas exchanger. In larger than a few centimeters in size, including all verte-
the case of snakes, the gas exchanger is a lung, although brates, depend on the process of convection to speed the
| 141
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Figure 6.1. Schematic representation of lung ventilation, blood circulation, and transfer of respiratory gases (O2 and
CO2) between the lung and blood and between the blood and tissues. The squiggly lines represent movement of
gases by convection (or bulk flow transport), and the straight lines represent movement of gases by diffusion: oxygen
from lung to blood (left part of schematic), and from blood to tissue and mitochondria (right part of schematic); CO2 in
the opposite directions. The circulation of blood is powered by muscular pumping of the heart (center of schematic).
The snake to which the schematic arbitrarily applies is a Deinagkistrodon acutus, photographed in Taiwan by
Ming-Chung Tu. The schematic representation of gas transport was drawn by Shauna Lillywhite.
movement of gaseous molecules as well as other substances the blood circulation as a “transport system” because this is
around the body (fig. 6.1). precisely how it functions in moving various things from
Convection refers to the bulk movement of something place to place within the body. These include not only respi-
when it is carried in a medium such as air, water, or blood. ratory gases but also blood cells, various ions, nutrients,
Imagine you are outdoors and standing in front of your waste metabolites, hormones, water, and heat.
house. If the outside air was perfectly still and your neigh- The circulatory system of a snake consists of a central
bor across the street opened a perfume bottle outside, you muscular pump, the heart, and distributing vessels that
would not smell it, and the movement of perfume mole- move blood (the transport medium) around the body. The
cules that happen to vaporize would be a slow process if it blood is red because of red blood cells that contain hemo-
depended solely on diffusion from the source. However, if globin, which is a pigment that binds oxygen reversibly and
there is even a gentle breeze, you could smell the perfume if permits the transport of much larger amounts of oxygen
the vaporized molecules were carried by the air movements than would be possible otherwise (i.e., in simple solution).
from the neighbor to you, assuming of course the wind is Thus, when the blood is oxygenated in the lung, the large
blowing in the right direction. Similarly, we could imagine majority of oxygen molecules is attached to hemoglobin
the enhanced movement of a dye when a drop of it enters a and is transported within the red blood cells, which move
body of water such as a pond or lake. The dye would not freely while suspended in the blood plasma. The plasma is
disperse very rapidly without movement of currents in the the liquid part of the blood and contains various dissolved
water (say by stirring) that would carry it from place to substances—red blood cells, nutrients, and the like—and
place. This is essentially the reason that circulatory systems flows through the blood vessels. In the capillaries, which are
evolved in animals. Indeed, some physiology books refer to the smallest blood vessels that service tissues, oxygen
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comes off the hemoglobin and diffuses into the cells that the cardiac (heart) muscle contracts, much of the blood is
are oxidizing substrates in the process of respiration. ejected from the ventricle through outflow vessels that con-
There are two fundamental circuits in the blood circula- vey the blood to the various arteries. Before the blood enters
tion of snakes and other terrestrial vertebrates. The pulmo- the ventricle, it flows from the veins into two atria (individ-
nary circulation consists of all the vessels that convey blood ually termed atrium) that are capable of muscular contrac-
from the heart to the lung, where the blood is oxygenated tion and positioned between the veins and the ventricle. It
in pulmonary capillaries before returning to the heart for is the ventricle, however, that possesses stronger muscle
pumping to all other body tissues. The systemic circulation and imparts the greatest force to the blood in order to pro-
consists of all the vessels that convey oxygenated blood duce movement throughout the system.
from the heart to the body tissues where oxygen is ex- The heart of snakes is fundamentally similar to that of
changed for CO2 in the systemic capillaries. Ideally, if the other squamates and turtles, but it differs substantially
system operated as it does in a mammal, which has a four- from that of crocodilians, birds, and mammals. The sinus
chambered heart, all of the oxygenated blood from the venosus is the first heart chamber to receive venous blood
lungs would be pumped to the systemic tissues, and all the from systemic veins, and it contains a “pacemaker” that ini-
relatively unoxygenated (termed deoxygenated) blood tiates contraction and determines its timing. From here
returning to the heart from the tissues would be pumped to blood enters the right atrium. In comparison with “primi-
the lungs for reoxygenation. In this system the blood flows tive” (basal) early vertebrates, the sinus venosus is reduced
from the systemic circuit through the heart to the lung, and the originally single atrium is divided into two distinct
hence back to the heart for return to the tissues again, and chambers. The muscular ventricle joins the two atria where
so forth. The blood flows in series from the pulmonary ves- each of two atrioventricular valves guards the entrances to
sels to the systemic vessels, then back to the pulmonary the ventricular chambers. From the ventricle blood flows
vessels, and so on, and the blood in the two respective cir- into three large arteries, and the base of these vessels is de-
cuits is kept separated. In vertebrates other than crocodil- rived in evolutionary terms from the primitive conus arteri-
ians, birds, and mammals, however, there is possibility for osus. The three arterial outflow vessels branch to form the
mixing of the two bloodstreams in the ventricle, which is pulmonary trunk and the right and left aortic arches, the
not anatomically divided into two separate chambers. latter vessels sending blood flow to the systemic tissues.
There is a valved interaortic foramen that forms a tiny con-
nection between the bases of the adjacent aortic arches.
The Heart: Central Pump and Controller This opening allows possible shunting or movement of
of Shunts blood from one aortic arch to the other, but the functional
The heart is a muscular pump and serves the important role significance of this connection has not been well studied in
of imparting motion to the blood that circulates throughout snakes. Contractile muscle tissue is dense near the base of
the system of interconnected blood vessels (fig. 6.2). Blood the three outflow tracts and is especially important in con-
is returned to the heart in vessels called veins, which fill the trolling the resistance of the pulmonary trunk to the blood
heart with blood during its state of muscle relaxation. When that is flowing to the lungs.
Figure 6.2. Heart of a Florida Cottonmouth

(Agkistrodon piscivorus conanti). The snake
weighed 656 g, and the heart shown weighed
1.6 g. At the left, the ventricle is shown in
diastole, with the atria contracted while filling
the ventricle with blood. The ventricle contracts
in systole at the right, with the atria filling with
new venous blood. Symbols are CA, cavum
arteriosum; CP, cavum pulmonale; CV, cavum
venosum; LAo, left aortic arch; RAo, right aortic
arch; PA, pulmonary arch. The abbreviations CA,
CP, and CV overlie the locations of the respective
heart chambers, which are internal and cannot
be seen. Note the coronary arteries that are
visible as small vessels branching over the
surface of the ventricle. Photographs by the
author.
Internal Transport | 143
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The right atrium receives deoxygenated blood returning cavity called the cavum pulmonale. The muscular ridge is an
from the systemic body tissues, and the left atrium re- incomplete muscular septum that partially divides the ven-
ceives oxygenated blood that is returning from the lungs. tricle by separating the cavum pulmonale from the cavum
When the atria contract, their respective bloodstreams fill arteriosum and cavum venosum. The latter two chambers
somewhat separated regions of the ventricle and are sub- are partially separated by a structure called the vertical sep-
sequently ejected into the appropriate outflow tracts: de- tum and joined by an interventricular canal that communi-
oxygenated blood to the lungs via the pulmonary trunk cates between the two. During filling of the ventricle, termed
and arteries, and oxygenated blood to the body via the aor- diastole (pronounced dye-ASS-toh-lee), the opened right
tic arches. The movement and separation of bloodstreams atrioventricular valves lie across the opening to the inter-
within the ventricle is complicated and subject to consider- ventricular canal and temporarily close it. Thus, oxygenated
able variation depending on the prevailing physiological blood from the left atrium enters the cavum arteriosum and
demands. remains there during the period when the inter-ventricular
The ventricle is anatomically a single chamber and serves canal is occluded by the valve structures. During contraction
as a single pump to power the movement of blood into the of the ventricle, termed systole (pronounced SIS-toh-lee),
major arterial branches leaving the heart. Internally and the atrioventricular valves close and prevent a reversed flow
functionally, however, the ventricle is subdivided into three of blood back into the atria, also removing the physical
interconnected compartments (fig. 6.3). The cavum arterio- occlusion of the interventricular canal. Hence, blood in the
sum receives oxygenated blood from the left atrium but has cavum arteriosum flows to the cavum venosum via the in-
no direct connection to an outflow tract. Deoxygenated terventricular canal, and from this compartment it is
blood from the right atrium flows into a cavity called the expelled into the aortic arches. The contraction of the ven-
cavum venosum and then across a muscular ridge to a third tricle also compresses the muscular ridge against the oppo-
site wall, which separates the cavum
venosum from the cavum pulmonale. De-
oxygenated blood residing in the cavum
pulmonale exits the ventricle through the
pulmonary trunk (hence pulmonary
arteries) to the lung, but some of this
blood may leak across the muscular ridge
to enter the left aortic arch.
The contraction of ventricular muscle
is not synchronous, and deoxygenated
blood is propelled into the pulmonary
arteries before oxygenated blood exits the
ventricle. When the oxygenated blood is
compressed by contraction of the adja-
cent ventricular walls, it encounters high
resistance in the pulmonary trunk that is
mostly filled with deoxygenated blood.
Therefore, oxygenated blood enters the
systemic arches partly because they offer
less resistance.
A single ventricle such as that of a snake
presents the potential for intracardiac
shunting of blood from systemic to pulmo-
nary streams, or vice versa. The term shunt
basically refers to an alternate pathway.
Thus, some of the blood that returns from
the body tissues and is normally directed
Figure 6.3. Schematic drawing of a generalized heart of a snake. This drawing
to the lungs might instead be “shunted” to
illustrates the three chambers of the ventricle, which receive inflowing blood from the
atria, and the connections to outflow vessels are shown. Label abbreviations are LA, left
the systemic circulation and thereby re-
aortic arch; RA, right aortic arch; PA, pulmonary artery. See text for further explanation. turn to the body, whereas some of the oxy-
Drawing by Dan Dourson and the author. genated blood that returns from the lung
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and is normally directed to the body might instead be High degrees of shunting have also been shown to occur
“shunted” back to the lungs. These circumstances are termed in sea snakes, which dive to considerable depths (maximum
intracardiac shunts and may result in either pulmonary by- recorded about 100 meters) and breathe intermittently at
pass or systemic bypass (or both), involving some fraction of the surface of the ocean. Some species appear capable of
blood that is passing through the single ventricle. remaining submerged for very long periods, however, by
Partial or complete pulmonary bypass is called a right-to- “cutaneous breathing” (uptake of oxygen diffusing across
left shunt (R-L shunt), and partial or complete systemic by- the skin, with release of CO2 in the opposite direction).
pass is called a left-to-right shunt (L-R shunt). The mechanisms Another important issue associated with diving is the
controlling the magnitude and direction of shunting involve prevention of decompression illness (also known as the
nervous control of the relative resistance or pressure differ- “bends” or caisson disease). This occurs when nitrogen that
ences in the pulmonary and systemic outflow tracts. For ex- diffuses into blood from the pulmonary air becomes pres-
ample, an increase in pulmonary vascular resistance will surized at depth and “loads” the circulation. Then it forms
promote the translocation of a fraction of blood from the bubbles when the blood is depressurized and the gas comes
pulmonary to systemic circuit; that is, blood normally leaving out of solution as the snake ascends to breathe air. Small
the ventricle through the pulmonary trunk encounters in- bubbles that form in the blood circulation can block smaller
creased resistance and instead is redirected to the systemic blood vessels and thereby cause tissue damage, but this has
outflow tracts (R-L shunt). Such a mechanism has been not been evaluated well in snakes or other reptiles that
termed pressure shunting. Alternatively, a passive mechanism might have vessel size and properties that are different
for shunting can involve blood that is located within a space from humans or other mammals in which decompression
of the ventricle that is common to both pulmonary and problems have been better studied. Roger Seymour and his
systemic circulations at different phases of the heart cycle colleagues have performed elegant studies that establish
and is subsequently “washed” into the “wrong” circulation by avoidance of decompression problems in sea snakes by vir-
inflowing or outflowing blood that is moving in the correct tue of a combination of shunting blood away from the lung
direction. This condition has been termed washout shunting. (thus avoiding nitrogen loading from the compressed lung
Both pressure and washout shunting probably occur under gas) and losses of blood nitrogen to the ambient water
various conditions in most or all species of snakes, but the across the skin. All of the nitrogen that enters the blood in
subject has not been well studied in reptiles other than tur- the lung is mixed with nitrogen-poor blood that has come
tles, crocodilians, and lizards. Furthermore, mixing in the from the skin. This goes out into the body, but the pressure
ventricle can create both shunts simultaneously. of nitrogen never increases enough to cause the bends. So it
One of the more dramatic examples of pressure shunt- is central shunting plus the ability to lose nitrogen through
ing in snakes occurs in the aquatic file snake, Acrochordus the skin that prevents the bends.
granulatus, investigated by myself and John Donald, who
was a postdoctoral associate in my laboratory at the Univer-
sity of Florida. This snake is a resident of mangrove swamps Blood Vessels and the Vascular
and shallow tropical waters, where it remains submerged Distribution System
for periods up to several hours. During submergence when The heart is connected to a marvelously complex system of
the snake is quiescent, blood flow completely bypasses the vessels that distribute the blood throughout the body and
lung except for periodic moments when flow is directed to return it for repeated pumping in a conventional manner
the lung briefly and at low flow rates. This pattern of inter- that is fundamentally similar to what occurs in mammals.
mittent shunting, attributable to increased resistance in The vessels transporting blood away from the heart are
the pulmonary artery, keeps the partial pressure of circu- termed arteries. As in mammals, they are characterized by
lating oxygen low. This condition favors the uptake of ox- having relatively thick walls with layers of smooth muscle
ygen across the skin (from a higher partial pressure in and elastic tissue. The vessels that return blood from the
water) and inhibits the losses of oxygen to surrounding tissues to the heart are called veins, and these are generally
water under conditions where the ambient water is low in thinner than arteries but also contain muscle and elastic
oxygen. In a crude sense, this has been likened to “meter- tissues. The veins are more “stretchy” than arteries and con-
ing” the oxygen stores in the lung and allowing the transfer tain the major part of the circulating blood and thereby
of lung oxygen to circulating blood at low or minimal rates. serve as a blood “reservoir.” Capillaries are the smallest ves-
Thus, the intracardiac shunt capabilities of ophidian hearts sels of the circulatory system and collectively constitute the
have advantages and would not be possible if the pulmo- sites where respiratory gases, nutrients, ions, and other
nary and systemic flows of blood were completely sepa- substances are exchanged with the interstitial fluid that
rated, as in mammals. surrounds cells of the various tissues. In the pulmonary
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circulation, the lung capillaries are where oxygen and CO2 The arterial outflow tracts from the ventricle include the
are exchanged between the blood and the air spaces within right and left aortic arches, which typically leave the ven-
the lung (fig. 6.4). The smaller arteries leading blood to the tricle ventromedially and arch around the esophagus to run
capillaries are called arterioles, and the smaller veins leading toward the tail. Not far from the heart these two arches
blood away from the capillaries are called venules. merge in the dorsal midline to form the dorsal aorta (fig.
6.5). The carotid arteries leave the right aortic arch near the
cranial ends of the atria and carry blood to the head and
brain. The left carotid artery is usually the dominant vessel
and typically about the same diameter as the right aortic
arch. The right carotid artery is smaller in diameter and
may be absent or vestigial in some taxa of more advanced
snakes (Caenophidia). A vertebral artery arises from the
right aortic arch near where it curves to run in a posterior
direction. The anterior vertebral artery courses toward the
head for variable distances and then disappears in the mus-
culature between the vertebrae. Branches of this vessel per-
fuse the muscles of the body wall, skin, esophagus, lung
fascia, and head. Progressing in the opposite direction to-
ward the tail, a series of vertebral vessels originates from
Figure 6.4. Respiratory, vascularized part of the lung of a Burmese
Python (Python molurus bivittatus). The lung has been severed and laid the dorsal aorta in addition to prominent branches to the
open to reveal its internal anatomy (head end is to the left). The bronchial principal organs of the body cavity. The caudal segment of
airway (B) opens into the lung where the internal air pockets (faveoli) are the aorta terminates within the tail.
seen. Three-dimensionally, the faveoli (F) form a thickness of highly The third arterial outflow tract from the ventricle gives
vascular red tissue comprising the wall of the lung. The density of blood
rise to the pulmonary artery (fig. 6.5). The pulmonary trunk
capillaries in this tissue gives rise to its intense red color. Oxygen and
CO2 are exchanged between the blood capillaries of the faveoli and the
originates from the ventricle immediately adjacent to the
lung air within the faveoli, derived from the pulmonary air that is aortic arches, and all three vessels emerge from the ven-
ventilated in and out of the lung. Photograph by John Roberts. tricle to course for a short distance as a truncus arteriosus,
Figure 6.5. A schematic diagram of a snake showing the major blood vessels in two regions of the body. The arrangement of internal anatomy
is based on that of a rat snake (Elaphe or Pantherophis spp.), which has a relatively anterior position of the heart. The ventricle, liver, and
kidneys are shown in black; the atria are stippled; and the vascular lung is crosshatched. The blood vessel abbreviations are ca, carotid artery;
da, dorsal aorta; icv, inferior caval vein; jv, jugular vein; hpv, hepatic portal vein; laa, left aortic arch; pa, pulmonary artery; pv, pulmonary vein;
raa, right aortic arch; va, vertebral artery; vv, vertebral vein. Redrawn by the author after fig. 1 in J. A. Donald and H. B. Lillywhite, Adrenergic
innervation of the large arteries and veins of the semiarboreal rat snake Elaphe obsoleta, Journal of Morphology 198:25–31, 1988.
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Figure 6.6. Corkscrew structure of the portal
vein in a Florida Cottonmouth (Agkistrodon
piscivorus). The corkscrew turns of this
segment of portal vein can be seen in the
central part of the photograph, adjacent to the
posterior aspect of the liver. The posterior
direction (toward the tail) is to the right in the
illustration, indicated by the arrow in the
inset. The inset is a schematic illustration of
how “damming” of blood movement can occur
hypothetically if there is retrograde (reversed
and wrong direction) flow in the vein, e.g.,
through a gravitational surge of blood. The
damming effect is seen in the lower part of the
inset where blood (dark stippling) collects at
one of the turns of the “corkscrew,” which
collapses on itself because of pressure of the
surging blood. The direction of normal blood
flow, returning to the heart, is from right to left.
Photograph and drawing by the author.
bound together by common elements of fibrous fascia. the artery. The lymphatic fluid (also called lymph) that fills
Eventually the pulmonary artery divides in variable pat- these vessels resembles blood plasma and is derived from ex-
terns in different taxa, but there is usually a single cess filtration of fluid at the capillaries. This fluid eventually
prominent branch, or two branches that course in opposite merges with the venous system, where it is returned to the
directions away from the heart. In most species the ante- heart and recirculated in blood. The lymphatic vessels of
rior branch is the predominant and longest pulmonary snakes are fascinating in their structural complexity but have
vessel, which services a vascular lung that is near the heart not been well studied.
(see below).
Blood from the lung is returned to the heart in one or
more pulmonary veins, and the pulmonary drainage paral- Properties of Blood
lels the pulmonary arterial system. Pulmonary venous
blood returns from the lung to the left atrium. Anterior Blood Volume
drainage from tissues other than the lung returns to the The volume of blood contained in the circulation is an im-
heart in usually two jugular veins, one being dominant (the portant parameter that is, of course, essential for ade-
right) or the two joining to form a superior caval vein that quate pressure and flow in the vascular distribution
conveys blood to the right atrium (fig. 6.5). The inferior system. Circulating blood volumes have been measured in
caval vein originates from two renal veins in addition to a a few species of snakes and generally correspond to about
hepatic portal vein and numerous parietal veins, returning 6 percent of the body mass. File snakes (Acrochordus spp.)
blood to the heart from the posterior body cavity. The por- may have blood volumes about twice this amount, and the
tal vein branches profusely within the liver but also conveys extra volume is thought to improve the storage of oxygen
blood directly to the inferior caval vein. Variable portions of and thereby prolong the diving times in tropical waters
the portal vein may show a “corkscrew” configuration at the where this species lives (see below). Measurements of fluid
level of the liver and immediately posterior to it in terres- movements between blood vessels and the surrounding
trial taxa of snakes (fig. 6.6). This structure conceivably acts interstitial fluids have been evaluated in some snakes and
as a bidirectional valve and prevents gravitational surges of suggest that capillary permeability is relatively great.
large volumes of blood that is associated with the liver and Therefore, plasma can move relatively freely across capil-
vessel lumen. The inferior caval vein and the hepatic portal lary walls, and the blood volume is potentially labile. For
vein run parallel in close proximity posterior to the liver. example, interstitial fluid moves into the blood compart-
Snakes have an extensive system of lymphatic vessels, ment when there are losses of blood due to hemorrhage,
which often parallel the blood vessels as perivascular lym- whereas activity such as locomotion may filter blood in the
phatics. Major arteries, for example, might be surrounded by opposite direction and transiently reduce the blood vol-
a sleeve of fluid that flows in the lymphatic vessel surrounding ume (as much as 17 to 22 percent in some rattlesnakes).
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Although the circulating blood volume may be subject to Hemodynamics: The Physics of Flow in the
transient disturbance, this important parameter is, in Vascular Fluid System
fact, well regulated over time. The lymphatic system may The transport function of the blood circulation requires
also provide an important reservoir of fluid that might that fluid moves at appropriate rates throughout the body,
contribute to the regulation of blood volume, as is the case and this depends on the pumping action of the heart and
in amphibians. the nature of the vessels that distribute blood from the
arteries to capillaries. There must also be sufficient flow in
Blood Oxygen Capacity the venous system so that blood returns to the heart for
The amount of oxygen that is present in the blood is re- further pumping. The distributing vessel system, especially
lated to the absolute volume of blood, and to the amount the smaller arterioles and capillaries, presents a certain re-
of circulating red blood cells with their characteristic con- sistance to the flow of the blood, and the quantitative ex-
tent of hemoglobin. Considering somewhat sparse data pression of this resistance is called peripheral resistance. The
that are available for snakes, the amounts of red blood resistance depends on the geometry of the vascular system,
cells and oxygen that are present in the blood are gener- especially the diameter of the distributing vessels. Smaller
ally similar to that in other reptiles. Hematocrit values, diameter vessels present a greater resistance to flow than
which represent the volume of red cells per unit of blood do larger diameter vessels. Thus, most of the resistance to
volume, generally range between 20 and 30 percent with blood flow occurs in the microvasculature, which includes
marine species representing the higher values. Exception- the smaller arterioles and capillaries.
ally high values (around 50 percent) have been reported in The viscosity of the blood is another parameter influ-
marine file snakes. Maximum oxygen capacity is around encing the resistance to blood flow. In essence, this refers to
10 vol% (which indicates the volume of oxygen per unit the interaction of the vascular geometry with the viscosity
volume of whole blood, expressed as a percentage). Again, of the flowing fluid that determines how well the blood
file snakes (Acrochordus) exhibit higher values that are moves. Frictional interactions between concentric layers of
thought to be important for the storage of oxygen in rela- blood moving past each other vary with the velocity of
tion to diving. movement and the size and length of the vessels. The na-
The molecular properties of hemoglobin are also im- ture of the blood also is important. The viscosity of blood is
portant and determine its affinity for oxygen at a given greatly increased over that of water by the presence of red
pressure of oxygen to which the blood is exposed. Typi- blood cells, which also have frictional interactions with the
cally, hemoglobin binds oxygen in adequate amounts to surrounding blood plasma and especially suspended pro-
saturate its binding sites at normal atmospheric pres- teins that have “sticky” qualities when contacting the outer
sures of oxygen in the air that is breathed into the lungs walls or membranes of the red blood cells. The greater the
by snakes and other air-breathing vertebrates. Diving number of red blood cells the greater the viscosity of the
aquatic snakes may have hemoglobin with slightly greater blood relative to water.
oxygen affinity because of the requirement for extracting The muscular contraction of the heart’s ventricle cre-
oxygen from lung air that becomes relatively depleted ates pressure in the blood that is contained within it. This
of oxygen (which reduces the oxygen pressure propor- pressure adds energy to the blood, which imparts motion
tionately) during the time underwater when the snake is and powers its circulation. Because of the heart’s pumping
not breathing atmospheric air and the lung becomes es- action, the energy content of blood is highest in the arte-
sentially a “closed system.” Differences in oxygen affinity rial outflow tracts and is dissipated during flow in over-
of hemoglobin might also be related to differences in coming the peripheral resistance. Thus, there is a gradient
levels of behavioral activities, or other factors that are of energy from the heart to the capillaries, and on to the
not yet well studied. veins, which induces flow. Blood pressures in the veins are
The blood properties of snakes can vary substantially very low, nearly zero, and the heart reenergizes the blood
with temperature, ontogeny, nutrition, and activity. The to produce continued flow into the arteries. This system is
amount of data is limited for snakes, and the significance of somewhat analogous to the continuous movement of
all the variation that has been observed has not been fully water through a fountain, as example one that sprays
evaluated. We may conclude however—with some measure water in an upward stream that falls into a quiet pool be-
of caution—that the transport of respiratory gases is max- low. The spout of water flow at the fountain is powered by
imal or “optimal” in supporting activities at preferred body a pump that pressurizes the water. The water in the pool is
temperatures in characteristic environments in which a relatively still and flows at low energy level back to the
given species has evolved. This appears to be generally true pump where it is again pressurized and sprayed into the air
in a variety of ectothermic vertebrates. against gravity.
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The parameter of foremost physiological importance in state of constriction of the smooth muscle. Circulating cate-
the snake’s circulatory system is the actual flow of blood, cholamines have similar effects, and mostly these cause con-
which is of course necessary for the transport of materials striction of the smooth muscle (called vasoconstriction), but
around the body. The related parameter that energizes the they may also cause dilation or relaxation of the smooth
flow is the blood pressure, and this is what a physician usu- muscle (called vasodilation) in certain parts of the vasculature.
ally measures as an indicator of the overall health and Acetylcholine is another chemical that is released from nerve
well-being of a person’s blood circulation. The pumping endings at the heart and causes slowing of the heart rate.
action of the heart produces repetitive “pulses” of arterial Generally, the heart rate is determined by a balance or a
pressure that vary from a systolic high (related to ventric- “push-pull” action between acetylcholine and catecholamines.
ular contraction) to a diastolic low (when the ventricular How do the nerve endings and adrenal medulla know
muscle is relaxed and the heart chambers are refilling when and how much of these regulatory substances to
with blood). Thus, in a human, the arterial systolic pres- secrete? Regulation is accomplished by a feedback system
sure is around 120 mm Hg and the diastolic pressure is of information involving sensitive structures called baro-
around 80 mm Hg, giving a geometric mean of about receptors that monitor the moment-to-moment changes
100 mm Hg. The mean value and the difference between in arterial blood pressure. The baroreceptors are actually
systolic and diastolic pressures are related to the heart a discrete collection of nerve endings located in the walls
rate (frequency of heart contractions) and the level of pe- of central arterial outflow vessels, especially the base of
ripheral resistance in the blood vessels. Mean levels of the pulmonary artery and possibly the carotid artery.
systemic arterial blood pressure in snakes typically vary These are sensitive to stretch, which indirectly monitors
from lows of 20–30 mm Hg to highs of 50–80 mm Hg in the blood pressure. Increasing pressure tends to stretch
various species. Pulmonary arterial pressures run lower at the vessel wall slightly, and a decrease in pressure has the
about 15–30 mm Hg (see below). Venous blood pressures opposite effect. Information from these nerve endings is
in both systemic and pulmonary circuits are very low, ap- sent via nerve signals (“impulses” or “action potentials”)
proaching zero, except when the vessels are compressed to the central nervous system and interacts with other
by the body during activities such as locomotion, climb- nerves in the brain to direct an outflow of nerve signals
ing, constricting prey, and so on. External compression of to modify the release of chemicals from nerve endings at
the veins produces transient increases of pressure inde- the heart, peripheral blood vessels, and the adrenal
pendent of the action of the heart and the levels of blood medulla. So, as an example, a decrease in blood pressure
pressure in the arteries. reduces the stretch of baroreceptors, which then send
Although there are mechanisms that ensure that re- signals to the brain, where integration results in in-
gional or local blood flow rates are adequate for the needs of creased signaling from the nerves that release catechol-
the tissue, the overall ability of the central circulation to amines at the heart, blood vessels, and adrenal medulla.
provision these collective flows is related to the regulation Simultaneously, the integration also decreases the re-
of the central arterial blood pressure. The principal deter- lease of acetylcholine from other nerve endings that are
minants of the arterial blood pressure are the ventricular acting on the heart. The result is an increase in the rate
outflow of blood (called cardiac output) and the level of pe- and strength of the heartbeat, which increases the car-
ripheral resistance. Both of these parameters are regulated diac output, and a simultaneous increase in peripheral
principally by the nervous system, with lesser but impor- resistance due to vasoconstriction of peripheral vessels.
tant controls exerted by circulating hormones and the in- These actions collectively tend to restore (increase) the
fluence of tissue metabolites and chemicals that act locally arterial pressure. Alternatively, any transient increase of
on the smooth muscle of the blood vessels. arterial pressure (above normal) produces the opposite
The cardiac output is determined by the rate and st- effects.
rength of the heart contractions, which are driven pri- There are undoubtedly multiple baroreceptors associ-
marily by the influence of chemicals called catecholamines. ated with the central blood vessels near the heart. In mam-
These are released from nerve endings (as “neurotransmit- mals, stretch-sensitive receptors are located in the aortic
ters”) at the heart muscle and may also be circulating as arch, the carotid artery, heart muscle, and major veins.
hormones derived from the medullary (deeper, internal) Many of the blood vessels, including veins, can be to some
portion of the adrenal glands. The familiar catecholamines degree stretch-sensitive in relation to the monitoring of
are known as epinephrine and norepinephrine, which are blood pressure. The situation is probably similar in snakes,
chemically very similar both in structure and actions. These but these various receptors involved in the regulation of
same catecholamines also act at nerve endings in the walls blood pressure have not been well studied in this group of
of the blood vessels, especially arterioles, to influence the vertebrates.
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Gravity and Blood Circulation: Putting bottom of any fluid column is dependent on the absolute
It All Together height of the column. If a fluid column such as a blood
vessel is turned from horizontal to vertical, the pressure
Gravity’s Challenge decreases at the top of the column and increases at the
Gravity has an important influence on blood circulation bottom. There is a point or level near the center of the
that is potentially expressed in animals that are espe- fluid column where the pressure necessarily does not
cially long or tall with upright posture. According to the change, and this is called the hydrostatic indifferent point.
third “law of Pascal,” fluid pressure increases with depth Importantly, these changes in pressure within a fluid
in any fluid column (fig. 6.7). Such pressure is indepen- column attributable to gravity occur whether the fluid is
dent of any other force, such as heart pumping that pres- stagnant or is circulating, as in the blood vessels of a
surizes the fluid, and is called gravitational pressure or, living animal.
more commonly, hydrostatic pressure. It also follows that Snakes are excellent model animals for studies of gravi-
the pressure increase at the bottom of a fluid column de- tational effects on blood circulation owing to their elongate
pends on the height of the column, and therefore the body form and diversity of behaviors and habitats. At one
gradient of pressure (attributable to gravity) from top to extreme, arboreal or scansorial (climbing) species of snakes
bottom of a column depends on its height. The pressure at times adopt fully upright postures when the blood ves-
also increases from top to bottom of a fluid column that sels become long fluid columns with gradients of gravita-
is tilted at an angle and not necessarily fully vertical. The tional pressures related to the absolute height of the blood
increased pressure at the bottom of the column depends column. The ambient pressure is atmospheric, or by con-
on both the length of the fluid column and its angle of ventional reference zero, so the fluid pressures in vessels
tilt. More specifically, the increased pressure at the push outward on the vessel walls and tend to distend them.
At another extreme, fully aquatic snakes
exist in a fluid medium in which vertical
gradients of gravitational pressure in
water counteract the nearly identical gra-
dients in a snake’s blood circulation
owing to the near match of fluid density
between blood and water. Thus, gravita-
tional fluid pressures in the blood vessels
are almost exactly counterbalanced by
the external water pressures (which act
across the body tissues) and there is no
tendency for the gravitational blood
pressures to distend vessels (fig. 6.7).
Consequently, selection pressures for
cardiovascular adaptations to counteract
gravity are effectively not present in the
aquatic medium in which fully aquatic
Figure 6.7. Schematic drawing to illustrate the effects of pressure on a liquid such as forms have spent much of their evolu-
blood that is held within a vessel, for example, a vein. The magnitude of pressure is tionary history (fig. 6.8).
indicated by the width of the arrows. Pressure increases with depth in any column of Gravity challenges the circulation pri-
liquid. If the vessel containing liquid is in water, the external pressure is nearly equal to
marily in two ways. First, when the body
that of the blood within the vessel at any point of depth in the liquid column, so the
pressures (P) acting on opposite sides of the wall of the vessel are essentially equal and is upright, the heart must pump against
cancel each other (left-hand figure). If the vessel is in air, however, the ambient pressure the pressure at the base of the arterial
outside the vessel is everywhere atmospheric (zero by convention), whereas the pressure column between the heart and head. In
in the blood inside the vessel increases with depth according to the Law of Pascal. animals like giraffes, long snakes, and
(Pressure also increases with depth in a column of air, but the effect is negligible at this
perhaps certain longer-necked prehis-
scale because of the lesser density of air compared with water.) Therefore, in the case of
a vessel in air (right-hand figure), the net pressure acting across the wall of the vessel
toric dinosaurs this pressure can be con-
(inside to outside) increases with depth in the vessel. This net increase in transmural siderable. More specifically, the ventricle
(across the wall) pressure causes the vessel to distend in its lower part and creates a must produce a pressure that exceeds the
condition called “blood pooling.” See text for further explanation. Drawing by the author. pressure at the point of outflow into the
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Figure 6.8. Views of two aquatic snakes
illustrating the effects of gravity on internal body
fluids. In the photo on the left, Arne Rasmussen
holds a sea krait (Laticauda colubrina) vertically in
seawater, and there is no evidence for blood
pooling in this individual. In the photo at the
right, Warren Watkins holds an aquatic file snake
(Acrochordus granulatus) vertically outside of
water. One can easily see the distension of the
lower body, which is due to body fluids—
especially blood—“pooling” in response to gravity.
A part of the distension is probably attributable
also to sagging of viscera. Compare these
photographs with the illustration in fig. 6.7. The
photo at the left was taken by Erik Frausing in
Sulawesi. The photo at the right was taken by the
author on the Embley River, Cape York Peninsula,
Australia.
arterial column above the heart in order to promote flow. aquatic snakes are immune to the gravitational disturbance
Such pressure should exceed the gravitational pressure by a of blood circulation because of the stabilizing effects of ex-
considerable factor if there is to be sufficient pressure at the ternal hydrostatic pressures that match the intravascular
head to perfuse the cranial blood vessels. Moreover, these gradients of gravitational pressure during postural changes
pressures should be positive because if the blood pressure (see above). Second, relatively short species of snakes
falls to zero or becomes negative anywhere along the arte- (< about one meter) experience little problem during ver-
rial branches, the vessel will collapse because of greater ex- tical postures because of the limited length of blood col-
ternal pressure acting on the vessel wall. Again, there would umns and, therefore, limited gradients of gravitational
be no flow of blood in this circumstance. Therefore, blood pressure. However, for many terrestrial species of snake
flow into the head and brain becomes a challenge for long that utilize vertical dimensions of habitat, gravity poten-
snakes that climb with the head up. tially challenges the capacities of snakes to regulate arterial
The second challenge to blood circulation from gravity is blood pressure and to maintain adequate blood flow to the
the tendency for pressures to increase in blood vessels be- head and other critical organs.
low the heart, especially at the feet and lower legs of terres- Many terrestrial species of snakes, and especially those
trial tetrapods and near the tail or caudal end of an elongate that climb, have evolved marvelous defenses that guard
snake. These pressures can cause excess filtration of blood against gravity’s effect on blood circulation. Semiarboreal
plasma at capillaries, thereby producing edema and swelling colubrid (especially rat snakes, genus Elaphe or Panthero-
in tissues, and may also cause blood to “pool” in vessels that phis) and elapid snakes have demonstrated abilities to regu-
are especially distensible or compliant, particularly veins late arterial blood pressure and to maintain adequate blood
(fig. 6.7). The tendency for blood to pool in these lower ves- flow to the head during head-up postures. In some individ-
sels reduces the rate at which venous blood returns to the uals, the precision of such regulation is excellent, and ca-
heart, which in turn diminishes ventricular filling and car- rotid blood flow remains at usual levels even when the body
diac output. Under this scenario, severe or even moderate is fully vertical. Note that the carotid artery is the principal
blood pooling can reduce the cardiac output sufficiently to route of blood flow to the head of snakes. The cardiovascu-
lower the arterial pressure. lar “performance” of various scansorial species is consistent
with a suite of physiological and morphological characteris-
Snakes, Posture, and Gravity tics that evidently coevolved to counteract gravitational
Gravity clearly poses a challenge to three-dimensional uses forces acting on the circulation, and these are quite similar
of terrestrial habitats by long snakes. The problem is dimin- to comparable adaptations that have been studied in hu-
ished or goes away in two circumstances. First, completely mans and other mammals.
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The arsenal of adaptive traits that counteract gravity’s might not be possible in some other tetrapods in which
effect on blood circulation include morphological, physi- the heart is constrained to a thoracic cavity that is
ological, and behavioral attributes (fig. 6.9). Morpholog- surrounded by rigid vertebrae and ribs.
ical traits include anterior location of the heart, which In contrast with scansorial terrestrial species of snakes,
can be as close as 11–12 percent of body length to the fully aquatic species such as file snakes and sea snakes
head, and relatively “tight” tissues that surround blood exhibit generally looser tissues surrounding blood vessels
vessels and counteract the tendencies to blood pooling, and a more central position of the heart (generally 30–45
especially in lower body veins. The tight nature of the tis- percent of total body length from the head). Other things
sues includes properties of the skin and body wall as well equal, a central heart location is energetically more efficient
as the tissue spaces immediately surrounding certain with respect to pumping of blood throughout the entire
vessels (for example, in the tail). The position of the elongated animal. Thus, natural selection probably favors a
heart close to the head shortens the gravitational column central location in circumstances where gravity’s influence
(pressure) against which the heart must work during is reduced. The variation in heart position among species of
head-up posture and tends to ensure adequate perfusion snakes is quite likely related to the extent of time that an-
of head and brain tissues at all angles of body attitude. cestral species have been subjected to selection forces asso-
Such heart position, of course, increases the problem ciated with particular habitats. Of course, other factors
when the snake is in a head-down position. However, such as the size of prey and feeding habits might also influ-
perfusion of the tail and lower body is less important ence heart position in snakes.
than is the adequate and uninterrupted perfusion of the Roger Seymour and I demonstrated that the mean (resting)
brain. It is interesting to think about the evolutionary arterial blood pressure ranges from higher (50 to 70 mm Hg)
migration of the heart in different taxa of snakes, which to lower (20 to 30 mm Hg) in species of snakes ranging from
Figure 6.9. Schematic features of snakes that counteract gravity disturbance to blood circulation. Upper drawing features a sea snake that is
characterized by an elongate vascular lung and a relatively short saccular lung segment. The middle drawing features a ground-dwelling
rattlesnake that has a comparatively central heart position (with respect to length) and an elongate tracheal lung. The saccular segment of lung is
relatively short, but less so than in the sea snake. The lower drawing features a semiarboreal rat snake that has a relatively anterior heart and a
very short vascular lung that is located near the heart. The saccular lung comprises a relatively elongate segment of the lung structure. The rat
snake is relatively more slender than the other snakes and has comparatively “tight” tissues surrounding blood vessels, in addition to superior
nervous control of vessel constriction compared with the other snakes (these features not shown). Drawing by Dan Dourson, after fig. 6 in
H. B. Lillywhite, Circulatory adaptations of snakes to gravity, American Zoologist 27:81–95, 1987.
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scansorial to aquatic in behaviors. Also, regulation of arterial when the jaws are normally closed. (A glottis with the mouth
pressure is much tighter in the arboreal/scansorial species. Fi- open can be seen in fig. 8.5.) The trachea communicates with
nally, mean arterial pressures in terrestrial snakes increases in the bronchial airway and remainder of the lung as a tubular
exact proportion to the distance between the heart and head. air-conducting system (see bronchial airway in fig. 6.4).
The lung proper is shaped somewhat like a spindle and
has a voluminous central space (lumen) that is free of tissue
Structure and Function of the Ophidian Lung (fig. 6.11). The inner surfaces are lined by a very thin layer of
Like other vertebrates, snakes possess a lung that is used for tissue, or parenchyma, that is typically less than 3 or 4 mm
exchange of respiratory gases between the animal’s blood in thickness. Fundamentally, the lung can be divided into
circulation and the outside aerial atmosphere. Air is breathed two functionally different regions: the “respiratory” seg-
in and out of the system by means of nostrils, or nasal open- ment consists of highly vascularized exchange tissue, here-
ings, which are paired and referred to as external nares (sin- after referred to as vascular lung, and in most cases there is
gular is naris). Some species such as sea snakes possess nasal also a simple extension of flat, thin epithelium known as
valves in the nostril consisting of erectile tissue (fig. 6.10). the saccular lung. The vascular lung, including sometimes
The nasal passages communicate with the roof of the phar- tracheal segments, is the region of the lung that functions
ynx, from whence air passes into the trachea via the glottis in respiratory gas exchange (O2 and CO2), whereas the
Figure 6.10. Views looking down on the snout of sea snakes, illustrating narial valves just inside the nostrils. The
upper left photograph shows the narial valves in a Little File Snake (Acrochordus granulatus) photographed by the
author in Queensland, Australia. Note the fleshy valves come together in a vertical plane. The upper right photograph
shows the closed fleshy valves in a Shaw’s Sea Snake (Lapemis curtus) photographed by the author in Queensland,
Australia. The lower photographs illustrate a Yellow-bellied Sea Snake (Pelamis platurus) breathing naturally outside
water. The photos capture the narial valves open (left) during inhalation of air and closed (right) during pauses between
breaths. This specimen was photographed in Costa Rica by Coleman M. Sheehy III.
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Figure 6.11. Histological cross-section through the lung of a king snake (Lampropeltis getula). The bronchial
conducting airway is continuous with the central lumen, which opens into numerous faveoli. The bronchial airway
has walls that are stiffer than the other lung structure, and comprised of cartilage (dense blue tissue, c). Adjacent
faveoli are separated by a connective tissue septum, and the luminal end of each septum contains a bundle of
smooth muscle. The histological stain is H & E. Microphotograph by Elliott Jacobson.
Figure 6.12. Ventral view of the anterior

coelomic cavity featuring segments of the right
(dominant) lung in a Diamond Python (Morelia
spilota spilota). The respiratory segment of the
lung, termed the vascular lung, is adjacent to the
esophagus and near the liver. The vascular lung
is red because of the numerous blood capillaries
involved in gas exchange. Note that the vascular
lung gradually transitions to the saccular lung, in
which three-dimensional faveoli are lacking and
there are no blood vessels involved in gas
exchange. Individual and increasingly shallow
faveoli are seen in the region of transition in the
center of the photograph. The head and the heart
of this snake are to the left in the illustration.
Photograph by Elliott Jacobson.
saccular lung receives only a nutritive blood supply and greatly reduced or vestigial in most species of snakes, and
does not function in gas exchange (figs. 6.9, 6.12). the right lung becomes elongated as the prominent single
Of the internal viscera of snakes, the lung is perhaps the functional lung that is evident to the observer. In various
most variable in size and complexity. Unlike other verte- species, including both primitive and advanced taxa, the
brates having symmetrically paired lungs, the left lung is left lung has been lost entirely. When present, the length of
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Figure 6.13. Ventral view of the tracheal lung of a Florida Figure 6.14. Streams of air bubbles can be seen rising from the
Cottonmouth (Agkistrodon piscivorus conanti). A cut in the lung nostrils of a Chinese Sea Krait (Laticauda semifasciata). This snake is
reveals the inner aspect featuring partly collapsed faveoli (F) and the adjusting its buoyancy by exhaling air after it submerged in a tank of
cartilaginous trachea (T) above. The lumen of the trachea and the seawater. Photographed by the author in Taiwan.
lung are continuous, and the vascular lung shown here expands
outward during normal breathing by the snake. Photographed in
Florida by the author. The lung volume can be very large and represents from 30–
53 percent of the body volume in some European vipers.
When snakes are engaged in defensive displays with the
the left lung varies from 1 to 31 percent of snout-vent lung fully inflated, these percentages are no doubt even
length, whereas the length of the right lung varies from 8 to larger but have not been measured. Obviously, the lung vol-
82 percent of snout-vent length. Only in some primitive ume at any time varies considerably with the ventilatory
snakes (e.g., xenopeltids and boids) do the lungs function status of the snake, and aquatic species adjust the volume
as paired structures. A nice summary of quantitative mea- to regulate buoyancy at various depths (fig. 6.14).
surements of ophidian lungs has been published by Van Respiratory gases are exchanged between the pulmo-
Wallach in the Biology of the Reptilia series. nary blood and ventilated air across the thin, vascular-
With the exception of certain aquatic snakes (see below), ized parenchyma of the vascular lung. The parenchyma is
the vascular lung in the majority of species is best devel- variously sculptured in different species to increase the
oped near the heart, often beginning at or just anterior to area of exchange surfaces. The structural elaboration of
the heart or ventricle, and extending for variable distances parenchymal surfaces varies from a single layer of low re-
in a posterior direction. Additionally, members of about lief trabeculae, or pockets, that lie in a polygonal pattern
half of living snake families possesses a tracheal lung, which on the lung wall to a multilayered honeycomb-appearing
functions as the principal gas exchange organ in the region structure consisting of raised walls or septa that form cu-
anterior to the lung. This is especially prominent in viperid bicles or compartments that may be deeper than wide
species of snakes (figs. 6.9, 6.13). (figs. 6.4, 6.11, 6.13). These structures are somewhat sim-
The lungs of snakes are generally cigar-shaped (fusiform) ilar to the alveoli present in mammalian lungs, except the
and have an elongated central lumen that is arranged as a parenchymal units in snakes are not homologous struc-
single longitudinal unit. One exception to this structure is tures and are termed faveoli (singular faveolus) because
the lung of the aquatic file snakes, Acrochordus spp., which they resemble a honeycomb. The faveolar parenchyma of
consists of either two or four longitudinal lungs that are snakes is highly variable and may exhibit up to four levels
fused into a single organ having two or four corresponding of subdividing walls or septa (figs. 6.4, 6.11). The septa
air chambers in transverse sections. In all snakes the entire separating individual faveoli contain capillaries on both
lung is attached to the body wall or associated membranes sides and are supported by connective tissue with col-
and is surrounded by other viscera. The internal surfaces lagen and elastin fibers. The diameters of individual fa-
are lined with a thin layer or vascularized tissue (vascular veoli typically vary from a fraction of a millimeter to
segment) and thin, membranous tissue (saccular segment). several mm (e.g., 7 mm in the viperids Atheris and Cau-
The total length of the lung can be somewhat short (e.g., 16 sus). The faveolar parenchyma of the vascular lung is var-
percent of total body length in Uropeltis), or extremely long iable within individuals as well as among species. It is
(94 percent of total body length in Acrochordus granulatus). most deeply partitioned near the heart and more sparsely
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partitioned with increasingly shallow depressions or (fig. 6.1). The exchanges occur within capillaries, which have
pockets posteriorly where the vascular lung transitions thin and very permeable walls that are designed for such
to saccular lung (fig. 6.12). exchange.
The amount of respiratory gases that might dissolve
Lung Ventilation: How Do Snakes Breathe? freely in the blood plasma would not be sufficient to meet
The lungs of reptiles, including snakes, are filled by a mech- the transport needs of an active vertebrate animal such
anism that involves aspiration of air into the lungs. The as a snake. Therefore, the role of hemoglobin—carried
lungs are expanded by muscular effort, and this creates a within red blood cells—is very important. Once oxygen
negative pressure with respect to atmospheric pressure diffuses into the blood plasma across the capillary wall, it
around the animal. Thus, air moves in response to a pres- diffuses very rapidly to hemoglobin, where it attaches to
sure gradient from outside to inside during the inflow phase specific sites. Each “molecule” of hemoglobin has four
of the breathing cycle, called inspiration. The opposite out- subunits, each with a heme group containing iron. Once
flow of air, or expiration, is attributable to passive elastic oxygen attaches to one of the heme sites, the probability
recoil of the stretched lung and surrounding tissues, in ad- increases that the other sites will bind other oxygen mol-
dition to ventilatory muscles that help to squeeze the lung ecules. When all the sites are bound on all the hemoglo-
and thereby assist the expulsion of air. Gravity may also as- bin molecules, the blood is said to be “saturated” with
sist the passive component of expiration by creating a oxygen and exhibits its maximum transport capacity. The
downward force on the expanded ribs and elevated body. maximum transport of oxygen by hemoglobin is, very
Paired ribs surround the internal organs, including the roughly, about 20 to 40 times greater than the amount
lung, and run the length of the body cavity in snakes. Inter- that might be carried in simple physical solution (plasma)
costal muscles between adjacent ribs act to move the ribs without hemoglobin.
forward and outward, thereby expanding the lung and body There are two important features of the physical envi-
wall during inflation, while other sets of muscles pull the ronment of hemoglobin that determine how much oxygen
ribs inward to compress the lung space during expiration. it carries and can provide for respiration. First, the ten-
Breathing is intermittent, and the air that is inspired dency for oxygen molecules to bind with hemoglobin de-
into the lung typically is held there for variable periods pends on the partial pressure of oxygen in the blood.
(called apnea) before the air is expired. Only a fraction of Typically, oxygen binds to hemoglobin at pressures that
the lung air is inspired or expired in a given breath, and sev- occur within the ventilated lung, and the pulmonary blood
eral cycles of breathing are usually required to “turn over” saturates with oxygen during its passage through the vas-
the lung air completely. The glottis is open during inspira- cular lung parenchyma. Second, the physical diffusion of
tion, allowing air to flow into the lung when its internal oxygen either from the lung air into pulmonary capillaries,
space expands. Following the active inspiration of air, the or from systemic capillaries into respiring tissues, depends
inspiratory muscles relax and the glottis is closed. Elastic on the gradient of oxygen pressure. That is, there must be a
recoil of the lung causes the lung space to compress slightly, difference of oxygen partial pressure in order for oxygen to
but the lungs are maintained in a partly inflated state diffuse, and it will move from a region of higher to lower
during the period of apnea. After some while consisting of pressure. This is why lung ventilation is important, because
fractions of a minute or longer, the glottis is opened and air it maintains the oxygen pressure closer to the ambient at-
is expired from the lung, which empties partially and then mospheric value and thereby maximizes the pressure that
expands immediately for the next cycle of inflation. Terres- drives diffusion into the lung capillaries. Because some of
trial snakes usually take a single breath at a time, spaced the oxygen is removed from the blood during its passage
apart by variable apneic periods depending on the need. through systemic capillaries, the relatively oxygen-deficient
Aquatic snakes, however, typically have long apneic periods, blood that is returned to the heart from tissues and sent to
or breath-hold, while they are submerged. When these the lung for reoxygenation is at an oxygen pressure lower
snakes surface to breathe, several or more breaths are than that of the pulmonary air within the lung lumen.
exchanged before the animal dives once again. Therefore, oxygen diffuses from the lung air into the
capillaries within the lung. At the other end—systemic
Respiratory Properties and Functions of Blood tissues—the removal of oxygen by respiring mitochondria
The blood of snakes serves to transport oxygen from lungs within cells lowers the oxygen pressure well below that of
to body tissues, and carbon dioxide from body tissues to the systemic blood, so now the oxygen diffuses from the
lung. These gases diffuse freely across the thin barrier be- pressure in the blood (equilibrated to atmospheric air
tween the blood and lumen of the lung, and across the thin within the lung) to the much lower pressure in tissues that
barrier between blood and cells of the various body tissues act as the “sink” for the oxygen.
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low pressures that might prevail in water. The high affinity
of the hemoglobin ensures that oxygen will be attracted
from the aqueous environment that is near to the skin cap-
illaries as well from lung air, and that diffusion losses to
water that might be deficient in oxygen are minimized. In
addition to this feature of acrochordid hemoglobin, the
skin capillaries are associated with arterial vessels that can
shunt blood toward or away from the skin.
In the case of Little File Snakes (Acrochordus granulatus)
that live in the Philippines, I have measured nearly zero ox-
Figure 6.15. Schematic representation of oxygen transfer by ygen in water within mud burrows where these snakes
diffusion from lung air into blood of a pulmonary capillary. The density occur at the bottom of mangrove habitats. Presumably in
of bubbles in the illustration represents the concentration and these situations blood is shunted away from the skin to
pressure of oxygen molecules, which are greatest where the air is avoid cutaneous losses of oxygen due to diffusion from
ventilated in and out of the faveolar exchange unit (upper and left part
blood to water. On the other hand, high levels of oxygen
of figure) and becomes relatively depleted where oxygen diffuses into
the blood capillary. The blood capillary carries relatively oxygen- pressure occur in the open waters of these mangroves espe-
deficient blood returning from the body tissues (entry at left), and this cially at certain times of the day. During these times blood
blood becomes relatively more oxygenated as it passes through the flow is presumably shunted to the skin in order to capture
lung faveolar exchange unit (center to right). Drawing by the author. oxygen from the ambient water as well as diffuse away CO2.
These comments are speculations, and the phenomena as-
sociated with blood flow patterns to skin require much
Thus, there are two competing processes that occur in the further investigation. Sea snakes, incidentally, exchange
lung with respect to oxygen: diffusion into blood tends to higher proportions of respiratory gases across the skin, and
lower the oxygen pressure, and renewal of oxygen by ventila- they are probably subjected to higher environmental pres-
tion tends to elevate the oxygen pressure. The actual oxygen sure of oxygen than are file snakes living in mangroves.
pressure in the lumen of the lung at any given time depends on Here we need to mention that the gaseous by-product of
the balance between these two opposing processes (fig. 6.15). respiration, CO2, is transported in the blood with a reversal
It is important to realize that the oxygen that binds to of features that have been described for oxygen. Thus, CO2
sites on hemoglobin does not contribute to the blood levels diffuses from respiring cells into systemic blood capillaries
of oxygen pressure. Thus, the oxygen pressure is deter- and then flows to the lung, where it diffuses across the vas-
mined by the amount of free oxygen in the blood plasma cularized pulmonary parenchyma into the air of the lumen,
immediately surrounding the hemoglobin. At any given from where it is ultimately ventilated away to the atmo-
level of this pressure, the hemoglobin saturates to the ex- sphere. Some of the CO2 forms an attachment with hemo-
tent determined by its binding properties in relation to the globin, but in a way that is different from oxygen and in far
oxygen pressure. lesser amounts. The majority of the gas becomes hydrated
Like other vertebrates, the hemoglobins of various spe- and is transported in plasma in the form of bicarbonate ion
cies of snakes are adapted to load and deliver oxygen ac- (HCO3−). Carbon dioxide is highly soluble in water, and rel-
cording to evolved properties that are appropriate for the atively little is transported as a gas in physical solution. He-
gaseous environment, rate of metabolism, and the activity moglobin also plays an important role in buffering the pH
regimen of the animal, but these have been studied in but a of the blood, for acid is formed when CO2 combines with
few species of snakes. The blood of file snakes (Acrochordus water to form H+ and HCO3−.
spp.) is unusual because of their generally sluggish behav- The control of breathing and transport of blood gases is
ior, comparatively low rates of metabolism, and especially driven by the need to eliminate CO2 as much as the need to
their tendency to be reclusive—probably to avoid possible acquire oxygen. Also, the need to eliminate CO2 is coupled
predators. These snakes have a comparatively large volume to the requirement for regulating the pH of blood and other
of blood, a high ratio of red blood cells (and thus hemoglo- body tissues. Because the hydration reaction of CO2 to form
bin) to plasma, and possession of hemoglobin that has an bicarbonate (HCO3−) also produces acid (H+), respiration
unusually high affinity for oxygen and is capable of binding tends to acidify the blood unless the H+ is buffered and/or
oxygen at relatively low oxygen pressures. These aquatic removed from the body. Both processes occur. Hemoglobin
snakes exchange a portion of their respiratory gases across and other components of the blood tend to buffer the H+,
the skin (8–24 percent of O2; 33–76 percent of CO2), so it is but over time the CO2 being produced from metabolism
important that the hemoglobin not release its oxygen at must be eliminated or the pH will ultimately decrease to
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lethal levels. Decreases in blood pH and increases in blood displays. Irritated rattlesnakes, for example, characteristi-
CO2 tend to provide the more important respiratory signals cally coil with an inflated body while rattling (fig. 6.17). Also
controlling ventilation in tetrapod vertebrates, although in connection with defense, this inhaled air can be expelled
diminishing levels of blood oxygen also participate. to produce loud hissing sounds in a variety of species (see
chapter 8). More about inflation displays is explained in the
Nonrespiratory Functions of the Lung next section.
The saccular segment of lung—simply called “air sac” in ear- Bayard Brattstrom is one of the first of many herpetolo-
lier literature—functions as a “bellow” because the volume gists to have suggested there are various other functions of
expansion of the entire lung pulls air into the “sac” and this the saccular lung that are related to physiology. When
same air exits the lung when it is expired. Hence, the rela- snakes become overheated, they may begin to pant, as do
tively large volume of the saccular region of the lung helps lizards and other terrestrial vertebrates. Panting consists of
to ventilate the vascular lung, in essence alternately “pull- rapid, shallow breathing that exchanges air across the moist
ing and pushing” air across it. The saccular region also al- membranes of the lung and its associated airways. This con-
lows storage of air, in addition to that which is within the vection removes water by evaporation, and in the process
vascular lung. This means there is added storage of oxygen, heat is also removed from the evaporating surfaces. This is
which can be moved to the faveolar surfaces either by diffu- called evaporative cooling and is a mechanism employed to
sion or, more effectively, by convection due to body move- cool the body, or at least slow the rate of warming toward a
ments or active contractions of smooth muscle that occurs lethal temperature. If the body has been warmed through
in the lung wall. The bellows and storage functions of the accumulation of heat from solar radiation or contact with a
saccular lung are, of course, indirectly related to respiration. warm substrate, it likely will be warmer than the sur-
The storage function might be particularly important in rounding air. Therefore, air that is moving in and out of the
aquatic or semiaquatic species of snakes because it in- lung will remove heat by internal conduction and radiation
creases the time that a snake might remain submerged from the body surrounding the lung as well as from evapo-
without needing to surface for breathing air. In sea snakes rative cooling of the lung parenchyma (largely in the ante-
the terminal saccular segment of the lung is exceptionally rior part of the lung and associated airways such as the
thick and muscular (fig. 6.16), presumably important for trachea). Of these phenomena, evaporative cooling is likely
storage but with capability to “inject” by muscular contrac- to be most significant (see fig. 4.13; also chapter 4).
tion the pressurized air into the respiratory parenchyma at The saccular lung might also play some role in reducing
periodic intervals. No one knows if, or how, this feature is the temperature of the testes in male snakes. Sperm devel-
actually used by sea snakes. opment is sensitive to temperature, and heat-induced ste-
Inflation of the total lung increases the body size of a rility is the probable reason for the descent of the testes in
snake, and extreme inflation is typically used in many pit vi- mammals, which keeps the testes generally at temperatures
pers to enlarge the appearance of the body during defensive that are lower than the core body temperature. Cooler air
Figure 6.16. Muscular termination of the

saccular lung of a Chinese Sea Krait (Laticauda
semifasciata). The white, opaque, and thick
appearance of this organ reflects its function for
storage, having lots of muscle and thick tissue that
is not well vascularized for gas exchange. The
arrow points to the termination of the vascular lung
that is functional with respect to gas exchange.
The red lung tissue to the left of the arrow is the
posterior aspect of the vascular lung, the arrow
indicating its transition to saccular lung near the
termination of the pulmonary artery. Above the
lung structure an engorged portal vein can be seen
returning systemic blood to the heart through the
liver. Photograph by Coleman Sheehy III.
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Figure 6.17. A Western Diamond-backed Rattlesnake (Crotalus
atrox) in a defensive posture. The lung is abnormally inflated by the
snake to increase its apparent size, which accounts for the spreading
of scales to reveal the interscale tissue—most notably visible in the
lower front of the figure. This snake was photographed in Texas by the
author.
that is ventilated in the posterior saccular lung might play

some role in the regulation of testes temperatures in
snakes.
The entire lung including the extensive saccular segment Figure 6.18. Defensive posture being displayed by a Hill Death
Adder (Acanthophis rugosus) in northern Queensland. The upper
in terrestrial species appears to be important in assisting
photo shows the snake’s normal body form before flattening. The
support of the body, given that ribs are free ventrally except lower photo shows the snake while it is flattened in defensive
for attachment to skin and there is no sternum. When air is posture. Note the body is extremely flattened, likely in attempt to look
withdrawn entirely from the lung, terrestrial snakes can be- larger to a potential predator. The color of this snake matches that of
come extremely flattened when fully extended on a flat sur- “red” soils characteristic of the region in which it was photographed.
face (fig. 6.18). Adjustments of the total lung volume also Photographs by Lauren Dibben.
are important for the ability of sea snakes to control buoy-

ancy and orientation. Diving marine snakes have been ob- The tracheal air sacs of the Asian Red-tailed Rat Snake,
served to vent excess air after arriving at a particular place Gonyosoma oxycephalum, are representative and illustrated
in a water column (sea snakes, fig. 6.14, and Acrochordus), or in figure 6.19. These structures are located in the ventral
to adjust their vertical location (Yellow-bellied Sea Snake, body cavity immediately below the trachea. They are de-
Pelamis platurus) soon after submerging from a bout of air- rived from the tracheal airway, but are secondary and acces-
breathing at the water surface. Presumably, these snakes sory parts of the pulmonary system. The air sacs are thin,
are adjusting buoyancy to a neutral condition that is appro- fragile, translucent, and poorly vascularized membranes.
priate for the particular depth at which they choose to re- They do not receive blood from the pulmonary artery and
main or be active. cannot have any direct significant role in respiratory gas ex-
change. Each individual air sac is separated from adjoining
Structure and Function of Tracheal Air Sacs neighbors by a transverse septum, and there are 11–15 sep-
More than 30 species of Asian snakes possess tracheal air arate sacs associated with the trachea and collectively ex-
sacs, which are nonpulmonary, saccular extensions of the tending from the head to the heart (about 16 percent of
trachea and have been called various names including tra- total body length). The air within each air sac communi-
cheal diverticula, neck sacs, and tracheal chambers. These are cates with tracheal air by means of a foramen (hole) in the
present in numerous colubrid snakes, especially arboreal tracheal membrane, just above the tips of the cartilaginous
species, and the King Cobra, Ophiophagus hannah. All of the tracheal rings (fig. 6.19). There is a single foramen associ-
genera, and probably all of the species, that possess these ated with each individual air sac.
structures engage in some form of extended neck display, The air sacs might be inflated by one or a combination
and all are restricted to central and southern Asia. of two mechanisms. Ventral expansion of the neck might
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membranes, in addition to control by adjoining lung pres-
sures or movements of the body wall.
There are two plausible functions of the tracheal air
sacs of snakes. First, Bruce Young has shown experi-
mentally that these saccular structures can act as reso-
nating chambers that modify the acoustic properties of
hissing sounds, especially in the King Cobra (see also
chapter 8). Second, the air sacs greatly enlarge the neck
in a vertical dimension during defensive neck displays.
In the Red-tailed Rat Snake, neck displays are easily
evoked when snakes are disturbed, and the air sacs be-
come prominent by extreme inflation during a display
(fig. 6.19). Both of these functions—sound modification
and neck inflation—are related to defense.
Concluding Remark
Few persons probably give much thought to how the blood
circulates within a snake and how the lung functions to as-
sist in the delivery of oxygen. Yet these are absolutely crit-
ical needs in the life of a snake, and both circulatory and
pulmonary functions depart from the ordinary because of
the elongate body of a snake, how it feeds, and how it
moves. Understanding the physics of blood circulation, for
example, can open one’s eyes to understanding some of the
environmental constraint that influences the behaviors of
snakes, and how evolutionary adaptation can be so very dif-
ferent in aquatic and terrestrial environments. Hopefully,
the subjects discussed in this chapter will help to stimulate
one to ponder more deeply, and to contemplate new ques-
tions, regarding the structure and function of these fasci-
nating reptiles.
Figure 6.19. Inflation of the neck by tracheal air sacs in the arboreal
Red-tailed Rat Snake (Gonyosoma oxycephalum). The upper photo
shows a snake with its neck inflated in a defensive display, and the
Additional Reading
individual air sacs can be seen as distinct bulges at the anterior
Brattstrom, B. H. 1959. The function of the air sac in snakes. Her-
aspect of the neck. The middle photo illustrates a dried cast of
petologica 15:103–104.
several air sacs with one unit cut open to reveal the open space inside
Brischoux, F., G. E. A. Gartner, T. Garland Jr., and X. Bonnet. 2011.
and its communication with an individual foramen (arrow) that
Is aquatic life correlated with an increased hematocrit in
perforates the tracheal airway. In the lower photo the foramen and
snakes? PLoS ONE 6(2): e17077. doi:10.1371/journal.pone.
cartilaginous tracheal rings are seen with more detail in fresh tissue.
0017077.
The foramen or aperture opens in the tracheal membrane and is about
Burggren, W., A. Farrell, and H. Lillywhite. 1997. Vertebrate cardio-
3 mm in diameter. Photographs by the author.
vascular systems. In W.H. Dantzler (ed.), Handbook of Physiol-
ogy, Section 13: Comparative Physiology, Vol. I. Oxford
University Press: New York, pp. 215–308.
enlarge the air sacs and draw air into them under negative Conklin, D. J., H. B. Lillywhite, B. Bishop, A. R. Hargens, and K. R.
pressure. Or air might be forced into the air sacs from the Olson. 2008. Rhythmic contractility in the hepatic portal
trachea and lung, which would be a positive pressure “corkscrew” vein of the rat snake. Comparative Biochemistry and
mechanism. Because the air sacs can be seen to bulge Physiology, Part A, 152:389–397.
during defensive displays (fig. 6.19), it seems likely that a Frenkel, G., and E. Kochva. 1970. Visceral anatomy of Vipera
palaestinae: An illustrated presentation. Israel Journal of Zool-
positive mechanism is active at least in some circum-
ogy 19:145–163.
stances. Also, the membranous air sacs are overlain by Graham, J. B., J. H. Gee, J. Motta, and I. Rubinoff. 1987. Subsurface
muscle, so there is some likelihood that contractile activity buoyancy regulation by the sea snake Pelamis platurus. Physio-
of these muscles exerts forces directly on the saccular logical Zoology 60:251–261.
www.pdflobby.com
Jensen, B., A. S. Abe, D. V. Andrade, J. R. Nyengaard, and T. Wang. Pough, F. H., and H. B. Lillywhite. 1984. Blood volume and
2010. The heart of the South American Rattlesnake, Crotalus blood oxygen capacity of sea snakes. Physiological Zoology
durissus. Journal of Morphology 271:1066–1077. 57:32–39.
Jensen, B., J. M. Nielsen, M. Axelsson, M. Pedersen, C. Löfman, Rosenberg, H. I. 1973. Functional anatomy of pulmonary ventila-
and T. Wang. 2010. How the python heart separates pulmonary tion in the garter snake, Thamnophis elegans. Journal of Mor-
and systemic blood pressures and blood flows. Journal of Biol- phology 140:171–184.
ogy 213:1611–1617. Seymour, R. S. 1974. How sea snakes avoid the bends. Nature
Jensen, B., J. R. Nyengaard, M. Pedersen, and T. Wang. 2010. Anat- 250:489–490.
omy of the python heart. Anatomical Science International Seymour, R. S. 1982. Physiological adaptations to aquatic life. In C.
85:194–203. Gans and F. H. Pough (eds.), Biology of the Reptilia, vol. 13, Phys-
Lillywhite, H. B. 1985. Postural edema and blood pooling in snakes. iological Ecology. New York: Academic Press, pp. 1–51.
Physiological Zoology 58:759–766. Seymour, R. S. 1987. Scaling of cardiovascular physiology in
Lillywhite, H. B. 1987. Circulatory adaptations of snakes to gravity. snakes. American Zoologist 27:97–109.
American Zoologist 27:81–95. Seymour, R. S., and J. O. Arndt. 2004. Independent effects of
Lillywhite, H. B. 1995. Evolution of cardiovascular adaptation to heart-head distance and caudal blood pooling on blood pres-
gravity. Journal of Gravitational Physiology 2:P1–P4. sure regulation in aquatic and terrestrial snakes. Journal of
Lillywhite, H. B. 2005. Cardiovascular adaptations to gravity: Lessons Experimental Biology 207:1305–1311.
from comparative studies of snakes. In A. Hargens, N. Takeda, Seymour, R. S., and H. B. Lillywhite. 1976. Blood pressure in snakes
and P. K. Singal (eds.), Adaptation Biology and Medicine, vol. 4, Cur- from different habitats. Nature 264:664–666.
rent Concepts. New Delhi, India: Narosa Publishing House, pp. Wallach, V. 1998. The lungs of snakes. In C. Gans and A. S. Gaunt
68–81. (eds.), Biology of the Reptilia, vol. 19. Ithaca, NY: Society for the
Lillywhite, H. B., J. S. Albert, C. M. Sheehy III and R. S. Seymour. Study of Amphibians and Reptiles, pp. 93–295.
2012. Gravity and the evolution of cardiopulmonary morphol- Young, B. A. 1991. Morphological basis of “growling” in the King
ogy in snakes. Comparative Biochemistry and Physiology Part A Cobra, Ophiophagus hannah. Journal of Experimental Zoology
161:230–242. 260:275–287.
Lillywhite, H. B., and T. M. Ellis. 1998. Structure and function of Young, B. A. 1992. Tracheal diverticula in snakes: Possible
tracheal air sacs in the Asian snake Gonyosoma oxycephalum. functions and evolution. Journal of Zoology (London)
Hamadryad 23:121–126. 227:567–583.
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PE RC E IVING T HE SNAK E ’S W O RL D
Structure and Function of Sense Organs
As one approaches a snake in the wild, the first evidence that the presence
of an intruder has been recognized is likely to be given by the tongue. The
eyes are without the possibility of expression or winking; there are no ears to
7
cock forward. Instinctively endeavoring to remain undiscovered through its
blending coloration, the snake will seldom move until it seems to detect that
it has been noticed by the trespasser. And so the flicking tongue is being
employed in some way to investigate the stranger; to give some indication of
his character and intentions. Until quite recently, the nature of the impression
conveyed by the tongue and the course of its transmission to the snake’s
consciousness were unknown. Now the tongue is believed to be an adjunct
to the sense of smell, although not the sole vehicle of that sense.
—Lawrence M. Klauber, Rattlesnakes. Their Habits, Life Histories, and

Influence on Mankind (1956), 396–97
The Need for Information environment first, sensory structures tend to be concentrated
Try to imagine how a snake perceives its world as it slithers at, or near, the head. This is true for snakes, although the body
through grass, makes its way through tropical vegetation is also rich in having numerous sensory structures and re-
high in a canopy forest, or swims through the ocean across sponses to the environment. In this chapter we shall explore
a coral reef. Behind your head is a long, thin body. You have the sensory world of snakes, considering what is known about
no external ears, but your eyes are large, your tongue flicks the various senses and the organs that acquire information in
regularly, and your long body pushes against fluid or objects various modalities.
in the physical environment. We know that snakes have The term modality refers to the qualitative nature of a
marvelous senses, including ways of perceiving their world stimulus—whether it is light, sound, vibration, and so on. A
in some ways that we cannot. Some senses have been well stimulus refers to any form of energy that excites a receptor,
studied, while others have been neglected relative to what and a receptor in turn is defined as a structure that is excited
is known in other animals. What is certain is the brain of a by, and transduces, a stimulus. Receptors are typically special-
snake receives a rich variety of information about its exter- ized nerve endings or sometimes other cells that are modified
nal world, and this information is important to the survival to receive a particular stimulus and are themselves coupled to
and success of snakes as a group. specialized nerve endings. The rods and cones of the eye are
During the evolution of vertebrates, increases in body size examples. A transducer is any device (biological or not) that
and specializations for living in many different habitats oc- changes energy from one form to another. So, continuing
curred only with an increase in capacity for constant sur- with the eye as an example, the rods and cones transduce cap-
veillance of the environment. Animals acquired increasing tured light energy that falls upon them into the bioelectric
sensory capabilities for acquiring information, as well as de- signals that travel along nerve membranes. It is amazing to
velopment of the central nervous system for processing think that, regardless of the modality of stimulus—light,
and using the information. Animals had to know what was in heat, sound, and so on—all stimuli are transduced into the
their environment and how to respond appropriately. Because same form of energy that travels as nerve impulses to the
the head end of bilaterally symmetric animals meets the brain. The specificity of the nerve pathway and the area of
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the brain receiving signals determine the sensation that the what is called the “white” of the eye in humans. The sclera of
animal perceives, such as light or sound. snakes does not possess a densely fibrous, cartilaginous, or
bony ring that is present in some other vertebrates, how-
ever. The entering light next passes through fluid within the
Vision: What the Eyes See eye chamber and is absorbed by the retina, which is a tissue
Snakes generally have good vision, but it is better developed layer containing the visual receptors, termed rods and
in arboreal snakes than in many others, and is poorly devel- cones. Just behind the cornea are the iris and lens. The iris
oped in burrowing and possibly some aquatic species living consists of pigmented smooth muscle surrounding an
in turbid waters. Fundamentally, the eye of a snake is quite opening called the pupil. The iris can constrict or dilate and
similar in physical features to the eyes of other vertebrates, thereby controls the aperture of the pupil, allowing more or
including humans (fig. 7.1). It is shaped like a cup. There is a less light to enter. In dim light the iris dilates, the pupil en-
bilaterally symmetric pair on the head, and the “eyeball” is larges, and more light is allowed into the eye (fig. 7.2).
spherical. Light entering the eye passes through a trans-
parent layer of tissue called the cornea, which is continuous
with connective tissue termed the sclera. The latter forms
Figure 7.2. Photographs of two viperid snakes illustrating differences

in pupil dilation. The upper photo is a Palestine Viper (Daboia
palaestinae) that was photographed in bright light. The lower photo
Figure 7.1. The eye of a Yellow-bellied Sea Snake (Pelamis platurus) features a Timber Rattlesnake (Crotalus horridus) that was
(upper photo) and a GreenTree Python (Morelia viridis) (lower photographed in dim light. Both species have a vertically elliptical
photo). Notice the diffuse pigments in the eye of the sea snake and pupil, but the pupil in the upper photograph is relatively more
the vertically elliptical pupil of the tree python. The upper photograph contracted to admit less light under the brighter condition. Both
is by Coleman Sheehy III, and lower photograph is by Nicholas snakes were captive specimens at the University of Texas at Arlington
Millichamp. and were photographed by the author with permission of Carl Franklin.
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In species having a so-called “slit pupil” (figs. 7.1, 7.2, 7.4. order to produce a clear image, the light must converge at a
7.5) the arrangement of muscles around the “slit” makes it focal point that is on the retina (fig. 7.3). This is accom-
easier to control the amount of light entering the eye with plished in snakes by moving the entire lens in relation to
minimum muscular contraction. Slit pupils can open to a the retina using muscles within the iris. Enlarged muscles
fully round pupil in dim light, and the slit is not required for of the iris apply pressure to the vitreous fluid, which forces
nocturnal vision. A number of nocturnal species do not the rigid, spherical lens forward. The lens moves back pas-
have a slit pupil and are well able to see under conditions of sively when these muscles are relaxed. Such a means of so-
dim light. The slit simply affords finer control over light en- called accommodation is a principal difference from other
try in nocturnal or crepuscular species having retinas that vertebrates in which the eye is focused by changing the cur-
are adapted for dim light conditions, but might also be ex- vature of the lens by means of ciliary muscles (also called
posed to bright light conditions. “ciliary bodies”) that were conceivably lost in the ancestors
The lens is behind the iris and bends the light rays to- of snakes. The peculiar mechanism for focusing the eyes of
ward each other as light passes through this structure. The modern snakes is presumably derived independently from
bending of light in this way is called refraction, and the de- other vertebrates, and likely represents the evolutionary
gree of refraction depends on the curvature of the lens. The “use” of the degenerated ancestral eye parts.
cornea also refracts light, and the further refraction af- Snakes lack eyelids, and what is called a spectacle consists
forded by the lens is simply “fine-tuning” of the process. of fused corneal and scleral tissue with epidermis. The spec-
The point at which the light rays converge after passing tacle is protective and serves the same function as eyelids.
through the cornea and lens is called the “focal point.” In In addition, the spectacle has been shown to contribute to
Figure 7.3. Schematic illustration of a generalized eye of a snake. Light passes through the lens and activates photoreceptors that are arrayed on
the retina. Snakes focus the light by means of contracting iris muscles that increase pressure on the vitreous fluid and thereby move the lens
forward. The dashed lines indicate such movement of the lens. Drawing by Dan Dourson.
Perceiving the Snake’s World | 165
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Figure 7.4. Head of an Emerald Tree Boa (Corallus caninus) that is
beginning to shed its outer generation of epidermis. The shed Figure 7.5. Head view of an arboreal Oriental Whipsnake (Ahaetulla
spectacle that previously covered the eye can be seen immediately prasina) featuring the keyhole eye and lateral depression along the side
behind the eye (white arrow). Note also a series of labial pits running of the head, extending from the eye to the snout. The inset illustrates
lengthwise along the series of upper labial scales (black arrows). The binocular vision and overlap of the visual field in this species, related to
external nostril is at the front of the head to the left in the photo. the narrowed snout and the relative position of the eyes. Note the
Photograph by Elliott Jacobson. extended tongue with tines together. Photograph by the author.
the refractive properties of the eye. The spectacle is renewed Depending on the pigments that are present, diurnal snakes
when the epidermis is shed at each skin-shedding cycle (fig. possess dichromatic or trichromatic color vision. Under cer-
7.4). Because of the lack of eyelids, snakes will never wink at tain conditions of moderate lighting, rod pigments may also
you in spite of what they might be thinking. be active and contribute to what some have called a “condi-
Most snakes, as well as most vertebrates, have two over- tional” form of color vision.
lapping visual systems within the retina. One contains rods, On the other hand, crepuscular, nocturnal, or burrowing
which are sensitive to dim light and are responsible for species of snakes often have a slit pupil and a retina that has
night vision, and the other contains cones, which provide exclusively or mostly rods. Only very recently have the mo-
color vision under conditions of bright light. Rods and lecular properties of visual pigments been studied in snakes.
cones are light-sensitive cells that are characterized by pos- Certain henophidian snakes that are partly nocturnal (Ball
session of different visual pigments called “opsins.” These Python, Python regius) or nocturnal and semifossorial (Sun-
are proteins that are conjugated with a light-absorbing de- beam Snake, Xenopeltis unicolor) were shown to possess du-
rivative of vitamin A. Eyes that possess both rods and cones plex retinas, although rods accounted for more than 90
are said to have “duplex retinas.” percent of the total photoreceptors. Although these snakes
Gordon Walls, who was a research associate in ophthal- are phylogenetically basal, their cones express two of the
mology at Wayne University College of Medicine, wrote an four classes of ancestral vertebrate cone pigments and pro-
early treatise on the adaptive diversity of vertebrate eyes vide these species with dichromatic color vision. In strictly
and pointed out that the eyes of snakes exhibit a wide range fossorial species, however, there is no need for color vision,
of ratios of rods to cones. Many snakes are considered to which is likely to be totally lacking in many such snakes.
have color vision, except for burrowing forms in which the Yang Liu and collaborators have investigated the varia-
eyes are degenerated to varying degrees. Diurnal snakes— tion of the size of eyes and how this correlates with behav-
especially many terrestrial colubrids and elapids—have a ior and habitat among colubrid species of snakes. The
round pupil and a retina that is characterized by a high ratio diameter of the eye is larger in diurnal than nocturnal spe-
of cones to rods. The various types of cones contain pig- cies, both in absolute and relative terms. Furthermore, ar-
ments that are sensitive to different colors, although color boreal species have larger eye diameters than do terrestrial
vision can be restricted depending on the degree of spectral and aquatic species. The eye diameters of terrestrial spe-
overlap of the pigments. Some diurnal elapids and colubrids cies are similar to those of semiaquatic species, but larger
(e.g., garter snakes, Thamnophis sirtalis) have been shown to than those of fossorial species. The findings suggest that
have a retina that contains strictly cones, and there are four variation of eye size reflects adaptation to specific habi-
distinct cell types expressing different visual pigments. tats, foraging, and other behaviors.
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The pair of eyes that occur on the head
of snakes occupy a considerable variation
of position, usually on the sides but
having varying distances from the snout
and sometimes positioned higher on the
head. Probably most snakes have a wide
field of vision, ranging from a little over
100° to more than 160° in various species.
Snakes also have binocular vision, which
refers to the overlapping visual fields of
the two eyes (fig. 7.5). Images are focused
on each of the two retinas simultaneously,
and this aids in the perception of depth
and distance. Binocular vision is espe-
cially well developed in species of arboreal Figure 7.6. Dorsally positioned eyes in two highly aquatic homalopsid snakes, Jagor’s
snakes, which must judge distances and Water Snake (Enhydris jagorii) (left) and the Rice Paddy Snake (Enhydris plumbea)
slight movements during prey capture. In (right). Snakes were photographed in Thailand by John C. Murphy.
the Asian colubrid Ahaetulla prasina (an
arboreal species), the range of binocular
vision is about 45° compared with 20° to 30° in some other some burrowing or desert snakes that spend time cratered
species. In this and some other arboreal colubrids, the into sand with just the eyes protruding (figs. 1.20, 3.16).
snout is pointed and there is a depression on each side of The coloration of the eyes of snakes shows much varia-
the head that minimizes the nasal area and thereby in- tion, often related to rendering the eye inconspicuous. Eye
creases the range of visual overlap for the two eyes (fig. 7.5). stripes and other forms of head coloration also serve to ren-
Snout attenuation is characteristic of many species of arbo- der the eyes cryptic (see figs. 1.29, 1.32, 1.36, 1.43, 1.48, 7.8).
real snakes, likely as an aid for enhancing binocular vision. However, in many snakes the eyes are also very conspic-
Also, when these snakes orient to a prey, the tongue is ex- uous, perhaps the inadvertent result of its necessary prom-
tended with the tines together, almost as if it acted as a inence as a sensory organ. To be quite honest, we do not
“pointer.” know why the eyes of many snakes are colored the way they
Perhaps a dozen or more arboreal colubrid snakes in Asia are, nor need we always assume that these colors have some
and Africa (e.g., Dryophis, Ahaetulla, Thelotornis) have hori- functional or adaptive value (see fig. 1.53).
zontal pupils that provide “wraparound” vision while en- Many snakes that are diurnal predators depend highly on
larging the forward binocular field. The shape of the pupil in vision for orientation to objects. They can maintain visual
some species also resembles a “keyhole” that is centered over contact with potential prey items and respond to subtle
the lens (fig. 7.5). These snakes are considered to have very cues such as respiratory movements of lizards and the
acute vision and comparatively keen abilities to detect move- movement of antennae of insects. Visual information about
ment and to judge distance. They also possess a fovea centralis, the position and prominence of an object is increased by
which is a depression on the retina where there is a relatively viewing it from more than one angle simultaneously, con-
high density of cones and therefore maximal visual acuity. ferred by binocular vision, or in rapid succession invoked by
Some aquatic or semiaquatic species that spend time movements of the head. Head swaying occurs in a number
with the head at the surface of water have eyes that are of snakes in contexts related to prey capture.
positioned higher up on the head (fig. 7.6; see also figs.
1.23, 4.8). This enlarges and shifts the binocular field of
vision so that these snakes can better see what is above Hearing, Vibrational, and Equilibrium
them, whether in water or at its surface. Examples are the Sense: Function of the Ears
file snakes (Acrochordus spp.) and some homalopsid spe-
cies (e.g., Cerberus rhynchops). Many bottom-dwelling Hearing and Vibration Sense
fishes also have dorsal binocular fields. Moreover, the Snakes do not have external ears such as the elaborate
higher the eyes, the lesser amount of head that needs to structures characteristic of terrestrial mammals that func-
protrude above the water when the snake is at the surface, tion to collect and focus sound energy onto a tympanic
which might render snakes less conspicuous to visually membrane. Nor do snakes have a tympanic membrane or
oriented predators. The eyes are also dorsally displaced in any external opening or canal that conducts sound energy
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to the inner ear, which is the organ of hearing. In other mammals. The columella is attached by means of a short lig-
words, snakes have (secondarily) lost a tympanum and ament, and sometimes cartilaginous structures, to the
middle ear, which previously evolved independently in all quadrate bone, which is the posterior element of the upper
major lineages of tetrapods. Because snakes are anatomi- jaw and articulates with the lower jaw at the rear angle of
cally peculiar in this way—possibly a reflection of fossorial the head (see fig. 7.7; also figs. 2.5, 2.6). Thus, either airborne
or aquatic ancestry—it was thought for many years during sound pressures or vibrations from the ground affecting the
the history of herpetology that snakes cannot hear. The body of a snake are transmitted through tissues surrounding
inner ear is well developed, however, so many herpetolo- the jaws, the bones and joints of the jaw, the long axis of the
gists assumed that it responds to vibrational stimuli that columella, and finally to fluid of the inner ear on which the
are first transmitted from the ground through the head tis- other end (footplate) of the columella is attached. The space
sues, and ultimately to the sensitive receptors that are re- that accommodates the columella is extremely reduced and
sponsible for hearing in other vertebrates. Since the 1970s immediately surrounds this structure, or is lost entirely.
it has been learned from both physiological and behavioral The inner ear of snakes is fundamentally similar to that
studies that snakes indeed respond to vibrational stimuli of other vertebrates (fig. 7.7). It consists of a bony structure
that occur on the ground, in air, or even water. Therefore, that encloses a labyrinth of liquid contained within saccular
the popular notion that snakes are deaf is not true, al- structures, semicircular canals, and a cochlear duct or canal.
though hearing is restricted to a limited range of sound The latter is an outgrowth of the saccular structure and be-
frequencies, from approximately 50 to 1000 Hz (= cycles comes elongated and coiled to form the cochlea of mam-
per second). By comparison, humans can sense airborne vi- mals. The structure is not elongated in snakes or other
brations in the range from 20 to 20,000 Hz. By definition, reptiles, but like the cochlea of mammals contains sensitive
hearing refers to the sensory detection of airborne vibra- hair cells that are arrayed on a vibration-sensitive membrane
tions by the inner ear, as distinct from very low-frequency called the basilar membrane. This is the region of the inner
vibrational stimuli transmitted by the ground or by solid ear that is sensitive to vibrational stimuli or sound and pro-
objects that might be in contact with an animal. vides the sense of hearing. Energy in the vibrational move-
Snakes lack a tympanic membrane, or eardrum, and the ment of the columella moves the oval window, a membrane
element responsible for transmitting vibrational stimuli to that moves to create vibrational waves in the liquid of the
the inner ear consists of a single thin bone called a columella. cochlear canal. These movements in liquid cause motion of
The columella is equivalent to what is termed the stapes in the basilar membrane, which in turn creates shearing move-
ments of the hair cells. The cellular mem-
branes of the “stimulated” hair cells create
the bioelectric potentials that are ulti-
mately expressed as nerve signals that
travel through the auditory nerves to the
brain where the “sound” is interpreted.
Christian Christensen and colleagues
recently demonstrated that Ball Pythons
(Python regius) are sensitive to sound-
induced vibrations, but they have lost
the sensitivity to airborne sound pres-
sure that is sensed by the tympanic
membrane of other tetrapods. Both
aerial sound and substrate vibrations
that are incident on a snake’s body are
transmitted to the inner ear by a me-
chanical pathway through the tissues of
the head. The ear transduces the tissue-
borne vibrations into a neural response
that travels to the brain via the auditory
nerve. The original stimulus of sound or
Figure 7.7. Schematic illustration of the hearing apparatus of a snake. The individual vibration can elicit a response regardless
elements of artwork were drawn by Dan Dourson and based, in part, on figs. 20-12, 20-16, of where it impinges on the snake (head,
and 20-21 in E. G. Wever, The Reptile Ear (Princeton, NJ: Princeton University Press, 1978). tail, trunk, or tail).
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It is not clear why the hearing of snakes is restricted to saccular structures (sacculus, utriculus) and semicircular
such a narrow band of frequencies. This could be related to canals of the inner ear. These hair cells are sheared by move-
several factors, including (1) the pathway of tissues through ments of fluid and solid structures that might be affixed to
which a sound stimulus must be conducted before reaching the tips of the hair cells when the animal changes position
the basilar membrane, (2) dampening of vibrational stimuli in space. As with auditory neurons, nerve endings associ-
by inner ear fluids that dissipate the pressure waves differ- ated with the vestibular hair cells relay messages on to the
ently than in mammals, and (3) properties of the auditory brain and provide a sense of movement and orientation.
neurons that behave somewhat differently than those of Very little neurobehavioral research has been conducted
other terrestrial vertebrates. Regardless of the frequency with the vestibular system of snakes, which is assumed to
limitations, the sensitivity of snakes to vibration and sound function similarly to that of other vertebrates. Movement
is remarkably good. The populations of neurons that re- and orientation also depend on appropriate inputs from
spond to airborne sounds or ground vibrations are thought proprioceptors in muscles, tendons, and joints. These provide
to largely overlap and could, in fact, be essentially the same. the sense of position and relative motion of body parts.
Given the repertoire of senses that snakes possess, one Interestingly, rat snakes (Elaphe quadrivirgata) have
might question whether hearing or vibrational sense is ac- been subjected briefly to microgravity that is induced mo-
tually useful to snakes and whether acquired acoustic infor- mentarily by parabolic flights using special research air-
mation is used adaptively. It is definitely clear that this is craft. Apparently, the loss of surface contact and normal
the case. An excellent example is the auditory localization proprioceptive stimuli from muscles and joints caused
of ground-borne vibrations in Desert Horned Vipers, these snakes to become aggressive and to strike their own
Cerastes cerastes. Bruce Young and Malinda Morain demon- body when they lost orientation momentarily during free
strated in laboratory studies that these snakes can localize fall that produced microgravity during the parabolic flights
and strike live mice using only vibrational cues. The foot- on the aircraft.
steps of a mouse cause the propagation of surface waves in
sand, and these are detected by the snake when it rests with
its lower jaw on the sand. The incoming surface wave sets Chemoreception: Flicking Tongues and
the two independent sides of the lower jaw in motion, and Sniffing Noses
these vibrational stimuli are then relayed through the quad- Anyone familiar with snakes has noted their tendency to
rate and columella to the inner ear. There are, of course, two protrude the tongue and flick it toward objects (fig. 7.8). In
receivers in the form of each inner ear. Because each side of folklore the serpent’s tongue has been regarded as a
the jaw can move independently of the other, a vibrational stinger, which surely brings death from a venomous spe-
wave originating in sand from the right side will stimulate cies such as the adder. The tongue has also been regarded
the right side of the lower jaw slightly earlier than the left, as a cleaning device and as a tactile structure providing a
and vice versa. A very small difference in the arrival time of sense of fine touch. Today, however, most herpetologists
the wave stimulus at the right and the left ear is sufficient regard the snake’s tongue to be a sensory aid that during
for the snake’s brain to discriminate the direction of the flicking acquires volatile chemical molecules from the envi-
vibration source. ronment and helps to guide the animal’s behavior. Scien-
It has also been shown experimentally that the midbrain tists working in the 1920s and 1930s demonstrated an
of sea snakes (Lapemis curtus) responds with electric poten- important connection between tongue-flicking and the
tials to vibrating motions and pressure fluctuations in chemical senses: molecules acquired by the tongue stimu-
water. The sensitivity is low but probably sufficient for the late chemosensory structures above the palate, which are
detection of fish-generated motions in water. Both file called vomeronasal organs or Jacobson’s organ. Although
snakes (Acrochordus granulatus) and sea snakes (Pelamis pla- much attention has been given to the role of the tongue in
turus) are sensitive to motions caused by swimming fish. chemoreception, it is only an accessory contribution to the
Some sea snakes have been observed to approach and even- rich fabric of chemical senses that help make up a snake’s
tually bite into a vibrating object. Bruce Young has also world. Functional distinctions of the chemical senses are
demonstrated that swimming anacondas will attack under- difficult because of the interplay with other senses and a
water speakers playing the sounds that are made by swim- requirement for very carefully controlled experiments in-
ming rats. volving invasive techniques.
Vestibular System and the Sense of Equilibrium Smell and the Olfactory Epithelium of the Nasal Cavity
As in other vertebrates, snakes possess what is called a The nasal cavity of snakes bears a rich sensory epithelium that
vestibular system consisting of patches of hair cells in the is sensitive to airborne molecules and allows the detection of
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volatile odors. How useful this information is in relation to
other sensory inputs is not entirely clear, and there is much
more scientific work that needs to be accomplished before we
will have a better understanding of this subject. Clearly in
snakes as in many other vertebrates, odorous molecules are
delivered to the olfactory mucosa by inhaling or sniffing with
the nose. Stimulating molecules must be both volatile and ad-
sorbed by the olfactory mucosa.
I once kept a Gaboon Adder (Bitis gabonica, fig. 1.28) for
some while and was impressed at how consistent was its
feeding behavior. Typically, it would lie within a box inside
its cage with its head protruding about half its length from
an opening in the box at the level of the cage floor. Whenever
I put a live mouse or rat inside the cage, the snake remained
perfectly still except for two changes that told me it was alert
to the presence of the mouse. First, there was a brief and
rapid eye movement. Second, body movements indicated the
snake was breathing more rapidly and shallowly, but the
tongue was not protruded in flicking that is characteristic of
many other species when they are presented with food. The
snake waited until the mouse came within a critical distance
of its head before striking and holding the mouse, which was
impaled by the snake’s fangs. This strike distance was sur-
prisingly short—about two mouse lengths—but the snake
always succeeded in capturing and paralyzing the mouse
quickly. One could suppose that the lack of tongue-flicking
was part of the furtive behavior of the snake while it was
waiting to ambush the mouse. It further seems likely that
the rapid but shallow ventilation enabled the snake to in-
crease the rate of sampling of airborne odors emanating
from the mouse. Thus, in this circumstance the chemosen-
sory input from the mouse to snake did not involve the vom-
Figure 7.8. Upper photo: Tongue flick of a False Fer-de-Lance eronasal system, but rather the olfactory epithelium.
(Xenodon rabdocephalus) photographed in Belize by Dan Dourson. Recently, two investigators from Kyoto University, led
Center photo: Tongue flick of a Yellow-lipped Sea Krait (Laticauda by Takushi Kishida, demonstrated that genes related to ol-
colubrina) photographed in Sulawesi by Arne Rasmussen. Note the
factory receptors are greatly reduced in completely aquatic
extent of tongue protrusion is different in the two species and is
exceptionally long in Xenodon. The extent of protrusion in marine sea snakes (hydrophiines) but are still maintained in semi-
snakes is typically less than in terrestrial snakes. Lower photo: terrestrial laticaudine sea kraits (Laticaudini). Relatively
Tongue flick of a Black-headed Python (Aspidites melanocephalus) large-scale degeneration of these genes in the hydrophiine
photographed in northern Queensland, Australia, by the author. Note sea snakes following separation from their terrestrial rela-
the tines are separated in all photographs.
tives supports the hypothesis that olfactory receptors have
little use in the aquatic environment.
volatile chemicals (fig. 7.9). There has been a popular notion
that the olfactory sense originating from activation of these Chemical Sense and the Vomeronasal System
nasal receptors triggers tongue-flicking and is of secondary The vomeronasal system appears to provide highly impor-
importance to the vomeronasal system. However, there are tant sensory input to snakes and influences many of their
behavioral circumstances in which olfaction appears to be behaviors. The vomeronasal organ consists of paired struc-
dominant, and the olfactory regions of the brain are relatively tures located near the nasal cavity from which it originates
large. Moreover, some studies have found the olfactory epi- (fig. 7.9). However, during development it becomes isolated
thelium to be more sensitive than the vomeronasal epithe- from the nasal passages to form two spherical structures,
lium to chemical stimuli. The principal conclusion here is that each bearing sensory epithelia on the inner surface. These
snakes can smell using their nasal passageways to sample open and communicate with the roof of the mouth through
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Figure 7.9. Photomicrograph of a cross-section through the anterior head region of an Eastern Corn Snake
(Pantherophis guttatus guttatus). The nasal cavity and vomeronasal organ both have paired chambers lined with
sensory epithelium. The tissues have been stained with a standard histological stain, H & E. Photomicrograph by
Elliott Jacobson.
two small respective orifices in the palate. Sensory cells to the vomeronasal openings. Early evidence that the tongue
comprising the vomeronasal epithelium contact and react was involved in delivery of particles to the vomeronasal
to molecules that are brought into the mouth by means of organ came from experiments published in 1932 by H. Kah-
the tongue, and the activated cells send nervous signals to mann in which snakes that tongue-flicked a piece of carbon
the accessory olfactory bulb in the brain via the vomerona- and were sacrificed shortly thereafter had sooty particles in
sal nerve. This nervous pathway is separate and different the lumen of the vomeronasal organ. Similarly, snakes that
from that associated with the nasal olfactory epithelium. have tongue-flicked cotton swabs soaked in prey extracts
The stimulus molecules are delivered to the vomeronasal mixed with tritiated proline were shown by subsequent sac-
openings either by direct contact with the tongue or by con- rifice and autoradiography to have radioactive material in
tact with ridges or pads on the floor of the mouth immedi- the vomeronasal organ but not on the olfactory epithelium.
ately anterior to the tongue sheath. Thus, in the latter case, Generally, it is not clear to what extent snakes apply the
stimulus molecules are first wiped from the tongue onto tis- tongue tips to the vomeronasal openings, or simply wipe
sues in front of the tongue sheath before being transferred the adjacent tissues. In many snakes, the tongue tips appear
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to be too blunt to actually enter the vomeronasal canal ori-
fices. Also, some species are observed to completely retract
the tongue into the tongue sheath before the mouth is
closed following tongue protrusion. Experiments using
X-ray cinematography and pythons have shown that the
tongue does not enter the lumen of the vomeronasal organ
during multiple investigative tongue-flicks.
The tongue of snakes possesses morphological specializa-
tions that appear to enhance its ability to collect and trans-
port odorants from the environment during tongue-flicking.
Histological and electron microscopic studies show there are
minute papilla-like processes and shallow depressions of var-
ious sizes on the tongue’s surface, and the forked regions of
some colubrids have modified epithelial cells that bear nu-
merous microscopic projections, termed “microfacets,” while
some other species exhibit ridges made up of projections re-
sembling microvilli and small pores. These are thought to aid
in the collection and retention of odorant particles. More-
over, tissues on the floor of the mouth beneath the openings
to the vomeronasal organs exhibit a surface anatomy of folds
and pores. These oral tissues also contain mucous glands that
provide lubrication and enhance the adherence of sub-
stances. It has been postulated that oral secretions pool in
this region, and these fluids conceivably absorb the odorant
molecules and transport them into the vomeronasal organ.
Thus, the snake’s tongue is used in flicking to sample
odors in the environment and thereby assists with the
detection of chemicals. When the tongue is protruded from
the mouth, the tines are usually spread and are swept through
the air or touched upon the substrate or other objects in
front of the animal and, in so doing, collect a sample of chem-
icals from the environment (fig. 7.10; see also figs. 5.8, 5.12).
The tongue is retracted into the mouth and transfers the
chemical stimuli to the vomeronasal organ via the small
ducts that lead to each organ. The odorant molecules then
bind to receptor cells on the sensory epithelia in the lumen of
each vomeronasal organ. Axons of the receptor cells are bun-
dled together and form the nerve that communicates signals
onward (via other higher-order nerve cells) to the brain.
The signals from each vomeronasal organ appear to be
processed separately within the brain, so that the animal is
able to discriminate stimuli from each tine of the tongue.
Theoretically, this provides a snake with the ability to dis-
criminate between paired stimuli from the two separate
tines and therefore to detect directional differences of Figure 7.10. Tongue-flicking behavior of a Sidewinder Rattlesnake
odorant molecules in the snake’s environment. Many (Crotalus cerastes) photographed by the author in the Anza-Borrego Desert
snakes (but not all) separate the tines of the tongue widely of California. The tines are sometimes together (upper photo) but usually
during flicking, which increases the distance between sam- spread widely as the tongue is waved in a vertical arc while protruded
for several seconds at a time (middle and lower photos). The change of
pling points when odor molecules are being sampled and
tine separation reflects the active muscular control of the tongue. This
retrieved (figs. 5.12, 7.8, 7.10). The greater the distance snake was in a defensive posture during this series of photographs.
between sampling points, the greater the likelihood that When investigating an object more directly, the tongue is protruded
a chemical gradient can be detected during a single flick. toward the object without the wide vertical swing that is seen here.
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Laboratory experiments have demonstrated, however, that given animal, and these are restricted to the mucosa of the
there is no change in the trailing ability of certain rattle- palate adjacent to the vomeronasal organ.
snakes (Crotalus oreganus) when a vomeronasal nerve is Sensory papillae considered to be taste buds also have
unilaterally severed. In other contexts, the tongue may be been described in sea snakes and also a colubrid snake
extended with the tines held together (e.g., fig. 7.5). (Elaphe quadrivirgata), wherein these were demonstrated to
Snakes are well known to use their vomeronasal system to be present along the tooth rows. Each sensory papilla is
detect prey odors, and many investigators consider this comprised of a single taste bud and free nerve endings in
system important for behaviors related to courtship, mating, the epithelium, and there are corpuscle-like structures in
feeding, and aggregation. At least in the more advanced associated connective tissue beneath. These are regarded to
snakes (viperids and colubrids) behavioral performance in represent a compound sensory system that may receive
these contexts falls off if the brain is deprived of input from both chemical and mechanical information from prey.
the vomeronasal receptors. An interesting example is the It remains equivocal whether taste buds on the tongue
well-studied predatory behaviors of rattlesnakes (Crotalus are functionally important, for their presence has been re-
spp.). The brain of the rattlesnake receives input from ported as well as refuted in different species. I have ob-
receptors related to both chemosensory systems, vision, and served behaviors of snakes that involve actions elicited
infrared stimuli from the facial pits (see below). All this in- from tongue protrusion before the tongue is withdrawn
formation is integrated within the central nervous system to back into the mouth, thus suggesting that the tongue itself
produce the appropriate motor response, for example, is sensory. Considering all the information available, there
striking to capture prey. There is convergence in the chemo- seems to be little doubt that snakes possess sensory recep-
sensory systems, which means that neurons conveying infor- tors within the mouth that probably respond to multiple
mation from separate olfactory and vomeronasal receptors stimuli including chemical, mechanical, and (possibly) ther-
act to influence the same cells to which they transfer stimula- mal characteristics of prey. Indeed, they may well possess
tion within the central nervous system. However, when the some of the more specialized and useful chemosensory
brain is deprived of vomeronasal input, strike performance systems that are known among vertebrates.
decreases and trailing behavior following a strike is lost en-
tirely. So the olfactory input does not compensate for the loss
of vomeronasal input, in spite of convergence in these two Sensing Thermal and Infrared Radiation
systems. Further, when snakes are deprived of chemosen-
sory input to the brain, the sensory information from vision Cutaneous Receptors and Temperature Sense
and radiation does not compensate and predatory perfor- Like other vertebrates, snakes are able to sense temperature
mance also declines. Thus, chemosensory information (espe- and respond to gradients of temperature and sources of heat
cially that of the vomeronasal system) seems to be very in their environment. As ectotherms, snakes thermoregulate
important in the multimodal sensory systems involved with most generally by basking at sources of heat that is absorbed
such complex behaviors as hunting and procuring prey. either by radiation or by conduction from the substrate (see
chapter 4). To function effectively and efficiently in its ther-
Do Snakes Have Taste Buds? mal environment, snakes therefore must have a good temper-
There are numerous sources of information about snakes ature or heat sense. Like other animals much of the sensory
that state categorically that these reptiles cannot taste and information related to heat and temperature is probably
they have no taste buds. Usually these statements are fol- sensed by free nerve endings in the skin. Therefore, it seems
lowed by descriptions of the vomeronasal system and its likely that a snake can sense the distribution of temperature
importance in the chemosensory abilities of snakes. Gener- along its body, as well as sense the nature of heat fluxes from
ally, there has been a tendency to downplay, or even ignore, the environment in relation to the length of the body. Much
the sense of taste in snakes—probably in large part due to is known about the properties of thermoreceptors in animals,
the obvious behavior of tongue-flicking and the intense in- but there is a paucity of such information as it applies directly
terest in its significance. The scientific literature on taste in to snakes. Instead, most attention to ophidian heat-sensing
snakes has been limited as well as contradictory. has been directed to understanding specialized infrared re-
Recently, taste buds have been reported to be present on ceptors in boas, pythons, and pit vipers.
the soft tissues inside the mouths of advanced snakes
(Crotalus) and in some basal scolecophidians. These struc- Facial Pits and Sensing of Infrared Radiation in Snakes
tures are similar in appearance in the two disparate groups The ability to sense infrared, or “thermal,” radiation has
and resemble taste organs that have been described in other evolved independently in crotaline pit vipers and in several
reptiles. The number of taste buds is relatively few in any taxa of boas and pythons. Anatomically, the facial pits of pit
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vipers (from which they get the name) occur as a pair of indi- spacing of nanopits on epidermis outside the receptor organ
vidually prominent pit organs, one on each side of the head, areas is different (330 nm). It is not clear, however, exactly
each located generally between the eye and the nostril (fig. where the epidermis from these pit organs was sampled, so
7.11). These are sometimes termed loreal pits as well as facial the functional significance remains uncertain.
pits or pit organs. In some boas and pythons there are multiple, In summary, scale surface and pit organ morphologies have
comparatively smaller pit structures that are aligned along been examined with high-resolution techniques that have re-
variable lengths of the upper and sometimes lower lip, in or vealed three-dimensional details of nanostructures on these
between the scales (figs. 7.4; see also figs. 1.17, 1.22). These are surfaces. The dimensions of micropits are shown to vary de-
termed labial pits in contrast to the loreal pits of pit vipers. The pending on their location on the snake’s body, and the surface
facial pits of pit vipers are considered to be more advanced, of the pit organ is distinct from other scale surfaces that bear
and they differ in some structural details from those of boas
and pythons. In both cases, however, pit organs enable snakes
to detect thermal contrast (fig. 4.13) and to form spatial im-
ages related to radiation from the environment within the in-
frared regions of the electromagnetic spectrum. The infrared
imaging system provides a spatial image of the thermal envi-
ronment and thus complements the snake’s visual system.
The individual pit organ of pit vipers consists of a deep,
saccular pocket having a thin membrane stretched across it.
There is an air-filled chamber behind the membrane, so each
side of the membrane contacts air. The membrane is highly
vascular and innervated with many heat-sensitive receptors,
which are formed at the terminal endings of the trigeminal
nerve. That is, each receptor is part of the trigeminal nerve
and not a separately modified sensory cell. The pit organs of
boas and pythons are similar except the membrane is not
suspended and instead lines the inner reaches of the recessed
pocket. Like the crotaline membrane, the membrane of boas
and pythons is richly innervated and vascularized, but it dif-
fers in not having an underlying cavity. Probably for this rea-
son, infrared detection in pit vipers has been shown to be
more sensitive than that for pythons both in electrophysio-
logical studies of neural responses and in investigations of
behavioral responses. The distance at which snakes can de-
tect an infrared stimulus also differs in the two groups of
snakes: about 100 cm in pit vipers and about 30 cm in boids.
Research using scanning electron microscopy (SEM) and
other imaging techniques has revealed that the stratum cor-
neum of the pit organ is covered with microscopic pores or
indentations termed micropits or nanopits. These vary from
1–2 μm in diameter to smaller than 0.5 μm diameters in
both boid and crotaline snakes. The average spacing of
Figure 7.11. Pit organs of pit vipers. The upper photo illustrates
nanopit arrays on the pit epidermis has been determined to
sensory structures on the head and scales of the Florida Cottonmouth
be from 520 to 808 nm, which is close to a structural spacing (Agkistrodon piscivorus conanti). The external naris (n) and pit organ
required for efficient reflection of ultraviolet and visible ra- (p) are prominent on the head anterior to the eye. Paired apical pits
diation (characteristic of sunlight) without affecting the ab- are visible on some of the body scales just to the left of the arrows.
sorption of infrared radiation. Thus, it has been suggested The white circle surrounds tiny projections on a head scale that are
that the “ultramicrostructural” (nanostructural) features of probably sensory (although this is speculation on the part of the
author). The lower photo illustrates the pit organ (p) just below the
the surface stratum corneum of pit organs protects the in-
arrow on the head of a Chinese Moccasin (Deinagkistrodon acutus).
frared imaging sensors from high-energy flux of photons in The membrane of the pit organ can be seen within the pocket of the
ambient light and selectively absorbs infrared radiation, structure. The cottonmouth was photographed in Florida, and the
thereby enhancing the resolution of infrared images. The Chinese Moccasin was photographed in Taiwan, by the author.
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these same structures. The dimensions, spacing, and size the rich vasculature and blood flow associated with pit
distribution of micropits depend on the scale type, and those organs constitute a cooling system (by carrying heat away)
that are associated with pit organs appear to enhance the ab- that enhances, or fine-tunes, the resolution of images.
sorption of infrared radiation while scattering ultraviolet and Numerous studies have demonstrated the abilities of boid
visible light in comparison with other body surfaces. One and crotaline snakes to utilize pit organs to image and target
other possible advantage of the nanostructural features of pit prey (see fig. 4.13), and these are the only animals known to
organ membranes is to lower the surface thermal conductivity, form images of infrared radiation and to use this information
which might enhance the detection of thermal contrasts re- adaptively. Rattlesnakes that are blinded experimentally, or
lated to patterns of radiation impinging on the pit membrane. are born blind, can target and strike prey accurately. Similarly,
In pit vipers there are roughly 1,600 sensory cells arrayed in boid snakes normal vision is not required for accurate prey
on the membrane, which has a field of view of about 100 de- targeting, although it is interesting that Burmese Pythons (Py-
grees. The open entry to the pit is relatively large compared thon molurus) born with a single eye preferentially target prey
to the membrane, and radiation entering the pit strikes on the sighted side. On the other hand, experimental occlu-
many points on the membrane. If the radiation intensity sion of the pit organs does not eliminate the ability of a rattle-
striking the membrane is larger than the emitted thermal snake to target prey accurately, although the targeting distance
radiation of the membrane itself, the membrane will heat up is decreased. Boid and crotaline snakes are further unique
at that location. The nerve fibers in the membrane are con- among animals in using information from two distinct parts
stantly firing (action potentials, or nervous “impulses”) at a of the electromagnetic spectrum (infrared plus vision) to form
low rate determined by the average thermal radiation of all spatial representations of their environments in the brain.
objects in the receptive field of the pit organ. When a local- Both infrared information and visual information are likely to
ized stimulus (fig. 4.13) raises the temperature of nerve fibers be normally involved in capturing prey. As with eyes and vi-
above “background,” the nerves are stimulated to increase sion, pit organs are often directed forward in such a manner as
their firing rate, which increases the rate of signal traffic to provide overlapping fields of environmental stimulus, anal-
going to the part of brain connected to those particular ogous to binocular vision (fig. 7.12).
fibers. These nerve fibers are estimated to be sensitive to
temperature changes of at least 0.001°C! All of the nerve sig-
nals from the pit organs arrive ultimately at the optic tectum
of the brain, which also receives information from the visual,
motor, and auditory systems. Some of the neurons in the op-
tic tectum respond to combined infrared and visual stimula-
tion, which produce overlapping maps that are relayed to the
forebrain. Thus, the infrared and visual information, along
with other sensory inputs, merges to form imagery of the
external world in a manner that we cannot well imagine.
The spatial heat distribution in the environment pro-
duces a heat image on the pit membrane, but it is blurred to
a large extent. In the brain, however, the superposition of
information enables a reconstruction of the blurred image
on the membrane so that what the snake “sees” in infrared
is conceivably clear and three-dimensional. This provides a
remarkable sense that can detect the difference in tempera-
ture between a moving prey, such as a mouse, and its sur-
roundings on the scale of thousandths of degrees Celsius!
Given the means by which the infrared-sensitive neu-
rons in the pit organ respond to a stimulus, scientists have
been interested in the observation that localized blood flow
in the rich vasculature of the pit membrane changes in re-
sponse to the heating of the receptors that are subjected to
Figure 7.12. Paired facial pit organs of a South American
an infrared stimulus. In response to heating, the smooth
Rattlesnake (Crotalus durissus) and a Chinese Moccasin
muscle elements of the pit organ blood vessels act locally (Deinagkistrodon acutus). The forward-projecting and overlapping
and directly to increase blood flow in response to localized sensory fields of the bilaterally paired pit organs and also the eyes of
heating by a focused laser stimulus. Thus, it is believed that these snakes are evident in these views. Photographs by the author.
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The majority of behavioral research on the use of infra-
red radiation has related to the targeting and capturing of
endothermic prey such as rodents. However, it seems also
obvious that pit organs can be used to survey all of the spa-
tial variation of the thermal environment, and this infor-
mation might be used for judging movements related to
thermoregulation, as well as capturing prey. Indeed, exper-
iments have demonstrated that rattlesnakes use their facial
pits to guide thermoregulatory behaviors. In one series of
interesting tests reported by Aaron Krochmal and George
Bakken, Western Diamond-backed Rattlesnakes (Crotalus
atrox) selected a relatively cool refuge when given choices of
retreat sites that simulated natural conditions of hot desert
habitat. The snakes detected the appropriate artificial
burrow from a distance of about 1 meter. However, when a
snake’s facial pits were blocked with insulating polystyrene
and covered with a piece of aluminum to reflect thermal ra-
diation, it could not locate the cooler burrow as before.
When the foil and polystyrene were removed, the snakes
quickly found the cooler burrows once again. These snakes
clearly were using their facial pits to seek refuge from heat
when placed in a hot environment.
Pit organs are probably used to survey the environment
in a general way, and the infrared imagery that is integrated
with visual and other sensory inputs likely guides a variety
of behaviors. Both prey capture and thermoregulation are
now accepted by scientists to be documented functions of
crotaline facial pits. Some infrared pit organs also respond
to touch, however, and the temperature sensitive neurons
can also function as touch neurons. The evolutionary origin
of these exquisite sensory organs remains an unresolved
mystery.
Figure 7.13. Scanning electron micrographs of the apical pits on
Supranasal Sacs of Vipers an individual scale of a Florida Cottonmouth (Agkistrodon piscivorus
The pit organs of boas, pythons, and pit vipers are exter- conanti). The upper photo illustrates paired pits near the caudal
nally obvious structures, and it is only natural that they (rear) end of a body scale. The lower photo is magnified another
have attracted early attention and study. Less obvious 25-fold and illustrates the transition of scale topography from the
structures in some other snakes might serve similar func- normal sculptured surface (lower aspect of photo) to the flat and
smooth depression of the apical pit (upper left aspect of photo).
tions, however. Many of the Old World vipers (Viperinae)
Photographs by the author.
and night adders (Causinae) possess a supranasal sac, which
is a recess located beneath the supranasal or internasal
scale and the nasal scale. The sac has an inconspicuous slit- Vipers (Daboia russelli) preferentially strike at warm objects
like opening and is innervated by nerve endings much like in the laboratory. Further research will shed more light on
those of the labial pits of boas and pythons. The inner re- the structure and function of these putative sense organs,
cess of the sac bears ciliated epithelium and secretory tu- and perhaps other similar structures are yet to be discov-
bules that evidently deliver mucus that forms a think ered in the facial anatomy of other taxa of snakes.
covering over the epithelium. A small pit has been described within each nostril of
The supranasal sacs of viperine snakes are rarely men- some species of Trimeresurus and in some other pit vipers.
tioned, but some researchers have suggested that they These consist of a minute pore lying on the inner posterior
might function as heat detectors similarly to the more fa- wall of the nostril, without any grooved connection with
miliar pit organs of boids and pit vipers. Behavioral studies the main nasal cavity. These structures have been termed
have shown that Puff Adders (Bitis arietans) and Russell’s “nasal pores,” but their function has not been investigated.
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Sensory Organs in Skin
Imagine again you are a snake, and you
have a very long body without limbs. It
seems a most justifiable conclusion that
sensory input along the length of the
body is an important requirement for
survival. Note also your body is covered
with scales, and there are cornified folds
in the epidermal layers between scales
that allow bending and mobility. Not sur-
prisingly, the scales of snakes have sen-
sory structures that provide important
information about the environment and
a snake’s sense of where it is and how
it should move in response to the envi-
ronment. Cutaneous sensory structures
have been known for a long time, yet we
Figure 7.14. Head of the Tentacled Snake (Erpeton tentaculatum, an aquatic
know comparatively little about the
homalopsid) illustrating the paired mechanosensory appendages (“tentacles”)
details of their function. protruding from the snout. These structures sense vibrational stimuli in water and are
Free nerve endings in the skin are ca- useful, for example, in capturing fish (see chapter 2). The inset shows the epidermal
pable of transmitting information about and scaled nature of the tentacles in closer detail, and also illustrates the closed mode
temperature and mechanical stimuli to of the narial valves. Photographs by John C. Murphy.
the central nervous system, and these are
probably important to the sensory world
of a snake. Other structures appear more prominent and The scales of all snakes have various microstructural fea-
specialized, with attached nerves suggesting these to be tures on their surfaces (see chapter 5), and these include hair-
sensory in function. File snakes (Acrochordus spp.) have like projections, pits, spinules, and what appear to be
prominent epidermal spines on each scale, and these are as- microscopic holes. Some of these features might act as collec-
sociated with a rich blood supply and connections with tion or transducing receivers of information from the envi-
nerves. They are speculated to be mechanoreceptors impor- ronment, but this has not yet been the subject of definitive
tant for detecting water displacements. Little File Snakes, research. Some scientists have even suggested that inner-
Acrochordus granulatus, are very sensitive to mechanical vated scale structures might be used for the detection of weak
stimuli in water, and they respond very rapidly to certain electric fields, as is known in some other aquatic animals.
movements that are made by nearby fishes. These snakes Many snakes (but not all taxa) exhibit structures near the
enwrap fish with body or tail coils with extreme rapidity in posterior tip of the dorsal scales termed apical pits. These are
response to these movements. Thus, it appears the inner- typically paired (symmetrically to either side of the scale
vated spines are used effectively in prey capture. Some sea midline) sense organs recessed in a small depression having a
snakes are sensitive to low-amplitude water motions, and smooth surface and visible to the naked eye in many species
the inner ear cells as well as scale structures may be in- (figs. 7.11, 7.13). They occur on scales over the body and the
volved in the detection of hydrodynamic stimuli. Behav- tail. Similar structures having variable appearances and
ioral studies also indicate that some sea snakes (Pelamis distribution occur on the head scales of snakes, and are
platurus) are sensitive to water motions caused by swim- known as head pits or parietal pits. These may have an elabo-
ming fish. Small spines are sometimes seen on the scales of rate three-dimensional structure within the skin and appear
this species and are probably sensory (fig. 5.9). Physiolog- to be possible sense organs. The function of all these superfi-
ical investigations have demonstrated nerve responses cially positioned “pits” is completely unknown, however.
originating from both mechanoreceptors and separate tem- Harold Heatwole has noted that the tails of certain sea
perature receptors in the skin of snakes, but the precise na- snakes are sensitive to light, and he postulates there are dif-
ture and identity of these receptors is unknown. Some fuse light receptors on the skin of the paddle-shaped tail.
mechanoreceptors of snakes (which respond to vibrations) Olive Sea Snakes (Aipysurus laevis) tend to rest at night with
resemble somewhat the Pacinican corpuscles of mammals. their bodies inside crevices of coral, but the tail remains ex-
They possess layers of lamellar cells, but they lack the cor- posed and extends upward outside the coral. When light is
puscular end-organs that are characteristic in mammals. shown on the tail, the snake is disturbed, suggesting a
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behavioral response to the stimulation of the cutaneous Campbell, A. L., T. J. Bunning, M. O. Stone, D. Church, and M. S.
light receptors. Grace. 1999. Surface ultrastructure of pit organ, spectacle, and
non pit organ epidermis of infrared imaging boid snakes: A
Finally, I mention the unique pair of scaled appendages
scanning probe and scanning electron microscopy study.
that protrude from the rostral margins of the head of the Journal of Structural Biology 126:105–120.
aquatic Tentacled Snake (Erpeton tentaculatum) (fig. 7.14). Caprette, C. L., M. S. Y. Lee, R. Shine, A. Mokany, and J. F. Down-
These tentacles are very sensitive mechanoreceptors that hower. 2004. The origin of snakes (Serpentes) as seen through
respond to vibrational movements in water. They are eye anatomy. Biological Journal of the Linnean Society 81:
densely innervated and are used to detect the position of 469–482.
Catania, K. C., D. B. Leitch and D. Gauthier. 2010. Function of the
fish that comprise their prey. Strikes at prey (see chapter
appendages in tentacled snakes (Erpeton tentaculatus). Journal
2) can be guided by either visual or mechanical cues, but of Experimental Biology 213:359–367.
normally the position of fish is signaled by integration of Chiszar, D., C. Andren, G. Nilson, B. O’Connell, J. S. Mestas Jr., H.
both visual and mechanosensory cues that are integrated M. Smith, and C. W. Radcliffe. 1982. Strike-induced chemosen-
in the brain. Tentacled Snakes are completely aquatic and sory searching in Old World and New World pit vipers. Animal
Learning and Behavior 10:121–125.
feed almost exclusively on fish. The tentacle appendages
Christensen, C. B., J. Christensen-Dalsgaard, C. Brandt, and P. T.
are perhaps most useful when snakes are in turbid water Madsen. 2012. Hearing with an atympanic ear: Good vibration
or feeding at night when visual cues are less useful to and poor sound-pressure detection in the royal rython, Python
localize prey. regius. Journal of Experimental Biology 215:331–342.
De Cock Buning, T., S.-I. Terashima and R. C. Goris. 1981. Python
pit organs analyzed as warm receptors. Cellular and Molecular
Neurobiology 1:271–278.
Concluding Remarks De Haan, C. C. 2003. Sense-organ-like parietal pits found in Psam-
As with we humans, so it is with snakes: our sense organs mophiini (Serpentes, Colubridae). Comptes Rendus Biologies
enable us to perceive the world around us, and they deter- 326:287–293.
mine how we view it. The amazing thing is that all the Ebert, J., S. Müller, and G. Westhoff. 2007. Behavioural examina-
tion of the infrared sensitivity of ball pythons. Journal of Zool-
sensory input of stimuli—light, heat, sound, and so on—
ogy 272:340–347.
becomes transduced into the same form of signals that Fuchigami, N., J. Hazel, V. V. Gorbunov, M. Stone, M. Grace, and V.
move almost instantaneously (along nerve pathways) to V. Tsukruk. 2001. Biological thermal detection in infrared im-
our brain as action potentials, where they are interpreted. aging snakes. 1. Ultramicrostructure of pit receptor organs.
How a snake “views” its world might be quite different Biomacromolecules 2:757–764.
from how we humans view ours. Consider, for example, Goris, R. C., Y. Atobe, M. Nakano, K. Funakoshi, and K. Terada.
2007. Blood flow in snake infrared organs: response-induced
what it might be like to view the world around us as ther-
changes in individual vessels. Microcirculation 14:99–110.
mal images that are constructed in the brain from sig- Grace, M. S., W. M. Woodward, D. R. Church, and G. Calisch. 2001.
naling that originates in pit organs. On the other hand, Prey targeting by the infrared-imaging snake Python: Effects of
perhaps our perception of the world around us is not really experimental and congenital visual deprivation. Behavioural
that different from that of a snake. Think about this. Brain Research 119:23–31.
Hartline, P. H. 1971. Physiological basis for detection of sound and
vibration in snakes. Journal of Experimental Biology 54:349–371.
Hartline, P. H., and H. W. Campbell. 1969. Auditory and vibratory
Additional Reading responses in the midbrain of snakes. Science 163:1221–1223.
Amemiya, F., R. C. Goris, Y. Masuda, R. Kishida, Y. Atobe, N. Ishii, Hartline, P. H., and E. A. Newman. 1981. Integration of visual and
and T. Kusunoki. 1995. The surface architecture of snake infra- infrared information in bimodal neurons of the rattlesnake
red receptor organs. Biomedical Research (Tokyo) 16:411–421. optic tectum. Science 213:789–791.
Bakken, G. S., and A. R. Krochmal. 2007. The imaging properties Jackson, M. K., and G. S. Doetsch. 1977. Functional properties of
and sensitivity of the facial pits of pitvipers as determined by nerve fibers innervating cutaneous corpuscles within cephalic
optical and heat-transfer analysis. Journal of Experimental skin of the Texas rat snake. Experimental Neurology 56:63–77.
Biology 210:2801–2810. Jackson, M. K., and G. S. Doetsch. 1977. Response properties of
Berman, D. S., and P. Regal. 1967. The loss of the ophidian middle mechanosensitive skin nerve fibers innervating cehalic skin of
ear. Evolution 21:641–643. the Texas rat snake. Experimental Neurology 56:77–90.
Bulloch, T. H., and R. B. Cowles. 1952. Physiology of an infrared Kahmann, H. 1932. Sinnesphysiologische studien an reptilien: 1. Ex-
receptor: The facial pit of pit vipers. Science 115:541–543. perimentalle untersuchungen über das Jakobsonische organ der
Burghardt, G. M. 1970. Chemical perception in reptiles. In J. W. eideschen und schlangen. Zoologische Jahrbücher Abteilung für
Johnston Jr., D. G. Moulton, and A. Turk (eds.), Advances in allgemeine Zoologie ünd Physiologie der Tiere. Jena. 51:173–238.
Chemoreception, vol. 1, Communication by Chemical Signals. New Kardong, K. V., and H. Berkhoudt. 1999. Rattlesnake hunting be-
York: Appleton-Century-Crofts, pp. 241–308. havior: Correlations between plasticity of predatory perfor-
Burns, B. 1969. Oral sensory papillae in sea snakes. Copeia mance and neuroanatomy. Brain Behavior and Evolution
1969:617–619. 53:20–28.
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Kardong, K. V., and S. P. Mackessey. 1991. The strike behavior Schwenk, K. 1994. Why snakes have forked tongues. Science
of a congenitally blind rattlesnake. Journal of Herpetology 263:1573–1577.
25:208–211. Schwenk, K. 1995. Of tongues and noses: Chemoreception in liz-
Kishida, T., and T. Hikida. 2010. Degeneration patterns of olfac- ards and snakes. Trends in Ecology and Evolution 10:7–12.
tory receptor genes in sea snakes. Journal of Evolutionary Biol- Sivak, J. G. 1977. The role of the spectacle in the visual optics of the
ogy 23:302–310. snake eye. Vision Research 17:293–298.
Krochmal, A. R., and G. S. Bakken. 2003. Thermoregulation is the Walls, G. L. 1967. The Vertebrate Eye and Its Adaptive Radiation. New
pits: Use of thermal radiation for retreat site selection by rat- York: Hafner Publishing. Facsimile of 1942 edition.
tlesnakes. Journal of Experimental Biology 206:2539–2545. Westhoff, G., B. G. Fry, and H. Bleckmann. 2005. Sea snakes (Lape-
Krochmal, A. R., G. S. Bakken, and T. J. LaDuc. 2004. Heat in evo- mis curtus) are sensitive to low-amplitude water motions. Zool-
lution’s kitchen: Evolutionary perspectives on the functions ogy 108:195–200.
and origin of the facial pit of pitvipers (Viperidae: Crotalinae). Wever, E. G. 1978. The Reptile Ear. Princeton, NJ: Princeton Uni-
Journal of Experimental Biology 207:4231–4238. versity Press.
Liu, Y., L. Ding, J. Lei, E. Zhao, and Y. Tang. 2012. Eye size variation York, D. S., T. M. Silver, and A. A. Smith. 1998. Innervation of the
reflects habitat and daily activity patterns in colubrid snakes. supranasal sac of the puff adder. Anatomical Record 251:221–225.
Journal of Morphology 273:883–893. Young, B. A. 1990. Is there a direct link between the ophidian
Molenaar, G. J. 1992. Anatomy and physiology of infrared sensitivity tongue and Jacobson’s organ? Amphibia-Reptilia 11:263–276.
of snakes. In C. Gans and P. S. Ulinski (eds.), Biology of the Reptil- Young, B. A. 1993. Evaluating hypotheses for the transfer of stim-
ia, vol. 17. Chicago: University of Chicago Press, pp. 367–453. ulus particles to Jacobson’s organ in snakes. Brain, Behavior
Newman, E. A., and P. H. Hartline. 1982. The infrared “vision” of and Evolution 41:203–209.
snakes. Scientific American 246:98–107. Young, B. A. 2003. Snake bioacoustics: Toward a richer under-
Nishida, Y., S. Yoshie, and T. Fujita. 2000. Oral sensory papillae, standing of the behavioral ecology of snakes. Quarterly Review
chemo- and mechano-receptors, in the snake, Elaphe quadrivir- of Biology 78:303–325.
gata: A light and electron microscopic study. Archives of Histol- Young, B. A., and A. Aguiar. 2002. Response of western diamond-
ogy and Cytology 63:55–70. back rattlesnakes Crotalus atrox to airborne sounds. Journal of
Parker, M. R., B. A. Young, and K. V. Kardong. 2008. The forked Experimental Biology 205: 3087–3092.
tongue and edge detection in snakes (Crotalus oreganus): Young, B. A., J. Marvin, and K. Marosi. 2000. The potential signif-
An experimental test. Journal of Comparative Psychology icance of ground-borne vibration to predator-prey relation-
122:35–40. ships in snakes. Hamadryad 25:164–174.
Povel, D., and J. van der Kooij. 1997. Scale sensillae of the file snake Young, B. A., and M. Morain. 2002. The use of ground-borne vibra-
(Serpentes: Acrochordidae) and some other aquatic and bur- tions for prey localization in the Saharan sand vipers (Ceras-
rowing snakes. Netherlands Journal of Zoology 47:443–456. tes). Journal of Experimental Biology 205:661–665.
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S O UND PRODU C T I ON
A cornered gopher or bull snake is the picture of a vindictive and dangerous

creature. It coils and vibrates its tail, and lunges repeatedly at any intruder.
It hisses violently, having a peculiar construction of the epiglottis that
accentuates the sound. This frightening pose will quite convince an observer
8
that so ferocious an animal had best be let alone, which is exactly its purpose.
—Lawrence M. Klauber, Rattlesnakes (1956), vol. 1, p. 22
Most people probably consider snakes to be generally silent as the vibrations of air sacs in fishes. In snakes, vibrations
creatures, making little noise during chance encounters, or are conducted through the tissues of the head (including
when being seen at a zoo or filmed for a television docu- the columella) to stimulate the inner ear, as described in
mentary. Limited knowledge also suggests to most people chapter 7.
that snakes cannot hear, or at least cannot hear well. This At lower frequencies, even for humans, there is some
view is strengthened by considering that snakes do not overlap (and fuzzy distinction) between what we might call
have external ears, and many older writings have stated or a “vibration sense” and hearing. This may be especially true
implied that snakes cannot hear, although they are sensi- for snakes, given they respond to vibrational stimuli largely
tive to ground-borne vibrations. Although snakes may not within the range of several dozens of Hz to about 600 Hz,
hear well, those that hiss or rattle can make loud enough with little or no ability to detect stimuli in excess of about
sounds to alarm persons who might encounter them. 1,000 Hz. Both the inner ear and the tissues of the body
surrounding it are capable of responding to both ground-
borne vibrations and airborne sounds (see chapter 7). So we
Sound in the Environment know that snakes can sense at least many of the noises that
What we call “sound” refers to fluid-borne vibrations (usu- they themselves produce. How they use this information in
ally in air) that impinge on a sensory structure (the ear) relation to various behaviors is a subject that is in need of
where the energy of the vibrations is transduced into nerve much further study.
signals (see chapter 7). The nerve signals travel to the cen-
tral nervous system, where they are interpreted by the ap-
propriate (auditory) region of the brain. If the vibrational Externally Produced Sounds
stimuli fall within the frequency range that is perceived by Many snakes use the external body surfaces to produce
human ears and brain, the stimuli are called sound. The sound, and various sounds are also made unintentionally
human ear can detect airborne vibrations in the range of by moving snakes in many circumstances. Thus, the “swish-
frequencies from roughly 20 to 20,000 Hz (Hertz, = cycles ing” sounds made by racers or other large snakes crawl-
per second). ing through dry grasses, the “humming” sounds of snakes
A similar phenomenon would be expected to occur in moving over damp sand (as on a beach), and the “scraping”
snakes, except that the animals lack an external ear and ear sounds of larger snakes that crawl among or over rocks all
canal. Therefore, one might suppose that snakes cannot provide detectable auditory stimuli that alert other animals
hear at all, but this is not true. There are many animals that to a snake’s presence and potentially inform the snake
lack externally obvious ears, yet they can “hear” vibrational about its movements. Other sounds are made in specific
stimuli that are transduced through the tissues of the contexts related to defense, sometimes using specialized
head, internal bony structures, or other mechanisms such features of a snake’s morphology.
| 181
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Rubbing of Scales and the mass and nature of the tail. A vibrating tail of, say,
The scales on the body of snakes are fortified at their outer a Bullsnake or Gopher Snake (Pituophis catenifer) will pro-
surfaces by numerous layers of keratin (see chapter 5). This duce a startling sound when it shakes among dry leaves, but
material is derived from living cells and consists of dead the sound would be very different and muted if the tail was
interlocking elements of protein. Keeled scales have the shaken upon sand or in damp grass. The ability of the tail to
outermost layers elevated into ridges or other protuber- produce sound also might depend on projections or ap-
ances on the scale surfaces, usually along the midlines pendages that are present at the tip of the tail in some spe-
(figs. 5.8–5.10). These scales can create sounds when they cies (rattlesnakes). In another context, I have observed that
are rubbed against objects or against each other. shaking the tail may serve to disperse musk in presumably
In certain snakes, the scales are deliberately rubbed to- chemical defensive responses (e.g., Cottonmouths, Agkis-
gether by precisely orchestrated body movements to produce trodon piscivorus).
sounds that are assumed to be defensive. The behavior is no- The most obvious example of enhanced acoustic signals
table in snakes of the genera Echis (Saw-scaled Vipers), Dasy- in tail shaking is that associated with the rattles of rattle-
peltis (egg-eating snakes), and Aspis (some adders). The snakes (genera Crotalus and Sistrurus). The rattle is similar
rubbing sound is especially pronounced in Saw-scaled Vi- in all species with respect to its fundamental structure,
pers, hence the common name. The lateral body scales are except for size. It can be considered an epidermal ap-
prominently keeled (fig. 8.1), and they rub against each other pendage, having evolved from proliferated horny tissue
when segments of the body trunk make contact and slide in that is derived from the outermost stratum corneum at the
opposite directions while the snake is in a loose, but writhing, tip of the tail (see chapter 5). The rattle consists of inter-
coil. The mutual abrasion of opposite-facing scales produces locking segments of keratin, each fitting loosely within
a “raspy” sound, which has not been analyzed in detail. another, and a new segment is added at each cycle of ec-
Two other observations are noteworthy. First, the lateral dysis (fig. 8.2). A prerattle segment on the tip of the tail,
location of the relatively more prominent scale ridges called a prebutton, is present at birth but is lost at the first
(where the rubbing contact occurs) suggests these are a spe- ecdysis. The first permanent and distal segment on the
cific adaptation that has evolved in relation to the scale- rattle is called the button (fig. 8.3). Only after the second
rubbing behavior. Second, the rubbing of scales occurs only ecdysis does the rattle consist of two interlocking seg-
in circumstances that suggest that the function of this be- ments that can make sound. Each added segment increases
havior is defensive. in size as the snake grows larger, becoming more uniform
as growth slows in adulthood (fig. 8.3). The rattle ap-
Tail Vibration and Rattling pendage, when shaken vigorously by its owner, produces
Many snakes, both venomous and nonvenomous, vibrate the buzzing or hissing-like noise (similar to escaping steam
or shake their tails when they are disturbed or threatened. or pressurized air) that results from the interlocking seg-
Such tail vibrations produce audible sounds depending on ments of the rattle striking against each other when the
the substrate that contacts the tail, the speed of shaking, tail is shaken vigorously by tail muscles that are special-
ized for “rattling.” The sound of such a rattle is weak when
there are only a few segments, but increases with the addi-
tion of more segments as the snake grows in size.
People generally find rattlesnakes to be “noisy” animals,
but many folks do not appreciate the elegant qualities of
the rattle and the tail that shakes it. The rattling of a rattle-
snake rattle is one of the faster movements made by verte-
brates, and the so-called shaker muscles in the tails of
rattlesnakes are among the faster muscles that are known
in nature. These muscles can sustain contraction frequencies
of 20–100 Hz for as long as several hours! The contraction
frequency, and hence the oscillation frequency of the rattle,
is dependent on temperature. In adult Western Diamond-
backed Rattlesnakes, Crotalus atrox, the contraction
frequency is 15 Hz at a temperature of 10°C, whereas the
Figure 8.1. A Saw-scaled Viper (Echis carinatus) in south India,
illustrating the highly keeled condition of lateral body scales (arrow) contraction frequency increases to 85 Hz at 35°C. The shaker
that are rubbed together to produce a defensive rasping sound. muscles have large deposits of glycogen and are quite
Photograph by Indraneil Das. resistant to fatigue. Numerous mitochondria and blood
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capillaries are present in the muscle, which has compara- “typical” rattling sound can be described as broad-band
tively small contractile elements and much noncontractile noise spanning from roughly 2,500 to 19,000 Hz with a
tissue. Consequently, the muscle is weak, albeit very effec- dominant frequency near 9,000 Hz. Note that this range
tive in moving the lightweight rattle segments very rapidly does not overlap with that of rattlesnake hearing (see chap-
to produce the characteristic rattling sounds. ter 7). There is no frequency or temporal modulation of the
There are three large shaker muscles on each side of the sound at constant temperature and uninterrupted rat-
tail in C. atrox. (These correspond to the M. longissimus tling. In some rattlesnakes not especially prone to rattle
dorsi, M. iliocostalis, and M. supracostalis lateralis in the body vigorously, the tail may twitch periodically or rattle for brief
of the snake.) Each muscle appears to be a single motor unit periods with resting pauses in between.
with fibers that contract synchronously. The individual con- As temperature increases the frequency of rattling, the
tractions (called twitches) are “all-or-none” and involve all frequency of muscle twitches that power the rattling move-
of the contractile elements. Brad Moon at the University of ments increase and the movements of the rattle segments
Louisiana, Lafayette, has shown that the muscle forces ex- require higher forces and accelerations. Yet the energy cost
erted on the rattle segments produce two motions: lateral per twitch of rattling has been found to be independent of
displacement and torsion (fig. 8.4). The twisting motion en- the twitch frequency. Recordings of the joint motions (be-
hances sound output, and particularly helps maintain tween segments) and associated forces by Brad Moon,
sound output in long rattles, which have heavily dampened Kevin Conley, and Stan Lindstedt indicate that the in-
lateral displacements. creasing force of a twitch is offset by a shorter duration of
Recent investigations by Bruce Young, Ilonna Brown, each twitch, which keeps the energetic cost per twitch cycle
Patrick Cook, and their colleagues have modeled the rattle nearly constant over a wide range of temperatures and
as a multidimensional oscillator, and the acoustic profile of twitch frequencies. Also, as the twitch frequency increases,
the rattling sound can be predicted by measuring the size of the lateral displacement of the rattle decreases. Therefore,
the rattle or even just the basal segment of the rattle. The the increasing forces that are acting on the rattle segments
rattle can be considered a kinetic chain, producing sound as are offset by reductions in the lateral displacement of the
interlocking adjacent segments of the rattle are shaken rattle, thereby keeping the mechanical work and force re-
against each other, generally back and forth from side to quired to shake the rattle low. At higher frequencies of rat-
side (the “oscillator”) (fig. 8.4). Lateral displacement of the tling (tail shaking), the decrease in lateral displacement of
rattle segments during rattling oscillations is greatest at the rattle is a major factor in keeping the work and energy
the tip and diminishes toward the base. In snakes having a demand from increasing as much as it would if lateral dis-
large number of rattle segments, the segments near the placement remained constant as the frequency increased.
base of the tail show little variation in size (fig. 8.3). This Fundamentally, the cost of any muscle contraction is pro-
consistency in size produces a corresponding consistency in portional to the force and duration of the contraction. In
the frequency of sound that is produced during rattling. A the rattlesnake shaker muscles, there is a trade-off between
Figure 8.2. Drawing of a rattlesnake rattle illustrating the interlocking of individual segments in the central part of the rattle. Drawing by
Amanda Ropp.
Sound Production | 183
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Figure 8.4. The rattle of a Western Diamond-backed Rattlesnake
(Crotalus atrox) illustrating the forces that are involved in movements
of the rattle (arrows) during shaking by the shaker muscles.
Photograph by the author.
oxygen from blood flowing through the shaker muscles, and

high rates of lactate removal by the circulation all contribute
to the avoidance of fatiguing muscle during rattling at high
frequencies. The unusually high glycolytic flux of lactate, and
the supply of ATP related to it, help to meet a substantial frac-
tion of the ATP energy demand of continuous shaker muscle
Figure 8.3. The upper photo illustrates the button at the tip of the contractions. Lactate results from the production of ATP en-
tail of a baby Eastern Diamondback Rattlesnake (Crotalus
ergy in metabolic pathways (glycolysis inside muscle) that do
adamanteus). This will become the terminal segment of the rattle as
the snake grows and adds rattle segments. The lower photo shows not require oxygen. With respect to the energetics of the rat-
the rattle of an adult Western Diamond-backed Rattlesnake (Crotalus tlesnake shaker muscles, their mechanical efficiency is com-
atrox). The terminal button has been lost to wear in this individual. parable to other muscles that operate at very high frequencies,
Both photographs are of living snakes and taken by the author. for example the flight muscles of insects.
According to the early thoughts of Lawrence Klauber,
published in 1956, “The rattle is used as a warning signal;
the force and duration of twitches with changing frequency, upon this, experience permits no argument: if it has alter-
which keeps the energetic cost per twitch constant. Thus, as native purposes . . . they are not matters of daily observa-
temperature increases, higher muscle forces accelerate the tion.” Although other hypotheses and theories have been
rattle faster, but for shorter periods and over smaller lateral proposed by various persons, it seems to be generally ac-
excursions. The diminished lateral displacement allows cepted that certainly the dominant, if not sole use of the
rattle motion and sound production to be sustained for very rattle, is in defense against potentially dangerous animals,
little work. such as predators or large animals that could trample a
Prolonged rattling of the shaker muscle necessitates con- snake. Some imagined uses of the rattlesnake rattle are
siderable blood flow, which supplies oxygen and removes amusing, including ideas that rattlesnakes always warn an
waste metabolites associated with the muscle activity (espe- intruder by rattling in advance of a strike. Some folks living
cially lactate). William Kemper, Stan Lindstedt, and their col- during the 1700s and 1800s believed that a snake always
leagues demonstrated that the sustained rate of blood flow rattles three times before striking! Some Brazilian peoples
through the rattlesnake shaker muscles (> 450 ml · min−1 · 100 believe that venomous snakes, including rattlesnakes,
g −1 muscle) is among the higher levels reported and exceeds decoy small birds and mammals by imitating their calls.
that of the skeletal and heart muscles in exercising racehorses! However, rattlesnakes rattle only in defensive contexts,
During rattling, the increases in blood flow, extraction of and not always before the snake strikes.
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The complex structure of the rattlesnake rattle is re- volume was maximized by the prolonged inhalation, and
markably similar across all species, suggesting to most her- the large storage of air permitted a prolonged hiss and
petologists that this structure evolved only once during thereby exaggerated the effect of instilling caution (and, at
rattlesnake evolution. Based on the dating of fossil rattle- best, fear) on the part of any would-be predator.
snakes, rattles have been in existence for at least 5 million
years. How rattles evolved is still unknown and basically a Hissing
matter of speculation and debate. Hissing is an important defensive action in snakes, which
otherwise have no “voice” to startle or alarm an approach-
ing predator. The most important function of the hiss is
Internally Produced Sounds probably to alarm an approaching animal and thereby ei-
Hissing is the most common means by which snakes pro- ther scare it away or, at least, instill caution on the part of
duce sounds. Surprisingly, however, there is another novel an advancing predator and slow its advance toward the
means by which sounds are produced, involving the oppo- snake. This delay gives the snake more time either to escape
site end of the animal. In all cases, the production of sound or to optimize the position from which it can launch a strike
involves compressive forces that act to dispel air from inter- or other defensive action, if necessary.
nal storage sites. The hiss of a snake is clearly audible to humans. The sounds
vary from low, guttural noises to sharper sounds resembling
Hissing and Related Sounds escaping steam or noisy gusts of air escaping through a tube.
I recall as a young boy the very first rattlesnake that I cap- However, the hissing sounds of snakes are thought to have a
tured, together with a person who was my best friend at the very low potential for encoding information and can be gener-
time. This dramatic occasion occurred during December in ally regarded as a simple defensive warning. There is a remark-
Southern California, at a site consisting of rocky caverns able acoustic similarity among hisses from many species of
and outcroppings on the Irvine Ranch (today very near the snakes, and the simplicity of the sounds has been said to ap-
University of California at Irvine campus). We were ex- proach the levels determined for “white noise.” Most hisses
ploring the region, as we often did for pure outdoor fun. are essentially high intensity, unmodulated, dynamic flows
Insofar as the seasonal weather was quite cool we were not of ventilatory air. These are characterized by a generally
even thinking about collecting snakes. However, we discov- simple acoustic structure with little frequency or amplitude
ered a very large Red Diamond Rattlesnake (Crotalus ruber) modulation and little or no temporal patterning.
visible within a rock crevice, so we pulled it out with a stick The mechanism of the hiss in most snakes involves sev-
and set it in the open where we could check it out—with eral elements. First, the energy that “drives” the production
what I must say was great excitement! The snake slowly of sound is attributable to the movement of air within the
drew itself into a coil but did not rattle. I do not recall the lung and through the opening of the trachea or larynx. The
temperature, but I suspect the shaker muscles of the tail release of air during exhalation that is associated with a
might have been too cold to rattle effectively, so the defen- hiss is due either to passive recoil of the inflated lung and
sive behavior was different from what we had anticipated. stretched body wall, or to active compression of the body
The snake slowly, over many seconds, inflated itself to a and lung by surrounding muscles, or both. Second, the pro-
girth that appeared more than twice its normal size. Then, duction of sound as a result of escaping air involves an in-
just as slowly, it gradually released the air during one, long, teraction involving the dynamic flow of the air, the length
drawn-out, extraordinary hiss. The defensive effect was of the tracheal airway, and the aperture (glottis) of the tra-
quite dramatic and twofold in purpose. First, the snake chea (fig. 8.5). The frequency of the hissing sound depends
appeared larger, and for two boys messing with their first on the length and diameter relationships of the trachea
venomous snake, the perception of size had a chilling ef- and/or larynx. The trachea is essentially a long tube with
fect. Second, the sound of the hiss clearly impressed on us one end that can be opened or closed by muscular actions of
the danger that was before us in the form of this large the glottis. Exhalation of air from the trachea through the
snake. To conclude the story, we captured the rattlesnake, glottis induces vibration of air within the trachea. The
took it home, and held it for a week in captivity, then re- frequency of such vibration, and thus the sound that is pro-
leased it back to the wild on the following weekend. duced, is directly related to the length of the tube. Of
This story helps to emphasize an important concept. As course, the trachea is not a solid tube (of cartilage) but con-
discussed in chapter 6, the elongated lung of snakes be- tains a flexible membrane for part of its circumference (figs.
stows numerous functions in addition to its primary job of 6.13, 6.19). Thus, vibrations of the tracheal membrane can
exchanging respiratory gases, oxygen and carbon dioxide. also influence the sound that is produced. Vibrations of the
In the case of the Red Diamond Rattlesnake, the lung tracheal membrane are dependent on the vibrations of the
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exchange of air between the trachea, lung, and environ-
ment is often accompanied by hissing sounds.
The noise of a hiss is a broad spectrum of sound, span-
ning frequencies from roughly 3,000 to 13,000 Hz. There is
a dominant frequency at around 7,500 Hz, with little varia-
tion related to species or body size. While some herpetolo-
gists have suggested that snakes have the capability to
modulate the amplitude and temporal properties of the
hiss (changes through time), there is no convincing evi-
dence for such modulation. Snakes have two muscles that
can act to alter the diameter of the glottal opening, which
could change the nature of the hiss by altering the velocity
of the air flow. Such active modulation of the glottal opening
could possibly be employed to modulate the hiss, but no
one has yet confirmed that this actually occurs in any of the
Figure 8.5. Lower mouth of a Neotropical Bird Snake (also called species that have been studied. Moreover, studies of artifi-
Puffing Snake) (Pseustes poecilonotus) showing the open glottis with
cial hissing in Puff Adders (Bitis arietans) by Bruce Young
tongue sheath beneath. Photograph by Dan Dourson.
suggest it would be nearly impossible for the snake to pro-
duce an acoustically complex hiss, and the trachea of this
air within the trachea, and the tensioning of the tracheal species imparts no distinct acoustic signature to the ex-
membrane. Finally, hissing sounds can be produced during haled airstream. The larynx is simply not able to modulate
both inhalation and exhalation of pulmonary air. frequency of the exhaled airstream even if the glottis is
Dr. Bruce Young, currently at the University of Massachu- forcibly occluded against the flow of air by electrical stimu-
setts, Lowell, has focused much of his research program lation of the Constrictor laryngis muscle.
on evaluating the sound production and sound-producing The hiss of the colubrid snakes Pituophis melanoleucus
mechanisms of snakes. He has suggested a good analogy for and P. catenifer is especially noteworthy. These species are
understanding the hissing noises of snakes, and this is the called Pine, Bull, or Gopher Snake depending on the subspe-
musical instrument that we call a flute. Flutes are classified cies and region of occurrence. The defensive hisses of these
according to their length, and the longer the flute the lower snakes can be very loud and have what has been described
the frequency it is able to produce. For a given flute, the as a “raspy” texture. Unlike most other species of snakes,
finger holes (allowing escape of exhaled air by the player) the frequency range of the hiss of P. melanoleucus spans the
farthest from the air source produce the sounds of lowest range from 500 to 9,500 Hz.
frequency, whereas those adjacent to the air source produce The larynx of Pituophis is unusual in having two mor-
the sounds having highest frequency. These features are phological specializations: (1) a dorsal extension of the cri-
analogous to the length of the trachea and the relative posi- coid cartilage that is sometimes referred to as an “epiglottal
tion of the opening (see also the section on “growling” below). keel”; and (2) a flexible, horizontal shelf of tissue called the
Ventilatory air flow in snakes is produced by localized “laryngeal septum” that divides the anterior portion of the
movements of the ribs, and such actions have been referred larynx. The laryngeal septum can be regarded as the first
to by Herb Rosenberg as the “costal pump.” In some snakes described “vocal cord” of a snake. It is a uniquely unpaired
the defensive hisses exhibit a quadriphasic temporal pat- structure compared with the paired vocal cords of other
tern characterized by (1) an initial exhalatory hiss, followed vertebrates, and it has not been found in species of snakes
by (2) a brief transitional pause; (3) an inhalatory hiss; and other than P. melanoleucus. Bruce Young and his coworkers
then (4) a second pause or period of rest. The costal pump is have studied sound production in this species and were
responsible for generating this pattern, and the role of the able to demonstrate that the laryngeal septum vibrates
pulmonary tract is generally passive. Abduction of the ribs and contributes harmonic elements in the defensive hisses
(movement away from the central axis) produces negative of Pituophis, whereas the epiglottal keel has little influence
pressure in the lungs and powers inhalation, sometimes re- on the quality of these hissing sounds. A harmonic is an
sulting in an inhalation hiss. Adduction of the ribs (move- overtone—present in the calls of some frogs, bats, and
ment toward the central axis) does the opposite, increasing other animals—whose frequency is a whole-number mul-
pressure within the lung and powering exhalation with as- tiple of a fundamental frequency. Vibration of the laryngeal
sociated hissing. Expansion of the body (on inhalation) is a septum of Pituophis produces harmonics that have a funda-
common feature of defensive displays of snakes, and the mental frequency of about 500 Hz.
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Several lineages of snakes have a means of expanding species in which they occur. Growling is best known (and
the trachea, which could clearly alter the acoustic nature of evaluated) in the King Cobra (Ophiophagus hannah), and
the hiss. Three means of expansion are (1) possession of a has also been recorded from a colubrid snake, the Red-
tracheal lung (see chapter 6), (2) “pleating” of the tracheal tailed Rat Snake (Gonyosoma oxycephalum). In the King Co-
membrane, and (3) tracheal diverticula, which are discussed bra, the growl involves frequencies below 5,000 Hz (and
below in relation to growling. The width of the tracheal often below 2,500 Hz), with a dominant frequency of ap-
membrane is taken up by large pleats in the membrane proximately 600 Hz. There is evidence for frequency modu-
when it is not under tension. Except for the role of diver- lation in the growl of the King Cobra, with higher intensity
ticula discussed below, the acoustical influence of tracheal sounds at the beginning and ending of the emitted noise.
expansion has not been well studied or documented. The defensive growl of the Red-tailed Rat Snake consists of
frequencies below 2,000 Hz, and a dominant frequency of
Bellowing about 625 Hz. The growling sounds of both species are dis-
During defensive hissing in Pituophis melanoleucus the epi- tinct from the hisses of snakes.
glottal keel functions merely to divide the flow of air and Modeling of the tracheal diverticula (air sacs; see fig.
evidently does not vibrate to contribute a pulsatile quality to 6.19) suggests that they act as resonating chambers,
the sound. However, during the beginning of a series of hiss- which means they essentially dampen or filter out some
ing sounds produced by P. melanoleucus there is a burst of frequencies while enhancing others. The size and shape
loud (high amplitude), broad-frequency sound that Bruce of the resonating chambers determine the frequencies
Young and his collaborators have called a “bellow.” The that are generated and thus the power spectrum of the
bellow has been distinguished from a hiss in having simple produced sound. The larger the diverticula, the lower the
modulation of both amplitude and frequency, evidently due dominant frequency of the growl. Both growls and hisses
to a brief period of imbalance between the air flow and ten- can be intimidating, depending especially on the size and
sion in the laryngeal septum. The brief duration of such bel- behavior of the snake!
lowing is less than 0.2 of a second. This represents the time
lag between dilation of the glottis to emit air flow and an Nasal Hissing
adjustment of tension in the laryngeal septum by means of Observers have long had the impression that many snakes,
an associated smooth muscle. The sound of a bellow includes especially vipers, can hiss through the nasal passages. Much
both temporal variation and harmonic elements that result of the impression comes from the observation of snakes
from vibrations of the laryngeal septum. hissing while the mouth is shut. In a very early experiment,
The bellow is unique to Pituophis and has not been de- Frank Wall in 1921 observed that the hiss of Russell’s Viper
scribed in any other species of snake. The presence of a (Daboia russelii) sounded different after the nares were par-
“vocal cord” (laryngeal septum) and the complex emission tially occluded.
of both a bellow and a hiss in these snakes appears to ex- It is now believed that, in many snakes, the exhalant
plain the anecdotal reports of the unusual defensive sounds airstream passes through the internal nares. A number of
that they emit. I once encountered a Gopher Snake in Cali- species are regarded as obligate nasal hissers, and these
fornia that was, in my experience, uniquely bad-tempered. include Eastern Hog-nosed Snakes (Heterodon platyrhi-
It struck repeatedly, falling forward with violent mo- nos), the Puff Adders (Bitis arietans), and Russell’s Vipers
mentum during each strike. Also, with each strike I remem- (Daboia russelii). The air flow associated with sound pro-
ber a very loud raspy hiss, probably with elements of duction passes through the nasal passageways, which are
bellowing that I would not have known about at the time. essentially static and do not actively modulate the sound.
Together, the striking and hissing were most dramatic, and During typical defensive behaviors of the rattlesnakes Cro-
they created as good of a show as the defensive displays of talus atrox (Western Diamond-backed Rattlesnake) and
many rattlesnakes or cobras. C. adamanteus (Eastern Diamondback Rattlesnake), air
flow occurs only through the nasal passageways. Hissing is
Growling produced during inhalation (inspiration), and it is possible
Other sounds emitted from the tracheal airways of snakes that these hisses are acoustically modified during passage
have been described by Bruce Young as “growls.” The growl through the nasal passageway. In other heavy-bodied
of a snake is the noise that is emitted when the exhalant viperid snakes, the external nares are variously modified
airstream of the trachea passes over openings in the tra- with complex openings (fig. 8.6). These are likely to func-
cheal membrane that lead to adjoining air sacs, or tracheal tion with respect to very loud and prominent hissing
diverticula (see chapter 6). These structures are not found in noises that are made by these snakes during exhalation
all snakes, but they potentially enable growling in those (expiration) of air.
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secretive habits, and the phenomenon is
sometimes associated with other defen-
sive behaviors. Therefore, Bruce Young
and others have concluded that this
form of sound production evolved as a
defensive behavior. As such, it is likely
this mode of sound production occurs in
other species that have poorly known
natural histories.
Closing Comments
Snakes clearly generate some very inter-
esting sounds, which are used largely in
defense. Several considerations are impor-
tant. First, there are many snake species
Figure 8.6. Head of a Gaboon Adder (Bitis gabonica) illustrating the complex external
naris. The inset is a higher magnification of the naris, showing there are two levels of around the world for which very little is
circumferential ridges overlying the deep internal opening to the nasal passageway. This known concerning their natural history,
snake has the ability to hiss very loudly, and the external opening of the naris possibly behavior, and ecology. Further studies of a
acts to produce the loud sound that is heard during hissing. Photograph by the author. broader range of species might yet reveal
other sounds or uses of sound in addition
to the ones described here. Second, al-
Cloacal Popping though the defensive use of sounds seems
Imagine a snake is making a sound like a popping noise, but to be a reasonable conclusion in many contexts that have
the sound is not coming from the head end. There are var- been widely observed or studied, other uses of sound are
ious anecdotal claims in literature that snakes can produce possible, including communication with other snakes. With
sounds using the cloaca. Such a phenomenon has been these two thoughts in mind, some additional thoughts arise.
reported in the genera Ficimia, Gyalopion (hook-nosed
snakes), Micruroides, and Micrurus (coral snakes). Snakes 1. A long-considered theory for the evolutionary origin
can produce the popping sounds both during, and indepen- of the rattle of rattlesnakes holds that the structure
dent of, cloacal evacuation. The sounds result from a rapid evolved as a warning device for numerous grazing
expulsion of air from the cloacal vent, driven primarily by
animals that might not otherwise avoid stepping on a
cloacal musculature (principally the M. Sphincter cloacae).
snake. If this were true, why did rattles or similar
The “cloacal pops” recorded from snakes consist of low-
structures not evolve in other snake lineages that live
amplitude sounds (around 50–70 dB) with a limited fre-
on the extensive plains of Africa or Australia?
quency range from about 350 to 15,000 Hz, and sometimes
Moreover, if the rattle evolved as an acoustic warning
harmonics. The sounds are brief (about 0.2 sec) and exhibit
device, what was the function of intermediate stages?
a distinct temporal pattern. There is some acoustic varia-
tion of cloacal pops both within and between species. The Gordon Schuett and colleagues have suggested the
relative size of the cloaca and the associated musculature possibility that an enlarged cap at the tip of the tail
influence both the amplitude and frequency of the popping could enhance caudal luring (of potential prey) and
sounds that are emitted by an individual snake. then subsequently evolved into a rattle. However,
Controlled attempts to elicit cloacal pops from the other herpetologists dispute this notion and point
Eastern Coral Snake (Micrurus fulvius) by means of visual out there is no evidence to support the idea. The
and tactile stimulation are generally unsuccessful, unless rattle is a complex structure and therefore unlikely to
the head is restrained. However, in the Western Hook- have arisen de novo. So what was the function of an
nose Snake (Gyalopion canum) cloacal popping can be elic- epidermal appendage that led to the eventual complex
ited by light tactile stimulation and is usually associated rattle at the tip of the tail in this clade of snakes? It is
with thrashing movements. In the Western Coral Snake of interest to note that Australian death adders,
(Micruroides euryxanthus) cloacal popping occurs in con- Acanthophis spp., have elaborate protrusions of scales
junction with elevation and curling of the tail. Cloacal pop- at the tip of the tail that suggests to the eye a possible
ping is characteristic of snakes that have fossorial or precursor to a rattle (fig. 8.7). What is the function of
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Figure 8.8. Photograph of the skin of a newly discovered sea snake
from Australia (Hydrophis donaldi). This species was found recently in
estuarine habitats in the Gulf of Carpentaria where it might encounter
murky or turbid waters. The skin of this new species is strongly
spinous, and each scale bears a prominent keel or sharp tubercle that
is likely to be sensory. Photograph by Kanishka Ukuwela.
Figure 8.7. The tail of an adult Common Death Adder (Acanthophis
antarcticus). The tail terminates with an epidermal spine, and there
are spinous epidermal appendages arrayed for a short distance along
the distal end of the tail (arrow). Photograph by the author. conjunction with other stories related to the research
he was conducting at the den site. One problem with
this idea is that the sounds produced by rattlesnake
this appendage, and what additional steps involving rattles do not overlap the hearing range of the snakes.
genetic mutations are required for natural selection However, it might be that visual cues are involved with
to produce a full rattle? Ximena Nelson and colleagues what Fred observed, or that many snakes rattling
have demonstrated that the motions involved in simultaneously might create vibrational stimuli that
caudal luring in Common Death Adders (Acanthophis could be detected by the sensory systems of the snakes
antarcticus) mimic the motion characteristics of (cutaneous receptors in addition to the inner ear).
invertebrates, and the snakes use this deceptive 3. Fully aquatic snakes such as sea snakes live in aquatic
signal to attract agamid lizards. Perhaps the epidermal environments where vibrational information is of
structures on the tail of death adders also mimic much value, and their behaviors as well as structure of
invertebrates (e.g., legs of crickets), reinforcing the their skin suggest they are very sensitive to mechanical
possibility that tail structures used in mimicry might stimuli (fig. 8.8; see also 7.14). We know almost
precede evolution of the rattle as suggested by nothing about the hearing of sea snakes (or other
Schuett and his colleagues. These and many other aquatic species) and whether they live in an acoustic
intriguing questions relate to the evolution and uses world that is much richer and more useful to these
of the wonderful acoustic appendages that decorate animals than most persons might presently suppose.
the tails of American rattlesnakes. 4. How do sounds, as well as vibrations, affect burrowing
2. The late Professor Fred White once told me he was species that live subterranean lives, and do some of
convinced that rattlesnakes used their rattle for in- these species produce sounds that might communicate
traspecific communication. This was said following his with other conspecific individuals? Are there sounds
return from a visit to a communal den of Prairie that are produced by snakes, either underground or in
Rattlesnakes in the Midwestern United States (located, the sea, which we have not yet noticed or recorded?
I believe, in Colorado). At the time, he and a colleague
were embarking on a study of the thermal relationships As in other areas of snake biology, the production and
and energetic consequence of mass denning among uses of sounds by these animals are in need of much further
these snakes during the winter. I do not know Fred’s study. It is also true that there is a paucity of scientists who
explanation for this particular remark, and he never to have both the interest and training in the relevant areas of
my knowledge published on the idea. But I do remember physics to properly investigate the open questions. Hope-
how convinced he appeared when he mentioned this in fully, these circumstances will be remedied in the future,
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and we shall discover many more acoustic secrets that exist Rosenberg, H. I. 1973. Functional anatomy of pulmonary ventila-
in the world of snakes. tion in the garter snake, Thamnophis elegans. Journal of Mor-
phology 140:171–184.
Schaeffer, P. J., K. E. Conley, and S. Lindstedt. 1996. Structural cor-
Additional Reading relates of speed and endurance in skeletal muscle: The rattle-
Conley, K. E., and S. L. Lindstedt. 1996. Minimal cost per twitch in snake tailshaker muscle. Journal of Experimental Biology
rattlesnake shaker muscle. Nature (London) 383:71–72. 199:351–358.
Cook, P. M., M. P. Rowe, and R. W. Van Devender. 1994. Allometric Schuett, G. W., D. L. Clark, and F. Kraus. 1984. Feeding mimicry in
scaling and interspecific differences in the rattling sounds of the rattlesnake, Sistrurus catenatus, with comments on the
rattlesnakes. Herpetologica 50:358–368. evolution of the rattle. Animal Behaviour 32:625–626.
Fenton, M. B., and L. E. Licht. 1990. Why rattle snake? Journal of Young, B. A. 1991. Morphological basis of “growling” in the King
Herpetology 24:274–279. Cobra, Ophiophagus hannah. Journal of Experimental Zoology
Gans, C., and P. F. A. Maderson. 1973. Sound producing mecha- 260:275–287.
nisms in recent reptiles: Review and comment. American Zoolo- Young, B. A. 1992. Tracheal diverticula in snakes: Possible
gist 13:1195–1203. functions and evolution. Journal of Zoology (London) 227:
Kemper, W. F., S. L. Lindstedt, L. K. Hartzler, J. W. Hicks, and K. E. 567–583.
Conley. 2001. Shaking up glycolysis: Sustained, high lactate Young, B. A. 2003. Snake bioacoustics: Toward a richer under-
flux during aerobic rattling. Proceedings of the National Academy standing of the behavioral ecology of snakes. Quarterly Review
of Sciences (USA) 98:723–728. of Biology 78:303–325.
Klauber, L. M. 1997. Rattlesnakes: Their Habits, Life Histories, and Young, B. A., and I. P. Brown. 1993. On the acoustic profile of the
Influence on Mankind. 2nd edition. 2 vols. Berkeley: University rattlesnake rattle. Amphibia-Reptilia 14:373–380.
of California Press. Young, B. A., and I. P. Brown. 1995. The physical basis of the rat-
Martin, J. H., and R. M. Bagby. 1973. Properties of rattlesnake tling sound in the rattlesnake, Crotalus viridis oreganus. Journal
shaker muscle. Journal of Experimental Zoology 185:293–300. of Herpetology 29:80–85.
Moon, B. R. 2001. Muscle physiology and the evolution of the rat- Young, B., J. Jaggers, N. Nejman, and N. J. Kley. 2001. Buccal ex-
tling system in rattlesnakes. Journal of Herpetology 35:497–500. pansion during hissing in the Puff Adder, Bitis arietans. Copeia
Moon, B. R., J. J. Hopp, and K. E. Conley. 2002. Mechanical trade- 2001:270–273.
offs explain how performance increases without increasing Young, B. A., K. Meltzer, and C. Marsit. 1999. Scratching the sur-
cost in rattlesnake tailshaker muscle. Journal of Experimental face of mimicry: Sound production through scale abrasion in
Biology 205:667–675. snakes. Hamadryad 24:29–38.
Moon, B. R., T. J. LaDuc, R. Dudley, and A. Chang. 2002. A twist to Young, B. A., K. Meltzer, C. Marsit, and G. Abishahin. 1999. Cloa-
the rattlesnake tail. In P. Alerts, K. D’Aloût, A. Herrel, and cal popping in snakes. Journal of Herpetology 33:557–566.
R. Van Damme (eds.), Topics in Functional and Ecological Verte- Young, B. A., N. Nejman, K. Meltzer, and J. Marvin. 1999. The
brate Morphology. Maastricht, The Netherlands: Shaker Pub- mechanics of sound production in the puff adder, Bitis ari-
lishing, pp. 63–76. etans (Serpentes: Viperidae) and the information content
Moon, B. R., and A. Tullis. 2006. The ontogeny of contractile per- of the snake hiss. Journal of Experimental Biology 202:
formance and metabolic capacity in a high-frequency muscle. 2281–2289.
Physiological and Biochemical Zoology 79:20–30. Young, B. A., S. Sheft, and W. Yost. 1995. Sound production in
Nelson, X. J., D. T. Garnett, and C. S. Evans. 2010. Receiver psy- Pituophis melanoleucus (Serpentes: Colubridae) with the first
chology and the design of the deceptive caudal luring signal of description of a vocal cord in snakes. Journal of Experimental
the death adder. Animal Behaviour 79:555–561. Zoology 273:472–481.
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CO U RT SHIP AND R E P R ODU CTI O N
Young sea snakes have been found to be extremely numerous at certain

seasons, and it is quite possible that the pregnant females resort en masse to
protected bays to bear their young.
—William A. Dunson, The Biology of Sea Snakes (1975), p. 22

9
At the right time of the year—generally late summer in The Rainbow Serpent also is a mythological being for ab-
north temperate regions—various persons may see nu- original people across Australia, where it is part of a creation
merous young snakes that appear very near to one another, myth (fig. 9.2). In Fiji there is a serpent god who ruled the
and these are the wonderful product of reproduction by a underworld and caused fruit trees to bloom. A common
female snake of the same species that is no doubt in the symbol in many different religions and customs is a snake
same vicinity. For some it may challenge the imagination that is portrayed eating its own tail in the shape of a circle,
how a legless and armless animal crawling around on its and this represents life and rebirth. In ancient Greece it was
belly can be amorous and produce so many young. Fortu- in serpent form that Zeus was said to have fathered Alex-
nately, at least to my thinking, snakes are able to find one ander the Great. And in Christianity it was a serpent who
another of the opposite sex, court, mate, and reproduce enticed Eve with the promise of forbidden knowledge, and
even in the strangest of circumstances. Even so, studies this ultimately led to her mortality and bearing of children
have recently confirmed what many have witnessed: snake with Adam.
populations are in global decline, just like amphibians and
many other animals. The disappearance or increasing rarity
of snakes adds much emphasis to the importance of under- The Essentials of Reproduction
standing how these interesting creatures reproduce. Reproduction is, of course, one of the core essential attrib-
Snakes reproduce in diverse, complex, and fascinating utes of any living thing, and is part of the definition of life
ways, and there has been much human interest in this sub- that can be found in elementary biology textbooks. Organ-
ject ranging from folklore to scientific investigations, as isms are the expression of their DNA, the molecular blue-
well as the economic interests of the herpetoculturists who prints for their structure and function. Thus, for one living
breed snakes for sale (fig. 5.25). Since ancient times, snakes thing to be an offspring or product of another, the DNA
around the world have been regarded with symbolic and must be reproduced and passed from the first generation
mythical value. The word “serpent” is of Latin origin and individual (G1) to the second generation individual (G2). If,
means snake, or something that creeps. Hence the serpent as in cloning, the G2 was an exact DNA copy of G1, both
is one of the oldest and more widespread symbols in my- would be exactly alike unless there were accidental sponta-
thology, and reproduction is one of the more important of neous changes within the DNA (mutations) or the environ-
many varied contexts. ment changed and affected the expression of DNA in the
India is a land of many snake worshippers, and there are second individual. Such changes do, in fact, alter individual
rich traditions regarding snakes to represent rebirth, death, organisms and contribute to the variation of life that we see.
and mortality (fig. 5.1). There are several temples in Asia de- But there is even far greater variation in organisms because
voted to cobras, where it is believed that snakes are symbols of sex: two different individuals of the same species contrib-
of fertility and offer protection (fig. 9.1). Similarly, in West ute their DNA to a second generation individual, more or
Africa and Haiti a “rainbow-serpent” is a spirit of fertility. less equally, so the traits of the two individuals—one male
| 191
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them externally (fig. 9.4), or a blunt probe can be inserted
into the passageway that allows their eversion during
mating. Hence, if one attempts to push a blunt probe gently
into the base of the tail (insertion at either side of the mid-
line), it cannot enter the tail of a female but will slide for
some distance into the pocket that houses the copulatory
organs in a male.
The copulatory organs of male snakes are paired and
called hemipenes. Yes—the structure we term the penis in
humans is paired, and there are two of these in a snake.
Each one individually is called a hemipenis. In many species,
the hemipenes are highly ornamented and may be hooked,
bilobed, or bulbous in appearance. The terminal aspects of
these structures bear spines or spurs and are rough in sur-
face texture (fig. 9.4). These features secure internal attach-
ment within the cloaca of the female during mating, and
their variation among species has been useful as a taxo-
nomic character. Usually only one hemipenis is used during
copulation. When erected, internal sinuses become en-
gorged with blood and the structure is turned inside-out
while being forced out of the vent. Following copulation the
hemipenis is pulled back into the body of the male by a re-
tractor muscle and turns outside-in during the process.
When copulating, the erected hemipenis is inserted into
the cloaca of the female, and sperm travel down a narrow
groove on the hemipenis into the cloaca or vagina (part of
Figure 9.1. A temple to Buddha at Mount Popa, central Myanmar the oviduct) of the female.
(formerly Burma). The Buddha is under the protective umbrella of a
many-headed King Cobra. Photograph by Indraneil Das. The Gonads
The gonads of snakes are paired organs located in the ab-
dominal cavity, usually in close proximity to the anterior
and one female—are combined to produce new variation of ends of the kidneys and posterior to the gall bladder. The
traits in the new individual. As this process continues, the gonads of males are the testes (fig. 9.5), and those of the fe-
thousands of genes, or individual units of inheritance com- male are ovaries (fig. 9.6). In males, the right testis is typi-
posed of DNA, are recombined in different ways to produce cally more anterior than the left, and both are generally
variation among sexually reproducing organisms, including smooth and elongated, although in blind snakes of the ge-
snakes. nus Leptotyphlops the structures have multiple lobes. The
internal location of the testes is different from that in
Sex mammals, and the organs develop in close association with
Although individuals of any given species of snake look the kidneys inside the embryo.
more or less similar (albeit there is variation in size and The size of the testes may vary seasonally, with increased
color), populations include both male and female individ- size indicative of the production of sperm, called spermato-
uals. Herpetologists have developed ways of sexing snakes, genesis. The sperm are produced from germ cells within sem-
and these include probing or palping the base of the tale. In iniferous tubules, which are convoluted and comprise the
younger snakes, these procedures can be difficult and un- interior of the testis. These tubules are continuous with,
certain, but adult snakes of many species exhibit differ- and empty into, anterior efferent ducts that are lined with
ences in the shape of the tail that can identify the sex of the ciliated cells and smooth muscle. The efferent ducts drain to
individual when inspected visually. In comparison with fe- the epididymis where sperm will be stored for varying pe-
males, the tale of a male tends to be more elongate and is riods until ejaculation. The sperm are ultimately transferred
relatively broader near the vent due to internal copulatory to the hemipenes during copulation.
organs that are held within a pocket at the base of the tale The female reproductive tract consists of paired ovaries
(fig. 9.3). The copulatory organs can be everted to reveal and associated pairs of reproductive ducts. Ovaries vary
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Figure 9.2. The snake is a common motif in the aboriginal art and mythology of Australia. This aboriginal painting depicts people surrounded
by snakes, which are associated closely with water, land, fertility, birth, abundance (plants and animals), social relations, and protection. The
snake is a creator of human beings, and its life-giving powers send spirits of conception to all the water holes. In essence, the serpent embodies
regenerative and reproductive power in nature and in human beings. It is a principal character in major rituals. This painting is by Gavin
Delacour, who is an aboriginal painter born at Mt. Isa and presently living in Townsville, Australia.
in their location, but are usually found near the gall- Ovulation releases a mature egg from its follicle, and the
bladder. Each ovary is elongated and contains egg follicles egg is now ready to be fertilized. The remaining follicle
at different stages of development, degeneration, or re- forms a corpus luteum, which becomes an endocrine struc-
sorption (fig. 9.6). Vitellogenesis refers to the deposition ture and releases hormones until it regresses following
of fat reserves, or accumulation of yolk, in the ovarian birth of the young or the laying of eggs to hatch outside the
follicles, and vitellogenic follicles are developing eggs that body of the female. Ovulated eggs enter the oviduct, which
are being “yolked” within the ovary. The precursors of is a narrow tube extending from the ovary to the cloaca (see
yolk are synthesized in the liver. Vitellogenic follicles in- fig. 2.35). It is lined with smooth muscle, both ciliated and
crease in size and become increasingly yellow in color as nonciliated mucous cells, and various glands. The glands
the process advances (fig. 9.6). Like testes, their status produce various membranes that will surround the devel-
can be influenced by season, and the time that is involved oping egg, and their activity varies with the reproductive
in producing yolk-laden eggs varies among species. Hence, status of the female. The middle segment of the oviduct
small pre-vitellogenic follicles may characterize quiescent where eggs are retained before they are laid contains glands
ovaries for much of the year in many species that exhibit that produce the fibrous and calcium components of the
seasonal reproduction. The growth of follicles can be eggshell (see below). This is also the region where embryos
quite rapid just before mating in the spring. Ultimately, are incubated in live-bearing species (see below). The middle
each individual follicle either releases its egg (termed ovu- part of the oviduct is termed the uterus and is homologous
lation) or degenerates. to the uterus of mammals.
Courtship and Reproduction | 193
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Figure 9.4. Everted hemipenes of a sea krait (Laticauda semifasciata)
illustrating paired structures, each engorged with blood and showing
the sulcus and spiny terminus that assists internal attachment within
the cloaca of a female during copulation. A metric rule is shown for
scale. Photograph taken in Taiwan by Coleman M. Sheehy III.
Figure 9.3. Ventral tail morphologies in Florida Cottonmouths

(Agkistrodon piscivorus conanti). The male (left) shows a somewhat
engorged tail near its base, whereas the tail of the female (right) is Figure 9.5. Ventral views of the coelomic cavity of a Corn Snake
less “turgid” in appearance. The male condition is due to internal (Pantherophis guttatus). The upper view features the left testis,
presence of hemipenes (bracketed region), which are everted just which is elongate and lies adjacent to the small intestine. The lower
below the cloaca during mating. The cloacal opening in each photo is view illustrates both testes, the right testis being cranial to the left
immediately below the lowermost ventral scute, which is marked with testis. The cranial direction (toward the head of snake) is to the left in
a white “x” in each photograph. These snakes were lightly both photos. Photographs by Elliott Jacobson.
anesthetized, and the photographs were taken by the author.
Fertilization
In snakes, and in all reptiles, fertilization occurs internally.
Sperm unite with eggs near the upper, or cranial, end of the
oviduct following ovulation and prior to the deposition of
membranous structures that eventually envelope each egg.
Fertilization may occur relatively soon after mating, or fol-
lowing long periods when sperm are stored in the female’s re-
productive tract. Females of some species can store sperm in
seminal receptacles, which are pocket-like structures associated Figure 9.6. Ovary of a Reticulated Python (Broghammerus
with certain segments of the oviduct, primarily in the cranial reticulatus) showing multiple previtellogenic follicles (PF) and
region. However, sperm aggregations are associated with the vitellogenic follicles (VF). Photograph by Elliott Jacobson.
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lumen or deep furrows of the posterior oviduct in some species structures that envelope the egg, and there may also be super-
(fig. 2.35). One hypothesis related to sperm location is that ficial layers to which calcium salts are added to impart some
sperm enter the posterior oviduct following mating, reside for rigidity and to provide a likely source of calcium for the devel-
variable periods, and then are attracted to receptacles in the oping embryo. These structures are termed the eggshell and
anterior region of the oviduct. Sperm from one or more mating eggshell membranes, which protect the internal contents of
are maintained and nurtured in the storage receptacles. One the egg during its development outside the mother’s body.
should also appreciate that viable sperm can be stored in the Prior to “shelling” of the eggs, the oviparous oviduct exhibits
ducts of the testes and can live within males for long periods. increases in the height of tissue related to growth of the shell
Female snakes can store sperm for periods of months to glands and thickening of connective tissue and musculature
years, and thus mating and fertilization do not necessarily that will envelop the uterus. The oviduct and uterus provide
coincide closely in time. For example, some species might the eggs with water and oxygen prior to oviposition. After the
mate during the late summer or fall, but the young are born eggs are laid, embryonic development continues outside the
the following summer without the female having mated female, and the egg yolk provides the energy and nutrients
again. Moreover, females are able to produce two or more that are required for development of the embryo.
fertile cohorts of young from a single mating. This capability In other species the embryo is retained within the ovi-
can be advantageous in circumstances where a population is duct until development is complete (fig. 9.8). In this condi-
sparsely distributed and there are relatively few opportu- tion, the young are born in a developed state in contrast to
nities to mate. There is undoubtedly great variation in the laying eggs (fig. 9.9). Such reproduction is termed viviparity,
timing of mating, sperm storage, and fertilization in wild and snakes that exhibit this mode are viviparous. Nutrients
populations of snake species that are not yet well studied. and respiratory gases are exchanged across a placenta,
Examples of sperm storage are known largely from ac- formed by a close association (apposition) of extraembry-
counts of reproduction in captive snakes. Several instances onic membranes (the chorioallantois) with tissue of the ma-
involve females that were kept isolated from males for very ternal oviduct (uterus), and richly supplied with blood
long periods and then surprised their owners by giving vessels (fig. 9.10). The embryos of viviparous snakes in-
birth to healthy young snakes. Amazingly, a captive female crease in mass due to the uptake of water and nutrients.
Arafura File Snake (Acrochordus arafurae) was kept in isola- There are variable degrees of dependence on a placenta
tion for seven years and following its death was found to for nutrients. The developing young in some species are
contain an apparently viable developing embryo! nourished by egg yolk, and they hatch or break through the
egg membranes immediately before, during, or after the
Virgin Birth eggs are laid (fig. 9.11).
One of the reasons biology is so fascinating is that almost al- Whether a species of snake lays eggs or gives birth to
ways there are novel exceptions to the so-called general rules. developed young depends on the evolutionary history and
Hence, there is one species of snake that does not reproduce in geography. Viviparity has evolved convergently in 14 principal
a sexual manner as appears to be characteristic of all the other
snakes. The Brahminy Blind Snake (Rhamphotyphlops brami-
nus) is a small burrowing species, originally from India and
Southeast Asia, that has been accidentally introduced in many
other parts of the world because of it secretive habits and
ability to hide in small containers of soil (fig. 1.11). For this
reason it is also called the “Flowerpot Snake.” Every individual
is a female and, when mature, lays eggs that produce females
that are clones of the mother. Each egg develops without the
requirement of sperm from another individual and is thus an
example of asexual reproduction known as parthenogenesis.
This condition in Rhamphotyphlops is possibly unique among
snakes, although it is also known in several species of lizards.
Reproductive Modes
Figure 9.7. A Pueblan Milksnake (Lampropeltis triangulum
The majority of snake species lay eggs (termed oviposition), campbelli) with newly oviposited eggs. The white egg near the center
and this mode of reproduction is called oviparity (fig. 9.7). Spe- of the photograph is just exiting the cloaca where the skin is seen to
cialized glands lining segments of the oviduct lay down fibrous be stretched. Photograph by David Barker.
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On the other hand, viviparity confers
benefits of thermoregulation and permits
snakes to exploit environments where
suitable sites for nesting are limited or
absent. The evolution of viviparity ap-
pears to be causally linked to such bene-
fits related to temperature.
The terrestrial live-bearers, or viviparous
species, tend to occur at higher altitudes and
latitudes, representing locations where tem-
peratures are cooler. Carrying the young
snakes inside the mother’s body has the ad-
vantage that the female can keep the devel-
oping embryos warm by basking in warm
places (see chapter 4). Such thermoregula-
tion by pregnant females accelerates embry-
onic development and allows young snakes
to be born in time to feed and learn about
their environment before cold weather sets
in. By comparison, there are fewer sites
available where developing eggs could be ex-
posed to warm temperatures that are suffi-
cient to allow development to hatching
Figure 9.8. In the upper photo four embryonic Yellow-bellied Sea Snakes (Pelamis
platurus) are shown in the condition inside the mother snake immediately before birth.
before the first frosts occur. An important
The placental connection to the maternal tissues can be seen in the three embryos to point of this discussion is that carrying de-
the right. The lower photo illustrates the developed condition of these same snakes in veloping young inside the mother reduces
relation to the length of the mother. These four neonatal snakes represent the litter size chances that the vagaries of weather will kill
for this particular female. The mother snake died inadvertently for no apparent reason the embryos, because the female snake can
just before these photographs were taken by the author in Costa Rica.
respond behaviorally to temperature chan-
ges, whereas eggs are dependent totally on
the microenvironment in which they are laid. Thus, it is thought
that viviparity reduces the mortality of young in colder envi-
ronments. Species of snakes that inhabit very cold habitats—at
the extremes of ranges either by latitude or altitude—are all
viviparous.
Similar patterns of reproductive mode and geography
occur in lizards. Worldwide, viviparity has evolved indepen-
dently more than a hundred times in snakes and lizards
combined. Thus, it appears that colder climates have stimu-
lated the evolution of live-bearing in many lineages of squa-
mate reptiles. I should mention that the proportion of
viviparous species is much higher among snakes than
among lizards. For example, Donald Tinkle and Whit Gib-
bons estimated that among North American reptiles the
Figure 9.9. A captive newborn baby Yellow-bellied Sea Snake proportion of viviparous snakes is two to five times greater
(Pelamis platurus) with its mother. Photographed in Costa Rica by the than that of lizards at comparable latitudes. The reasons for
author.
this pattern are not clear. Rick Shine has suggested that the
evolution of live-bearing might be favored by defensive ca-
lineages of snakes representing virtually every type of hab- pabilities such as large size or venom apparatus, which char-
itat that they utilize. Viviparity can reduce the mobility acterize snakes more so than lizards. Finally, it should be
of female snakes, decrease feeding behavior, and constrain noted that completely aquatic marine snakes are all vivipa-
the size of a litter as well as the frequency of reproduction. rous, undoubtedly because there are no appropriate places
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for externally oviposited eggs to develop
if they were exposed to ocean water.
Placentation evolves together with vi-
viparity in snakes, and the functioning of
a placenta requires a thinning of the egg-
shell as well as changes in its composition.
As a consequence, there is an intimate as-
sociation between the fetal membranes
and the lining of the oviduct. Such an im-
portant union of tissues gave rise to sub-
sequent specializations for the transfer of
oxygen and nutrients from the mother to
the embryo (figs. 9.8, 9.10).
Eggs
The eggs of oviparous snakes vary consid-
erably in size and shape. They are generally
ellipsoid, but typically elongate rather than
spherical (fig. 9.12). The eggshell is gener-
ally leathery and flexible in most oviparous
species and consists of two principal layers.
The inner layer contains a thin network of
proteinaceous and elastic fibers that vary
in their size and orientation in different
species. These fibers give strength to the Figure 9.10. Schematic illustration of the placental membranes investing the embryo
shell, but they can also expand as the em- of a snake. The chorioallantoic placenta surrounds most of the embryo when its
bryo grows and the egg gains water during formation is mature, and the omphalallantoic placenta forms the ventral wall of the egg.
Each placenta is formed by the union of the fetal membrane with the lining of the
its development. Overlain onto this fi-
uterus. The developing embryo is shown in the center of the illustration. Drawing by
brous network is a mineral layer consisting Dan Dourson, based on the placental membranes in the natricine snake Virginia
of a sparse covering of calcium carbonate striatula (Stewart, J.R., and K. R. Brasch, Ultrastructure of the placentae of the natricine
crystals. The mineralized layer is thicker snake, Virginia striatula (Reptilia: Squamata), Journal of Morphology 255:177–201, 2003,
and denser in what are termed “rigid- and fig. 5.6 in R. D. Aldridge and D. M. Sever (eds.), Reproductive Biology and
Phylogeny of Snakes, vol. 9 of Reproductive Biology and Phylogeny, B. G. M. Jamieson,
shelled eggs.” These are characteristic of
series editor (Enfield, NH: Science Publishers, 2011).
many turtles and crocodilians, and some
lizards. However, the mineralized layer of
snake eggs is sparser and interspersed
with fibers, which renders the eggshell more flexible and vari- contrast with the eggs of snakes, those that are more
ably elastic (fig. 9.13). heavily calcified and rigid can be virtually inflexible and are
The “flexible-shelled eggs” of snakes are very permeable, more resistant to water exchange. Such eggs can be incu-
say compared to avian eggs. They take up water from moist bated in more open environments than is possible with the
environments during development and tend to expand less calcified eggs of oviparous snakes.
against the partially mineralized shell. The flexible shell Inside the egg, the developing embryo is surrounded by
stretches somewhat but also imparts pressure to the inter- other membranes that are internal to the eggshell. These are
nal fluid compartments of the egg. Such eggs may double or so-called extraembryonic membranes. One of these encloses
triple in mass due to the gain of water (fig. 9.13). On the the yolk to form the yolk sac, while three others surround the
other hand, these eggs also lose water easily, and the loss embryo in a fluid-filled space and function to transport nu-
can be substantial if the water vapor pressure surrounding trients, sequester metabolic wastes, and exchange respira-
an egg is only slightly less than saturated (< 99 percent). tory gases. A network of blood vessels functions to transport
The permeability of these eggs has much ecological signifi- nutrients from the yolk to the embryo (fig. 9.11).
cance, and eggs can dehydrate lethally if the microenviron- Female snakes lay eggs in various places where the temper-
ment is not appropriate, say because of a drought. In ature and surrounding moisture must meet requirements for
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Figure 9.11. Newly born Boa Constrictors (Boa constrictor) featuring
an albinistic neonate in the center. The young snakes are fully
developed at birth and enveloped temporarily within egg membranes,
in which blood vessels can be seen. The young break through the
membranes very soon after birth. Photograph by Tracy Barker.
proper development and hatching. Usually the eggs are buried

in moist soil or oviposited in crevices or other places where
they are protected from mechanical harm and from drying.
Female King Cobras (Ophiophagus hannah) actually construct
a nest for the eggs, consisting of a mound of leaves and or-
ganic debris, which provide a microenvironment that is char-
acterized by moderated and sometimes elevated temperature
(fig. 9.14). Also, the eggs are not exposed to the air and are less
subject to drying within the leaf mound. Some sea kraits (Lat-
icauda spp.) lay their eggs on rock ledges inside moist caves
that are adjacent to the sea. These places may be visited by Figure 9.12. A female Yellow-tail Cribo (Drymarchon corais corais)
from British Guyana, seen here with her clutch of eggs that were
large numbers of snakes, and many females probably return to
oviposited in captivity. The inset in the upper photo shows the
lay eggs at the same site year after year. There are many species complete clutch of eggs, which number 14. The lower photo shows
of snakes in which females aggregate communally to gestate two newborn cribos that have just emerged from their eggshells. Note
and lay eggs in places where the soil conditions are “just right.” there are slits in the shell of the lower right-hand egg, made by the egg
In some cases, females from a very wide area lay eggs in a com- tooth of the neonate inside the shell. Photographs by Elliott Jacobson.
munal nesting site, or they aggregate during gestation of the
young in areas that are limited in size. Such communal behav-
ior on the part of female snakes likely reflects a scarcity of sites smaller hatchling size can decrease the survival rate in
that are suitably moist or warm for eggs or gestation. Unfortu- some species of snakes. Even when conditions are within a
nately, there are many species of snakes for which little or normal range for hatching, subtle changes in these condi-
nothing is known about reproduction and oviposition. tions can cause shifts in the trajectories of embryonic
The proper development and hatching of snake eggs de- development. Such sensitivity suggests there is strong se-
pends on the temperature and moisture of the soil or other lection pressure for female snakes to recognize and use
medium in which the eggs are laid. These parameters are nesting sites that provide optimal conditions for the eggs to
extremely important during incubation, and they influence develop and hatch. This probably explains why some sites
the size, shape, growth rate, behavior, and other attributes are used repeatedly for communal nesting year after year.
of hatchling snakes. If temperature or soil moisture condi- Just before hatching the baby snake nearly fills the en-
tions are not adequate, the hatching success of eggs can di- tire space within the confines of the eggshell, and it has to
minish and birth malformations can occur. For example, create an opening in the eggshell from which it can emerge
drier soils can lead to a decreased size of hatchlings, and at hatching (figs. 9.12, 9.15). There is a deciduous toothlike
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are generally more prolific than lizards and produce clutch
or litter sizes that vary from 1 (a few species of boids and
colubrids) to more than 100 (some Thamnophis species and
elapids). Larger clutch sizes are characteristic of some spe-
cies of boids (e.g., Reticulated Python), and larger litter
sizes are characteristic of some species of viperids (e.g.,
Fer-de-Lance) and natricine snakes (e.g., Northern Water
Snake, Plains Gartersnake). Recently an invasive Burmese
Python captured in the Florida Everglades was reported to
be 17 feet and 7 inches long (a little less than 5 meters) and
contained 87 eggs. Most snakes, however, produce young
in the range of several to 20 in a single clutch or litter (figs.
9.8, 9.12).
The number of young relative to the length of a female
tends to be larger in viviparous than in oviparous species,
and in aquatic and semifossorial species compared with ar-
boreal and terrestrial species. Another general finding is
that the ratio of the total clutch mass to female mass (called
relative clutch mass, RCM) is about 20 percent higher in ovip-
arous compared with viviparous species, which implies ei-
ther a greater brood size or offspring size, or combination
of both, in the oviparous species. For a given RCM, the
number of eggs produced (clutch size) is related to the en-
ergy that is allocated by the female to each individual off-
spring. Both female size and clutch size vary among snakes,
even within a species. In general, marine snakes produce
larger young than do terrestrial species. Within marine
snakes, larger species produce the larger young, but smaller
species also produce relatively large young by reducing the
clutch or litter size. If one corrects for female body size,
larger clutches generally result in smaller young. Among
Figure 9.13. The upper photo shows the egg of a Black Rat Snake some oviparous species, larger females tend to lay larger
(Pantherophis obsoletus) that has completed 80 percent of incubation.
eggs, and for a given size of female, eggs in larger clutches
The outer shell layers including the calcareous components have
fractured because of swelling of the egg from the uptake of water. The
are shorter than those in smaller clutches.
lower photo is an electronmicrograph featuring the surface of the Because the body of a snake is tubular, the volumetric
eggshell and reveals the calcareous layer with pores. The pores geometry suggests that larger snakes can produce a larger
presumably enhance the exchange of gases across the eggshell. The number of similar size offspring and can increase clutch
bar in the upper photograph equals 1 cm, and that in the lower size with less effect on offspring size. All of these factors
photograph equals 50 μm. Photographs by the author.
complicate analysis and generalizations, but suggest there
are constraints on the size and number of young—which
determine the fitness or reproductive potential of the fe-
projection from the tip of the premaxillary bone that is male. The term fitness refers to the ability of an organism to
termed the “egg tooth.” This structure functions to cut or contribute genes to the next generation, and this equates
tear an opening in the leathery eggshell, from which the approximately to the number of offspring weighted by the
young snake can emerge (figs. 9.12, 9.15). The egg tooth is probability that those offspring will survive and reproduce.
temporary and is shed away at hatching.
When and How Often Do Snakes Reproduce?

Clutch and Litter Size This is an important question, and one that is not easily an-
There is quite a lot of information that has been published swered because we do not have sufficient knowledge of
on the number of eggs (clutch size) or live young (litter size) many species of snakes to generalize with confidence. In
that characterize reproducing snakes. As a group, snakes places where individuals of a particular species are quite
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metabolism, and prey availability to fe-
males (see chapter 4). Many snakes, espe-
cially in temperate climates, reproduce
once per year or less frequently depending
on both food resources and temperature,
which generally equate with the length of
the active season. Colder climates generally
tend to slow reproduction. For example,
European Adders (Vipera berus) reproduce
approximately yearly in southern Europe,
but every two years in northern France and
every three years in the Alps.
Environmental Cues Affecting

Reproduction
Physical signals from the environment that
Figure 9.14. A female King Cobra (Ophiophagus hannah) photographed while resting influence reproduction seem logically to be
on its nest where the eggs are attended in the Western Ghats of India. The female
more important in temperate than in trop-
snake constructs the nest by pulling leaves together with coils of its body. Photograph
by Gowri Shankar. ical environments. However, we know little
about what influences reproductive cycling
in the tropics, so this statement is a hypo-
thesis that remains untested. The more
common—garter snakes for example—it would seem that logical cues in temperate environments are
at least most females reproduce every year. On the other the amount of day length, or photoperiod, and temperature,
hand, species that appear to be very rare—sometimes an ar- both of which vary with seasons. Although photoperiod is an
tifact of human impressions or inability to find specimens— important cue for reproductive changes in birds and other
one might assume that reproduction occurs less frequently. animals, temperature is more important for ectothermic
The evidence at hand suggests that both situations occur reptiles such as snakes. This is especially true in regions
in natural populations of snakes, and that the frequency of where these animals spend much time beneath ground
reproduction is dependent on the environment and the during winter dormancy when changes in the levels and
food resources that are available to a given female. timing of light above ground are not evident below ground.
First, we know much about the captive breeding of snakes Increases in temperature—both below and above
through efforts at reproducing species on the part of zoos, ground—are thought to play an important role in influ-
private hobbyists, and commercial breeders who have pro- encing the spring emergence and subsequent reproductive
moted herpetoculture as a significant part of the pet industry behavior of many snakes that live in temperate environ-
(fig. 5.25). Not only are many snakes capable of reproducing ments. Emergence of hibernating rattlesnakes, for example,
every year, but numerous oviparous and several viviparous is stimulated by increasing temperature, or reversals of
species are capable of producing more than one clutch or litter temperature gradients, within dens where these snakes
during a year. Perhaps the best-known example of an unusu- spend the winter. However, it seems that increasing tem-
ally prolific snake is the African house snake (Lamprophis perature is not essential for spring emergence of garter
spp.), which includes several small- to medium-size species snakes that live in some of the Canadian provinces (fig. 4.7)
native to sub-Saharan Africa. The species Lamprophis fulgino- because they emerge with body temperatures as low as
sus has become a commonly kept snake because it is easy to 0.5°C. As in the garter snake, many other species of snake
maintain in captivity and breeds prolifically. If these snakes breed seasonally and experience a period of winter dor-
are well fed, females will lay clutches of eggs as often as every mancy at relatively low temperatures prior to mating in the
two months, and the tendency for individuals to mate is not spring. In cases where reproduction occurs immediately fol-
restricted seasonally! Examples of multiple clutches or pro- lowing the emergence from dormancy in the spring, signif-
lific live-bearing from captive snakes are artificial, however, in icant changes in reproductive physiology and behavior are
the sense that food is available in excess relative to what likely to occur during the period of winter dormancy.
snakes might actually enjoy as resources in wild populations. Because of the difficulties of access, there is, not surpris-
Temperature is an important factor that influences repro- ingly, much “underground” ecology and behavior of snakes
ductive rates because of its effect in determining activity, that is totally unknown. What are the metabolic status,
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cold, and temperatures could drop to lethal levels for ecto-
therms within a very short time (less than a day). What
happened to the snakes that had been active—which evi-
dently had occupied rather shallow retreat sites and could
respond to the brief period of warming? Perhaps they es-
caped again to underground retreats, or perhaps some had
been “caught” by the changes associated with the cold front
and were killed in the winter because of their premature
emergence. It is interesting to think about this, because
there must have been other snakes that were located, and
remained, in deeper places where they might not be aware
of the brief warming that occurred because of limited
ground penetration of the thermal changes.
Warmer temperatures induce courtship and mating be-
haviors of garter snakes, and they are probably important
for activity of the gonads as well. These behaviors are ex-
pressed more strongly, and in more individuals, when
snakes first experience a lengthy period of low temperature
that appears to “reset” an endogenous seasonal clock. Per-
sons who breed snakes subject various captive species to
periods of cooling in order to enhance the probability of
success when males and females are placed together to en-
courage mating. More generally, the scientific literature
suggests that temperature is the principal environmental
cue that regulates reproduction in snakes as well as in other
squamate reptiles.
The few snakes that have been studied in tropical loca-
tions generally exhibit seasonal reproduction. With respect
Figure 9.15. A hatchling Trans-Pecos Rat Snake (Bogertophis to populations or species outside of equatorial regions,
subocularis) as seen (upper photo) just as it has pierced the eggshell temperature is a potential environmental cue, although not
using the egg tooth (which is now gone) and (lower photo) as it as extreme in variation as in temperate regions. Seasonality
appears following emergence from the eggshell. The inset illustrates of rainfall can be important, especially in regions that have
a Black Rat Snake (Pantherophis obsoletus) inside its eggshell just
distinctly seasonal drought. The timing of reproduction
prior to hatching. Embryonic fluids can be seen inside the egg and
oozing out the openings that were made in the eggs by the respective
might be related to the availability of food resources (which
hatchlings. Photographs by Elliott Jacobson (upper, lower) and the might also be cyclic) to ensure successful vitellogenesis,
author (inset). mating, and embryogenesis in females, and/or to ensure
the availability of food for neonates during their early life.
awareness, and influence of environmental cues for animals The Neuroendocrine Regulation of Reproduction
that are overwintering very deep beneath the ground and Relatively little is known about how nerves and hormones
do not immediately experience warming temperatures of control the reproductive cycles of snakes, relative to the
spring? Are there endogenous circannual or seasonal cycles vast literature on this subject that exists for mammals and
that operate to stimulate the timing of emergence? What birds. Moreover, most of the knowledge presently available
happens to those animals that happen to occupy sites of ref- for snakes is focused on a single species, the Common Gar-
uge that are not very deep? When I was living in eastern ter Snake (Thamnophis sirtalis). Generally, signals from the
Kansas for about 13 years, I noticed that occasionally there environment related to temperature and light conditions
were unusual periods of warming that occurred during cer- are cues to changes in neural pathways (nervous system),
tain winters. I lived in rural countryside for part of this endocrines (hormones), and neuromodulators that influence
time, and I observed that certain species of snakes (espe- reproduction (fig. 9.16). The prefix neuro- refers to nerve or
cially garter snakes) emerged and were active during these neuron. Hence, neuromodulators are chemicals released
warm spells, crossing roads for example. Then what invari- from nerve endings that “modulate” or change the signaling
ably ensued was a cold front would turn the weather bitterly behavior of neighboring neurons that are part of a common
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Figure 9.16. Conceptual diagram of the controlling elements in the reproduction of snakes. The gray circles
represent factors that reside outside the animal, and the other elements interact within the animal. The scheme of
interactions is generalized, and many of the details are not well known in snakes. Drawing by the author.
pathway. Variation in neuroendocrine mechanisms has places in the body (e.g., retina, brain, and intestine), but
contributed to evolutionary variation in the patterns of re- the principal source is the pineal gland. Melatonin influ-
production in these, as well as other, vertebrates. ences both physiology and behavior, and it is therefore an
Environmental temperature plays a key role in regu- important communicator between environmental cues of
lating reproduction in snakes as well as in other ecto- light and temperature and the internal functions that affect
thermic vertebrates such as lizards. Temperature influences reproduction.
important centers of the brain, especially specific parts of In the absence of light, temperature alone can modulate
the hypothalamus and the pineal gland, a small organ that is the level of melatonin in garter snakes that are in winter dor-
formed near the roof of the forebrain. The pineal gland se- mancy. Studies by Deborah Lutterschmidt and Robert Ma-
cretes melatonin, which is synthesized and released rhyth- son showed that melatonin levels are lower in garter snakes
mically in response to environmental cues of temperature exposed to low temperature, but the amplitude of cyclic mel-
and photoperiod. Levels of melatonin (which circulate in atonin release is increased following a prolonged period at
blood) are higher during night, or darkness, and therefore low temperature. Other studies indicate that surgical re-
exhibit a circadian (daily) rhythm that is related to daily cy- moval of the pineal gland can change the courtship behav-
cles of light and dark. Melatonin is also produced at other iors of snakes. While the precise actions of melatonin are not
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understood, these and other investigations appear to estab- probable actions in modulating the reproductive system
lish that pineal secretions of melatonin both modulate and in snakes. Therefore, further discussion of these is not
synchronize reproduction with environmental cues. Addi- warranted.
tionally, melatonin also plays a role in synchronizing daily
patterns of activity with reproductive behaviors. Reproductive Cycles
A specific region of the brain—including the anterior The periodicity of reproduction in snakes is variable among
part of the hypothalamus and the nearby pituitary species, with underlying mechanisms or even changes being
gland—is an important center for integrating external not well understood except for a few species. Robert Al-
and internal cues related to reproduction. This site in the dridge and his colleagues (in addition to others) have de-
central nervous system also is important for responses to scribed several types of cyclic reproduction in snakes, with
temperature and the orchestration of behaviors related to various terminologies being applied to them. Here I shall
temperature regulation. With respect to reproduction, go- attempt to simplify the description into basic patterns.
nadotropic hormones that stimulate the gonads (follicle Reproductive processes cycle when the gonads or acces-
stimulating hormone, leutinizing hormone) are synthe- sory organs become quiescent for a period of the year. This
sized in this region—largely in the pituitary—and re- seems to be widespread in both temperate and tropical spe-
leased into the blood circulation by the external signals cies. Spermatogenesis does not need to coincide with
that synchronize reproduction. Yet other factors called mating, and sperm that are produced at another time can
gonadotropin-releasing hormones act in between to stimu- be stored in the ducts that are used for transporting sperm
late the release of the gonadotropic hormones (also called in males, or in the oviducts of females (e.g., if mating oc-
gonadotropins) when activated by signals related to the curs during the fall). Another pattern occurs when the go-
external cues. This describes the generally characteristic nads or accessory organs exhibit a reduction of activity
hierarchical control of gonadal function in tetrapod ver- during part of the year but do not become completely qui-
tebrates, including many reptiles, but we have very escent. Such a phenomenon has been inferred to exist in
sketchy information about the mechanisms that govern snakes, but the details are not completely verified. Finally,
this system specifically in snakes. For purposes of this the gonads might remain more or less constantly active
discussion, we will assume that episodic secretion of go- without any pronounced cycling in the level of activity.
nadotropin-releasing hormones and, secondarily, the Again, this pattern has been inferred to exist, but the evi-
release of gonadotropins from the hypothalamus, are dence is not conclusive.
required for normal reproduction in snakes. Whatever the pattern, variation occurs among species
At the level of the gonads—testes in males and ovaries with respect to the phase relationships between reproduc-
in females—steroids are secreted and stimulate gonadal tive behaviors and the cycling of activity of the gonads.
tissues as well as other distant target organs via circulation There can also be considerable variation among individ-
in the blood. The principal gonadal steroids in tetrapod ver- uals within a species, although generally speaking, repro-
tebrates are progesterone, estrogens, and testosterone. Pro- duction is highly synchronous among individuals of a
gesterone is essential for the development of eggs and population. The majority of snake species that have been
embryos. Estrogens have many effects including the devel- studied exhibit seasonal reproduction, and the synchrony
opment and maturation of egg follicles, vitellogenesis, and of reproduction becomes stronger as the latitude increases
growth of the oviduct, in addition to secondary sexual char- away from the tropics. Fewer species have nonseasonal re-
acteristics (changes in body coloration, for example) and production, and all of these occur in tropical or equatorial
reproductive behaviors. Testosterone is synthesized in the areas.
testes and regulates the secondary sexual characteristics Investigations of reproductive patterns are challenging,
of males. Testosterone belongs to a class of sex steroid and it is sometimes difficult to adequately judge the repro-
hormones called androgens. In both male and female rep- ductive condition of the gonads, especially testes. For
tiles, androgens can be converted to estrogens in the cen- example, Selma Maria Almeida-Santos and colleagues dem-
tral nervous system and elsewhere (see below). These onstrated that male Brazilian Rattlesnakes (Crotalus duris-
conversions in the brain affect the reproductive behaviors sus terrificus) retain sperm in reproductive ducts throughout
of both male and female animals, but very little is known the year. Although the volume of semen appears not to
about these effects in snakes. vary, the highest counts of sperm are observed just prior to
Various other peptide molecules and neuromodulators the mating season.
potentially influence reproduction and the reproductive be- The Common Garter Snake exhibits what is called a “dis-
haviors of snakes. As with the other factors mentioned sociated reproductive cycle.” This term refers to mating
above, very little is known about these chemicals and their when the circulating levels of sex steroid hormones are low
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Figure 9.17. The seasonal reproductive pattern of the male Red-sided Garter Snake (Thamnophis sirtalis parietalis). The variation of androgen
levels (high or low during spring emergence) is hypothesized to be related to annual variation in the severity of winter temperatures. Redrawn
by the author after fig. 8.2, p. 293 in R. D. Aldridge and D. M. Sever (eds.), Reproductive Biology and Phylogeny of Snakes, vol. 9 of Reproductive
Biology and Phylogeny, B. G. M. Jamieson, series editor (Enfield, NH: Science Publishers, 2011).
because of quiescent condition of the gonads (fig. 9.17), cues that trigger specific behavioral interactions between
which contrasts with most vertebrates, in which mating oc- male and female snakes. Males also interact with other
curs during periods when gonads are maximally active and males to compete more successfully for access to females.
circulating levels of sex steroids are elevated. In the garter Courtship, mating, and aggressive behaviors are complex
snake, levels of androgens vary during spring emergence and can vary among species. The expression of such activity
when mating occurs, evidently attributable to metabolic in snakes can be quite spectacular, but due to the cryptic
clearance of the hormones depending on the temperatures nature of many species, courtship and mating are rarely ob-
affecting snakes during winter dormancy following high go- served. Detailed knowledge of reproductive behaviors is
nadal activity in the summer and fall (fig. 9.17). Thus, the known for relatively few species of snakes, and is particu-
perception of the extent of “dissociation” of the reproduc- larly lacking in secretive, primitive, fossorial, and tropical
tive cycle in this species is temporal and might be attribut- species.
able to the variation of temperature during any particular James Gillingham has categorized the reproductive be-
winter dormancy. The pattern of reproduction in this garter havior of snakes into three distinct phases: precourtship,
snake is unusual when compared to many other species of courtship, and postmating. There is a wealth of natural his-
reptiles, likely due to the evolutionary influence of the ex- tory observations related to the courtship behaviors of
treme winter conditions to which these snakes are sub- snakes, but these are often not consistent in details, termi-
jected in the populations that have been studied. Research nology, or interpretation. Robust investigations involving
with snakes that experience “extreme” conditions in their both field observations and laboratory experimentation
environment can be very useful in elucidating the regula- have advanced our understanding of courtship behaviors
tory mechanisms that underlie reproduction generally. considerably—especially in recent years—but are lacking
for many taxa of snakes.
Courtship and Reproductive Behaviors Precourtship Behaviors

Like other vertebrates, snakes engage in ritualized court- Many snakes are not particularly social during much of
ship behavior prior to mating and the insemination of fe- the year, and we could imagine that encounters between
males. Courtship depends on visual, tactile, and chemical individuals of the same species might be somewhat rare
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(similarly to the rarity of encounters with humans). How- males, a trailing male relies on visual cues as well as chemical
ever, the persistence of a species or population depends ones to locate or relocate the female. Pheromone-based trail-
on male and female individuals finding one another, and ing behavior is presumably widespread among snakes, being
in the snakes’ world, awareness of one’s neighbors is prob- known for representatives of caenophidian, boid, and pytho-
ably much greater than we imagine. If you are a snake, nid species. Much evidence suggests that nonvolatile cuta-
knowing or finding your neighbors depends largely on neous lipids may communicate information about the
communication with chemical cues, as far as we know. species, sex, reproductive state, size, condition, and other
Chemicals on the skin of snakes adhere to the substrate properties of the individual snake that is the source of such
over which they move, and other individuals have the ca- pheromones. In some species, the ability of male snakes to
pability to detect these chemicals and to derive important trail females is seasonal and occurs only during the mating
information from such “signals.” These provide chemical season.
trails, and are a means by which one individual can locate Lipids that are dispersed from the skin are presumably
another. The ability of one individual to follow and locate less effective for intraspecific communication in aquatic
another has been termed trailing behavior. environments than in terrestrial ones. Richard Shine has
How do snakes detect a chemical trail, and what is the shown that pheromones appear to play no role in trailing
basis of perception that is used to follow it? Watch a snake behavior of the entirely marine Turtle-headed Sea Snake
that is moving through its environment in an exploratory (Emydocephalus annulatus), which depends on visual cues to
manner, undisturbed by any human observer, and you will locate potential mates.
notice it is frequently flicking its tongue to sample the So what about chemical cues that go airborne? One
chemical cues associated with its surroundings. The tongue study by Robert Aldridge and colleagues suggests that air-
collects the chemical cues and transfers them to the vom- borne chemicals can, in fact, be used to locate mates in the
eronasal organ in the roof of the mouth, where the chemi- Northern Water Snake (Nerodia sipedon). Male individuals
cals are sensed and the information is transmitted to the of this species orient preferentially to aerial cages that con-
brain (see chapter 7). These chemical “cues” communicate tained conspecific females. The use of volatile chemical cues
between individuals and therefore function as pheromones might be more important than previously supposed, partic-
(see chapter 5). Thus, pheromones are used in the trailing ularly in arboreal environments where chemical trailways
behavior of snakes, and certain ones also elicit sexual be- can be interrupted by gaps in the vegetation.
haviors in snakes.
The vomeronasal system primarily influences courtship Courtship Behavior
behavior, and olfaction plays a lesser or negligible role. Courtship behaviors are elicited by pheromones that render
Male garter snakes will not court female garter snakes if a snake sexually attractive as well as eliciting trailing behav-
the vomeronasal nerves are cut, whereas eliminating input ior. Once a male has located a female, whether by trailing or
from the olfactory nerves does not eliminate courtship. by closer association (e.g., simultaneous emergence from
The vomeronasal system is most responsive to non- overwintering dens), the lipid products in the skin of the
volatile chemicals, which are also most persistent in the en- female elicit a characteristic sequence of behaviors that are
vironment. The reproductive pheromones produced by well studied in garter snakes and are also known with little
snakes reside in the skin. Discharge from the cloacal glands variation in some other species. There is an important con-
plays either no role whatsoever or perhaps a secondary role nection here between the production of cutaneous phero-
that remains to be documented. The “sexual attractiveness mones and the act of skin shedding. Courtship is sometimes
pheromone” of garter snakes is well studied and is the only linked with the timing of ecdysis, and freshly shed females
pheromone that is adequately documented in reptiles. It is are particularly attractive to males (fig. 9.18). The compo-
a mixture of lipids consisting of long-chain methyl ketones. nents of cutaneous pheromones are also found in the older
How such compounds are produced and sequestered in the epidermis that is shed from female snakes.
skin for communication with other snakes is not well During periods of courtship male snakes that are com-
understood. peting for females engage in ritualized behavior referred to
Skin-based pheromones are the basis of trailing behavior as combat dance. This is a behavior in which one male chal-
in which male snakes follow females to initiate courtship. lenges another, usually of the same species, by elevating the
Trailing by males is complex and can involve multiple males anterior body and pushing the opponent in an attempt to
trailing a single female, for example in some colubrid species knock the individual to the ground. In some species, the
with seasonal occurrence of mating (garter snakes, racers). If two males engaged in “combat” both assume a nearly ver-
the pheromone trail is disrupted, either by configuration of tical posture and wave the fore-body, which may intertwine
the environmental substrate or by the movement of multiple (with each other) when contact is made between the two
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snakes (fig. 9.19). Biting is not part of the ritual, but rather At the next stage, the male attempts to align his body with
pushing the opponent to the ground and maintaining a that of the female, and he orients his head in the same direc-
higher position. Characteristically, the loser of the “com- tion as hers. The male next engages in caudocephalic waves,
bat” crawls away when it is defeated. which are horizontally undulating waves of the body that
Typically, larger males are dominant and win out in con- gently contact the female while lying upon or beside her.
tests that involve ritualized combat. In some species of These waves move from the posterior part of the body toward
snakes, larger males are more successful in mating with fe- the head and are thought to stimulate mating. Sometimes
males than are smaller males. Characteristically, male the wave movements are in the opposite direction, from head
snakes tend to grow larger than females of the same species toward the tail. The last stage of courtship involves move-
if intermale combat is part of the species’ reproductive be- ments in which the male attempts to align his cloaca with
havior. Also, the tail of a male snake is typically somewhat that of the female and then engage in copulation (fig. 9.20).
longer than is that of a female (fig. 9.3), which could be ad- In boas, courting male snakes use pelvic spurs to stimulate
vantageous for successful mating when courtship involves
“tail-wrestling” for cloacal alignment (see below).
Once a male snake has access to a female, courtship be-
gins with the male orienting toward the female and flicking
the tongue intensely. The tongue samples the chemical cues
from the skin, while both touch and vision are used during
these behaviors. Once the male has contacted the female, it
rubs its chin along the back of the female while continuing to
flick the tongue rapidly and maintaining contact. Biting the
body of the female is sometimes involved during this stage of
interaction, or even before. I have seen a male cottonmouth
trailing a female and, when in close range, crawl quickly for-
ward and gently nip the female on the posterior body near
the tail. Usually, however, biting is observed on the dorsal
surface of the female, closer to the neck. Such biting seldom
damages tissue, but it stimulates the female to assume a
more tractable position prior to coitus. Biting during court-
ship seems to occur principally in colubrid snakes.
Figure 9.18. A pair of Florida Cottonmouth Snakes (Agkistrodon Figure 9.19. Ritualized combat behavior between two male Florida
piscivorus conanti) resting together during a spring mating season. Cottonmouth Snakes (Agkistrodon piscivorus conanti) at Seahorse
The female snake is beginning to shed its skin (visible in the lower Key, Levy County, Florida. The upper photo shows the two males
part of photo), which imparts maximum attractiveness of the sexual with heads elevated in combat. The lower photo shows the same
pheromones in the skin. Photographed by the author at Seahorse Key, two males with the dominant male elevated over the snake that lost
Levy County, Florida. the contest and eventually crawled away. Photographs by the author.
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cloacal opening of the female just before insertion of the The use of chemical cues during courtship is documented
hemipenis (fig. 9.21). Courting snakes may vibrate or jerk the only in certain snakes, including viperids, natricine colubrids,
tail in rapid movements during the period just before coitus. and elapids. Other snakes such as boas and pythons appear to
rely principally on touch and body contact once a potential
mate has been identified. Although sea snakes do not use
pheromones for trailing, chemical cues are probably impor-
tant when mating pairs are engaged at close range.
Some intriguing research by Michael LeMaster, Robert
Mason, Richard Shine, and colleagues have shown that male
garter snakes can assess the body condition of a female
based solely on the information that resides in the chemical
cues from the cutaneous lipids of a female. The cue evidently
depends on the amazing fact that the mix of lipids in the
pheromone of a female becomes increasingly dominated by
longer-chain molecules as the length and body condition of
the female increases. The male snakes prefer to mate with
females that are longer and in better body condition.
During copulation the male engages the cloaca of the
female by inserting a single hemipenis into the cloaca or into
Figure 9.20. A pair of copulating Northern Copperheads
one of her vaginas (see figs. 9.4 and 2.35). The spiny distal
(Agkistrodon contortrix mokasen) with the tails entwined (arrow) just surfaces of the hemipenis help to maintain the physical union
prior to coitus. Photographed in Kentucky by Dan Dourson. between the two snakes. I once observed a dramatic example
Figure 9.21. Photographs of cloacal spurs in pythons. The photo at the left shows the paired spurs of a Ball Python (Python regius). The
photos in the center and at the right illustrate a single spur of a Water Python (Liasis fuscus), in use during mating and inactive respectively.
Photographs by David Barker.
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of just how strong this union can be when I watched a male Another interesting aspect of the mating aggregations
Eastern Yellow-bellied Racer (Coluber constrictor flaviventris) of garter snakes is the presence of “she-males,” which are
pull and drag a female nearly straight up into a pine tree that male snakes that are courted as females because they pro-
was being climbed while the two snakes were in copulation. duce female pheromones. The pheromones produced by
For part of the distance the female climbed upward and par- she-males are close enough to that of true females to con-
allel with the male in what appeared to be a cooperative effort found discrimination. Generally, however, larger females
to ascend together. However, there were moments during this receive more intense courtship than do she-males. Current
ascent when the female was facing head-down in a direction work by Robert Mason and others suggests that androgens
opposite to that of the male, and she was being pulled upward are converted to estrogens locally in the skin of male garter
solely by the means of physical contact at the cloaca. Thus, the snakes. Most, or nearly all, males emerge from winter dor-
full weight of the female was suspended by the hemipenis of mancy with some degree of “feminized” skin, but the
the male! Once these two snakes had ascended quite high into amount and quality of the female pheromones diminish
the tree, they came to rest in a horizontal position upon some with time. Several hypotheses regarding the supposed ben-
branches that were bearing pine needles, where presumably efits for having a presence of she-males have been put for-
copulation continued. In snakes generally, the duration of ward, but the phenomenon is presently poorly understood.
coitus varies from several minutes to many hours.
Following the successful mating of garter snakes, the Postmating Behavior
male deposits a seminal plug (sometimes termed copulatory Following mating there is probably little or no social behav-
plug) in the cloaca of the female. Dried seminal secretions ior that continues between male and female snakes in most
serve as a physical barrier to prevent the female from im- species. However, aggregations of gravid females have been
mediately mating again by blocking her vaginal opening. described in several species of viperid, colubrid, and elapid
The plug may also serve to prevent leakage of sperm from snakes. Reports of female snakes attending eggs following
the cloaca of the female. There is furthermore some evi- oviposition are numerous, especially involving colubrid and
dence that copulatory fluids from an actively mating male elapid snakes, pythons and pit vipers. Probably all pythons
garter snake contain an inhibitory pheromone that renders attend or brood their eggs as described in chapter 4, but
the female partner sexually unattractive for some while. there is little evidence for parental care of young snakes fol-
One very interesting behavior of snakes is the aggregation lowing their birth or hatching.
of large numbers of individuals during courtship to form Some interesting observations of pit viper behaviors
what is termed a mating ball. This is especially common in gar- should be mentioned here. Newborn pit vipers of several
ter snakes. There are anecdotal reports of the phenomenon in species remain with the mother snake for short periods fol-
other species, including sea snakes, but some of the accounts lowing birth, usually a matter of just a few days to two
are questionable. In garter snakes, males typically outnumber weeks until the very first shedding of skin by the neonates.
females in breeding aggregations when 10–100 males simul- Thereafter the young snakes disperse. There is little evi-
taneously court a single receptive female. In northern popula- dence for the adult female actively caring for the young
tions, numerous garter snakes emerge near-simultaneously during this period, but the newborn are tolerated and typi-
from overwinter dens where they engage in courtship and cally coil en masse with their bodies in close contact with
mating before dispersing for the active season (see fig. 4.7). I the mother. One function of such behavior could be protec-
have witnessed this phenomenon in eastern Kansas, where I tion from rapid evaporative water loss through the skin,
once found hundreds of garter snakes (Thamnophis sirtalis) in which builds a more protective barrier to water loss during
a so-called mating ball at the base of a dead tree near the edge the first ecdysis in some species. The South American Rat-
of a lake. I was most amazed to see how intense the males tlesnake (Crotalus durissus), having a tropical lowland
tongue-flicked and moved with jerky motions in attempt to distribution, is the only species of rattlesnake that is known
court a female. There is intense competition among males for not to engage in the parental attendance of neonates.
a female, and each male works to push other competing males The newborn young of Florida Cottonmouths (Agkistro-
out of the way. To be successful at mating, a male must phys- don piscivorus conanti) remain in close association with their
ically push aside and outmaneuver other males to engage the mother until their first ecdysis, as is known in several spe-
cloaca of a female in coitus. I picked up several individuals and cies of rattlesnakes. I have observed this on several occa-
held them in my hand. Each of these snakes seemed com- sions at the Gulf coast island of Seahorse Key. On one
pletely oblivious to being handled and steadfastly persisted in occasion, I found the newborn young of a cottonmouth in
rapid tongue-flicking while the body and head continued to attendance by both a male and female adult snake. Among
jerk rhythmically. I could not be sure about the ratio of males the larger adults on the island, male and female pairs are
to females in this circumstance. found in close association during all months of the year,
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and this possibly reflects some degree of pair-bonding in subsequent years of life. Thus, the eventual maximum size
this species. It seems highly likely that the pair of snakes of a snake can depend, in part, on this “silver spoon” effect.
that I found in association with the newborn snakes was a How rapidly can snakes grow? First, we need to distin-
mated pair. These social behaviors of cottonmouths are guish numerous anecdotes concerning rapid growth rates
presently the subject of more intensive investigation. and the large sizes of snakes that are raised in captivity.
Captive pythons generally increase their length nearly four-
fold during the first year of life. David Barker has informed
Growth and Sexual Maturation of Snakes me that Burmese and African Rock Pythons in his care have
The rates of growth and sexual maturation of snakes are im- increased in length as much as sixfold during the first year.
portant features of life history that determine the evolu- It is also important to note that many captive individuals
tionary success of a species and its persistence in nature. can be obese and very large in mass (weight) due to the
The investment of females in their offspring is reflected not “overfeeding” of such snakes by their owners. Nonetheless,
only in the number of young that are born, but also in the growth of snakes can also be very rapid in nature. Species of
size of the neonate and the amount of embryonic yolk that snakes living in warmer climates more than double in
remains to help fuel its metabolism. Newborn snakes that length during the first year of life and may achieve sexual
contain some residual embryonic yolk can grow in length maturity within one to two years. In some elapid species of
without feeding for variable periods of time, depending on snakes that were studied by Richard Shine, females first
the amount of yolk that is present at birth. It is the pres- mated at one year of age. Relatively early sexual maturation
ence of residual embryonic yolk that permits some snakes appears to be common among the Elapidae as well as some
that are born in the late summer to make it through their colubrid snakes, and many species will mate within the first
first winter without feeding if they happen to have bad luck one to three years after birth. In contrast, species of snakes
in finding food during their very early life. that live in colder climates (either at higher latitudes or
Eventually young snakes begin feeding, and the rates of higher altitudes) grow and reach sexual maturation more
growth that are achieved depend on the genetic constitu- slowly. For example, growth rates in colubrid and viperid
tion of the individual, the availability of heat and water in species living in colder climates are roughly half the rate of
its environment, and the success of the snake in capturing species living in warmer, tropical environments. Sexual
and digesting prey. There is considerable variation in rates maturation in the former species may require four to nine
of growth and sexual maturation among snakes, and the years. Viperid snakes as a group tend to exhibit “delayed”
differences are not always based in the “hard-wiring” of ge- sexual maturity, as do freshwater file snakes (Acrochordus
netic limitations. Rates of growth in captive snakes can ex- arafurae). In the latter species, males mature at five years
ceed those of the same species in nature because of the and females mature at seven years. Regardless of the envi-
constant availability of food and water. However, there are ronment, male and female snakes characteristically achieve
situations in which growth rates that are achieved in the sexual maturity at different times; females are generally
wild are similar to those of captive snakes. The rate of later than males by several months to a full year or more.
growth in snakes is indeed flexible, being determined partly Growth of snakes is more rapid during the early years
by genes and partly by the environment in which the nutri- of life and is generally most rapid during the first one to
tion of an individual is based. Within a species, the growth two years. This fact has great significance because smaller
of individuals can vary depending on the quality of habitat, snakes are generally more vulnerable to predation and to
the availability of resources, variation in weather patterns, death from other causes (such as dehydration). Also, growth
sex, and other attributes of morphology and physiology is required for snakes to reach sexual maturity. Research of
that can vary among individual animals. wild snake populations has documented repeatedly that
The growth and maturation of snakes also depend on the growth is faster, and survivorship lower, in younger snakes
size of the individual at birth, and generally larger species compared with older individuals. In some sea snakes, only
of snakes produce larger offspring. However, in many spe- 10–20 percent of neonates survive their first year, and only
cies of snakes in which the adult size is small, offspring are 6 percent of the females live to reproduce.
proportionately larger (relative to the size of adults) than Snakes continue to grow as adults, unlike many species
are those of larger species. This also is true among some of mammals. However, the rates of growth slow consider-
other animals such as certain lizards, birds, and mammals. ably as a snake ages, and larger snakes that are near their
Thomas Madsen, Richard Shine, and others have also found maximum size grow very slowly, or negligibly. Typically,
that young snakes growing with relative rapidity during the growth rates decline markedly when snakes reach sexual
first year of life because of a favorable abundance of prey maturity, likely as a result of increasing energy investment
continue to grow more rapidly than average during their to structures and behaviors that are related to reproduction
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(rather than growth). The energy demands for reproduction size, suggesting there is a lack of a “threshold” effect on the
can be quite different between the sexes. For the multiple behavior. Rather, increasing degrees of burdening due to
reasons discussed here, length is not a reliable indicator of egg development render foraging less productive and in-
age, and it is difficult to compare the growth rates among creasingly risky in relation to predators.
species if one uses a single metric for comparison. As a very
rough generalization, most snakes are likely to achieve
nearly half of their maximum body length during the first Snakes and the Future
three to four years of growth, including larger species such It seems fitting in this chapter to add a concluding com-
as pythons that grow to lengths of several meters or longer ment about the future of snakes. Indeed, this topic is tied
(see chapter 1). closely to the future of the world as it relates to impacts of
The longevity of snakes tends to fall in between that of human population, technology, and climatic changes. Like
lizards and turtles. Snakes in captivity tend to live from 10 many other vertebrates, snakes are documented to be in de-
to 20 years, with some aging up to 30+ years. A Ball Python cline, and the phenomenon appears to be global. What is
in the Philadelphia Zoo lived to be a little older than 47 further alarming is the impression in some parts of the
years. Demographic studies of snakes have shown that life world that the numbers of snakes are decreasing not only
spans in the wild may be similar to that in captivity, with where human presence offers obvious causes, but also in
maxima ranging typically between 15 and 30 years. Olive relatively pristine regions where there appears to be little,
Sea Snakes on the Great Barrier Reef live to about 15 years. or no, direct human impact. The reasons might relate in
various places to the indirect influence of invasive (intro-
Snakes on Islands duced) wildlife, effects of atmospheric pollutants or radia-
Studies of reproduction in snakes that live on islands are tion, climatic changes, or the subtle collapse of trophic
interesting because of the nature of resources, which can be systems. Of course, there could be unknown single or mul-
limited, ephemeral, or literally “boom or bust.” Clutch size tiple effects of which we are totally unaware.
and/or the mass of a young snake are significantly greater As long as appropriate habitat remains, I think that some
during years when prey resources are more abundant and species of snakes will survive even amid broad-scale reduc-
when females have a better condition of energy storage for tions in other forms of wildlife. Smaller burrowing species,
the production of young. In snakes generally, however, the for example, might remain prevalent in suburban areas or
relations between variation of resources and reproduction even cities, and aquatic species might persist in bodies of
are complex, and measures of reproductive output can bear water across varied landscapes. Some species might even
little relationship to the costs of reproduction in a given thrive in agricultural landscapes, whereon a food base of ro-
system. Assuming that resources are adequate or “normal,” dents tends to thrive. And there is an important question
other factors can intervene to reduce the reproductive out- regarding human impact that begs for more research. Do
put of a female. In many species of snakes reproduction is certain snake species become increasingly rare because of
associated with a decrease in the feeding rates of females, reduced numbers in the population, or is the rarity due
and gravid females may even exhibit anorexia! Such an- (perhaps in part) to a “switching” of behavior to more secre-
orexic females may not easily survive after parturition tive habits when encounters with humans increases?
owing either to starvation and depletion of energy reserves, What does appear certain is that larger, more spectac-
or to being susceptible to predation. ular species will disappear from landscapes where human
Various interpretations of this phenomenon have identi- impact is a dominant force. Loss of habitat, direct killing
fied several advantages of females not feeding. These include upon highways and roads, predatory losses to dogs and cats
easier and more careful thermoregulation by females, which that accompany human inhabitants in increasing numbers,
can also move more easily without prey in the digestive use of chemical pesticides, reduction in food base (frogs, for
tract. Locomotion can already be physically constrained example), and of course direct killing by humans all act with
due to the bodily distension from oviductal eggs. François multiplicity to reduce the numbers of snakes that are pre-
Brischoux and several coworkers have investigated the re- sent in a given area. Despite many years of education re-
production of sea kraits (Laticauda spp.) on some islets at garding the place and value of snakes, far too many people
New Caledonia. They report that female snakes cease feeding still have misconceptions about snakes, fear them irratio-
as their eggs develop, seemingly because the distension of nally, and will kill one at each opportunity. This may be es-
the body tends to impede locomotion. Therefore, these fe- pecially true in rural areas, where people tend to kill snakes
males would be less effective in movements and more vul- or, at best, want them removed from their property. I con-
nerable to aquatic predators if they continued to feed. The trast this with a personal impression I have that many Aus-
feeding rate decreases progressively with increasing follicle tralians are well educated and tolerant of snakes, even
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though numerous species they encounter are venomous. It I. Seasonal levels and interplay between steroid hormones
seems to me that Australians have learned to live with and vasotocinase. General and Comparative Endocrinology
139:143–150.
snakes being present in their surroundings, at least in com-
Andren, C., and G. Nilson. 1983. Reproductive tactics in an island
parison with some other cultures. I emphasize this is a population of adders, Vipera berus (L.), with a fluctuating food
strong impression that is based in my personal experiences, resource. Amphibia-Reptilia 4:63–79.
and not a statistically tested statement. Blackburn, D. G. 1998. Structure, function, and evolution of the
As one example, I knew an Australian couple who had oviducts of squamate reptiles, with special reference to vivi-
two children and lived in a rural setting. They not only tol- parity and placentation. Journal of Experimental Zoology
282:560–617.
erated, but in fact quite enjoyed, the presence of a Red-
Blackburn, D. G. 2006. Squamate reptiles as model organisms
bellied Black Snake (Pseudechis porphyriacus), which on for the evolution of viviparity. Herpetological Monographs
some mornings sunned itself on an open porch that was 20:131–146.
attached to the house. This snake had been given a name, Blackburn, D. G., K. E. Anderson, A. R. Johnson, S. R. Knight, and
as was a goanna that also appeared on somewhat regular G. S. Gavelis. 2009. Histology and ultrastructure of the pla-
cental membranes of the viviparous Brown snake, Storeria
occasion. The snake was part of the natural environment
dekayi (Colubridae: Natricinae). Journal of Morphology
that was both noticed and appreciated by the family. On 270:1137–1154.
the other hand, I cannot imagine many folks in Florida Brischoux, F., X. Bonnet, and R. Shine. 2010. Conflicts between
who would tolerate such presence of an Eastern Diamond- feeding and reproduction in amphibious snakes (sea kraits,
back Rattlesnake (Crotalus adamanteus). The first response Laticauda spp.). Australian Ecology 36: 46–52.
would likely be to kill the animal and remove it from the Burns, G., and H. Heatwole. 2000. Growth, sexual dimorphism,
and population biology of the olive sea snake, Aipysurus laevis,
property. There are exceptions to this statement, of
on the Great Barrier Reef of Australia. Amphibia-Reptilia
course. 21:289–300.
So I appeal to the readers of this book to please share Crews, D., and W. Garstka. 1982. The ecological physiology of re-
some of your excitement about the biology of snakes— production in the Canadian red-sided garter snake. Scientific
what they do and how they live—with others, especially American 247:159–168.
Ford, N. 1986. The role of pheromone trails in the sociobiology of
children. I believe that most people are fundamentally cu-
snakes. In D. Duvall, D. Mueller-Schwarze, and R. Silverstein
rious about snakes, especially if they have not been taught (eds.), Chemical Signals in Vertebrates 4. New York: Plenum
to fear them. This reminds me also to entreat filmmakers to Press, pp. 261–278.
show people the many fascinating behaviors of snakes and Gillingham, J. 1987. Social behavior. In R. Seigel, J. Collins, and
to avoid the all-too-common tendency to feature snakes S. Novak (eds.), Snakes: Ecology and Evolutionary Biology. New
predominantly in defensive postures or attitudes, which York: McGraw-Hill, pp. 211–217.
Greene, M., and R. Mason. 2000. Courtship, mating, and male
gives viewers the wrong impression that a snake is always
combat of the brown tree snake, Boiga irregularis. Herpetologica
ready to attack and to harm you. If people change their be- 56:166–175.
haviors and cease to kill snakes, we will come a long way Kubie, J., A. Vagvolgyi, and M. Halpern. 1978. Roles of the vomero-
toward preserving and appreciating environments in which nasal and olfactory systems in courtship behavior of male gar-
rich and varied wildlife entertain the senses and evoke ter snakes. Journal of Comparative Physiology and Psychology
92:627–641.
imagination. Remember there is nothing more practical
LeMaster, M., and R. Mason. 2002. Variation in a female sexual
and edifying than to learn about the world around you. For attractiveness pheromone controls male mate choice in garter
many, one or more species of snakes will be an important snakes. Journal of Chemical Ecology 28:1269–1285.
part of that world. Together we will celebrate each time a Lillywhite, H. B. 1985. Trailing movements and sexual behavior in
snake is born. Coluber constrictor. Journal of Herpetology 19:306–308.
Luboschek, V., M. Beger, D. Ceccarelli, Z. Richards, and M. Pratchett.
2013. Enigmatic declines of Australia’s sea snakes from a biodi-
Additional Reading versity hotspot. Biological Conservation 166:191–202.
Aldridge, R., A. Bufalino, and A. Reeves. 2005. Pheromone com- Lutterschmidt, D. I., and R. Mason. 2009. Endocrine mechanisms
munication in the watersnake, Nerodia sipedon: A mechanistic mediating temperature-induced reproductive behavior in red-
difference between semi-aquatic and terrestrial species. Ameri- sided garter snakes (Thamnophis sirtalis parietalis). Journal of
can Midland Naturalist 154:412–422. Experimental Biology 212:3108–3118.
Aldridge, R. D., and D. M. Sever (eds.). 2011. Reproductive Biology Madsen, T., and R. Shine. 1993. Costs of reproduction in a popula-
and Phylogeny of Snakes. Vol. 9 of Reproductive Biology and tion of European adders. Oecologia 94:488–495.
Phylogeny, B. G. M. Jamieson, series editor. Enfield, NH: Sci- Mason, R. T., and M. R. Parker. 2010. Social behavior and phero-
ence Publishers. monal communication in reptiles. Journal of Comparative Phys-
Almeida-Santos, S. M., F. M. F. Abdalla, P. F. Silveira, N. Yama- iology A196:729–749.
nouye, M. C. Breno, and M. G. Salomão. 2004. Reproduc- Mason, R., H. Fales, T. Jones, L. Pannell, J. Chinn, and D. Crews.
tive cycle of the neotropical Crotalus durissus terrificus: 1989. Sex pheromones in snakes. Science 245:290–293.
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Mason, R., T. Jones, H. Fales, L. Pannell, and D. Crews. 1990. Char- Shine, R. 1992. Relative clutch mass and body shape in lizards and
acterization, synthesis, and behavioral responses to sex attrac- snakes: Is reproductive investment constrained or optimized?
tiveness pheromones of red-sided garter snakes (Thamnophis Evolution 46:828–833.
sirtalis parietalis). Journal of Chemical Ecology 16:2353–2369. Shine, R. 1994. Sexual size dimorphism in snakes revisited. Copeia
Mullin, S. J., and R. A. Seigel (eds.) 2009. Snakes: Ecology and Con- 1994:326–346.
servation. Ithaca, NY: Cornell University Press. Shine, R. 2003. Reproductive strategies in snakes. Proceedings
Parker, M., and R. Mason. 2009. Low temperature dormancy af- Royal Society London B 270:995–1004.
fects the quantity and quality of the female sexual attractive- Shine, R. 2005. All at sea: Aquatic life modifies mate-recognition
ness pheromone in red-sided garter snakes. Journal of Chemical modalities in sea snakes (Emydocephalus annulatus, Hydrophi-
Ecology 35:1234–1241. idae). Behavioral Ecology and Sociobiology 57:591–598.
Parker, W. S., and M. V. Plummer. 1987. Population ecology. In R. Shine, R., and X. Bonnet. 2009. Reproductive biology, population
A. Seigel, J. R. Collins, and S. S. Novak (eds.), Snakes, Ecology viability, and options for field management. In S. J. Mullin and
and Evolutionary Biology. New York: Macmillan, pp. 253–301. R. A. Seigel (eds.), Snakes, Ecology and Conservation. Ithaca, NY:
Reading, C. J., L. M. Luiselli, G. C. Akani, X. Bonnet, G. Amori, J. Cornell University Press, pp. 172–200.
M. Ballouard, E. Filippi, G. Naulleau, D. Pearson, and L. Rugie- Shine, R., B. Phillips, H. Wayne, M. LeMaster, and R. Mason. 2003.
ro. 2010. Are snake populations in widespread decline? Biology Chemosensory cues allow courting male garter snakes to as-
Letters 6:777–780. sess body length and body condition of potential mates. Behav-
Rigley, L. 1971. “Combat dance” of the black rat snake, Elaphe o. ioral Ecology and Sociobiology 54:162–166.
obsoleta. Journal of Herpetology 5:65–66. Shine, R., J. Webb, A. Lane, and R. Mason. 2005. Mate location
Ross, P., and D. Crews. 1977. Influence of the seminal plug on mat- tactics in garter snakes: Effects of rival males, interrupted
ing behaviour in the garter snake. Nature 267:344–345. trails and non-pheromonal cues. Ecology 19:1017–1024.
Schuett, G. W., S. Carlisle, A. Holycross, J. O’Leile, D. Hardy, E. Van Slip, D. J., and R. Shine. 1988. The reproductive biology and mating
Kirk, and W. Murdoch. 2002. Mating system of male Mojave system of diamond pythons, Morelia spilota (Serpentes: Boi-
rattlesnakes (Crotalus scutulatus): Seasonal timing of mating, dae). Herpetologica 4:396–404.
agonistic behavior, spermatogenesis, sexual segment of the Stewart, J. R., and K. R. Brasch. 2003. Ultrastructure of the placen-
kidney, and plasma sex steroids. In G. W. Schuett, M. Hoggren, tae of the natricine snake, Virginia striatula (Reptilia: Squama-
M. Douglas, and H. Greene (eds.), Biology of the Vipers. Eagle ta). Journal of Morphology 255:177–201.
Mountain, UT: Eagle Mountain Publishing, pp. 515–532. Sun, L.-X., R. Shine, D. Zhao, and T. Zhengren. 2002. Low costs,
Shine, R. 1985. The evolution of viviparity in reptiles: An ecological high output: Reproduction in an insular pit-viper (Gloydius
analysis. In C. Gans and F. Billett (eds.), Biology of the Reptilia, shedaoensis, Viperidae) from north-eastern China. Journal of
vol. 15. New York: John Wiley, pp. 606–694. Zoology 256:511–521.
Shine, R. 1988. Constraints on reproductive investment: A com- Tinkle, D. W., and J. W. Gibbons. 1977. The distribution and evolu-
parison between aquatic and terrestrial snakes. Evolution tion of viviparity in reptiles. Miscellaneous Publications of the
42:17–27. Museum of Natural History, University of Michigan 154:1–55.
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GLOSSARY OF TERMS
abduction (v. abduct). Movement of a part away from the alimentary canal. See gastrointestinal tract.
medial axis or plane of the body, or movement of two allantois. See extraembryonic membranes.
parts away from each other. Cf. adduction.
allele. Shorthand form of allelomorph, representing one of a
acclimation. A reversible change in morphology, behav- number of possible alternate heritable forms of a given gene.
ior, or physiology that occurs in response to a prolonged
change in the condition of a laboratory environment allometry. Changes in the relative proportion of a body
(e.g., temperature). Cf. acclimatization. part in relation to the rate of growth of the whole body,
or another body part, as total body size increases. Such
acclimatization. A reversible change in morphology, changes can be either positive or negative.
behavior, or physiology that occurs in response to a pro-
alpha (α) keratin. See keratin.
longed change in the condition of the natural environ-
ment (e.g., temperature). Cf. acclimation. ambush forager. Reference to an animal that remains
sedentary for periods, usually in strategic locations, and
accommodation. The eye’s action or ability to bring an
waits for prey to come within capture distance.
object into focus.
amelanistic partial albinism. A condition where skin
acetylcholine. An important neurotransmitter in many
color lacks melanin, but other pigments are present to
different types of neurons, having actions on the heart,
impart some, or partial, color.
smooth muscle of blood vessels, and the activation of
muscle at neuromuscular junctions. amnion. See extraembryonic membranes.
action potential. A nerve “impulse” or propagated bio- androgen. A class of sex steroid hormones that stimulate
electric change in a nerve membrane. This is the unit of male characteristics and promote protein synthesis. In
signaling in the nervous system. female reptiles, androgens can be converted in the cen-
tral nervous system to estrogens or other steroids. This
active forager. An animal that moves through its envi- also occurs in males.
ronment actively searching for potential prey.
ankylosis. A rigid union between two parts, usually with
adduction (v. adduct). Movement of a part toward the reference to attachment between teeth and bone by hard
medial axis or plane of the body, or movement of two mineralized tissue.
parts together. Cf. abduction.
aorta. See dorsal aorta.
aglyph (adj. -ous). A snake in which teeth lack a groove or
aortic arches. Two (right and left) outflow vessels of the
canal, therefore unable to transport venom effectively.
ventricle, which convey systemic blood and join to form
air sac. See tracheal air sac. the dorsal aorta.
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apical pit. A sense organ recessed in a small depression the boundary. This region is responsible for frictional
usually on the posterior tip of the dorsal scales of cer- drag of moving objects.
tain reptiles, particularly snakes. Little is known about
brille. See spectacle.
the function of these structures.
buoyancy. The tendency to float or sink in a fluid environ-
apnea. Breath-hold; cessation of breathing.
ment, water or air.
aposematism (adj. aposematic). Reference to charac-
button. The first permanent and distal segment on the rat-
ters, especially coloration, that advertises an organism
tle of a rattlesnake, the prebutton being lost at the first
as dangerous or unpleasant to potential predators.
ecdysis.
arteriole. A smaller artery that immediately precedes cap-
cantilever. A projecting beam or body that is supported at
illaries.
only one end.
artery. A blood vessel that conveys generally well-oxygenated
capillary (pl.-ies). The smallest (microscopic) blood ves-
blood from the heart to tissues. Pulmonary arteries con-
sels that are lined by a highly permeable endothelium
vey relatively deoxygenated blood to the lung. Cf. vein.
and exchange gases and chemical substances with tis-
ATP. Adenosine triphosphate, an energy-rich nucleotide sues through which they pass.
used as a common energy currency in all living cells.
cardiac. Reference to the heart.
atrioventricular valves. Valves separating and regulat-
cardiac output. The volume rate of blood outflow from the
ing the flow of blood from the atria to ventricle of the
heart, expressed as volume of blood leaving the ventricle
heart.
per time. In snakes with a single ventricle, it is best to
atrium (pl. atria). One of the receiving chambers of the specify the cardiac outflow as systemic, pulmonary, or
heart, filling with blood returning from veins and emp- total.
tying to the ventricle.
cardiovascular system. See circulation.
baroreceptor. A sensory receptor that is stimulated by
catecholamines. A group of molecules that act as neu-
changes in pressure. Typically, this term refers to re-
rotransmitters and hormones, including epinephrine and
ceptors in the walls of central blood vessels where they
norepinephrine. These play important roles in accelerat-
detect stretch or distension of the vessel wall due to in-
ing the heart and constricting blood vessels in the car-
creased blood pressure.
diovascular system.
basal. Reference to the earliest lineage, or early lineages,
in a phylogeny. The internal nodes of a phylogeny in con- caudocephalic wave. A horizontal undulating wave of
trast with terminal branches. the body that results in gentle body contacts between
a female snake and a courting male that produces the
basilar membrane. The delicate strand of elastic tissue movement while lying beside or upon her. The undula-
bearing the auditory hair cells in the inner ear. tion characteristically moves from posterior to anterior
behavioral thermoregulation. Regulation of body tem- and is thought to stimulate mating.
perature attributable to behaviors of an animal that con- cavum arteriosum. One of three cavities in the single
trol its interactions with environmental heat sources. ventricle of noncrocodilian reptiles, which receives
See thermoregulation. oxygenated blood from the left atrium but has no direct
beta (β) keratin. See keratin. connection to an outflow tract.
binocular vision. Overlapping visual fields involving two cavum pulmonale. One of three cavities in the single ven-
eyes, such that images are focused on both of two retinas tricle of noncrocodilian reptiles, which lies on the left
simultaneously and thereby enhance the perception of side of the vertical septum and conveys blood into the
depth and distance. pulmonary outflow tract.
body wall. The part of the animal body that encloses the cavum venosum. One of three cavities in the single ventri-
internal body cavity. cle of noncrocodilian reptiles, which lies to the right side
of the vertical septum and conveys blood to the systemic
boundary layer. A layer of fluid (air or water) adjacent to
aortic arches.
a physical boundary or surface, in which motion of the
fluid is affected by the boundary and exhibits a mean ve- centrifugal. Acting in a direction outward from a center
locity that is less than the free stream velocity away from of rotation.
214 | Glossary of Terms
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character, or character state. Reference to an observ- color polymorphism. See polymorphism.
able phenotypic property or trait of an organism. It
columella. The auditory ossicle (bone or cartilaginous ele-
represents the particular condition or expression of a
ment) that crosses the middle ear cavity and transmits
feature that might have variable expressions in different
sound or vibrational stimuli from the surrounding tis-
organisms.
sues of the head (in snakes) to the oval window and fluid
chorioallantois, chorioallantoic membrane. An extrae- of the inner ear.
mbryonic membrane formed by union of the chorion
combat dance. A challenge behavior between two male
and allantois (see extraembryonic membranes).
snakes, usually of the same species, involving vertical
chorion. See extraembryonic membranes. postures, intertwining of bodies, and pushing of the op-
chromatophore. A generalized term for a cell that con- ponent in attempt to force the individual to the ground.
tains pigment and imparts color to skin. Such behavior occurs typically during the mating season
of the species involved.
chyme. Partially digested food (also called digesta) in the
form of a liquefied mass after it enters the intestine. concertina locomotion. A mode of locomotion in snakes,
characterized by sequential extension and contraction
circadian rhythm. A cycle of behavior or physiologi- of the body from one anchored or stationary site to the
cal process that is repeated daily on a 23–25 h interval next as the animal moves with accordion-like appear-
(roughly one day), attributable to an “internal clock” but ance in one direction.
synchronized to time-related factors in the environment.
cone. A photoreceptor in the retina, functioning in bright
circulation (also blood circulation, cardiovascular light and differentially sensitive to light of different
system, transport system) The heart and blood ves- wavelengths (thus imparting color vision). Cf. rod.
sels, which in aggregate move blood throughout the
body. The pulmonary circulation transports blood to and contact zone. See resistance site.
from the lungs (where it becomes oxygenated), and the conus arteriosus. A thickened part of the amphibian
systemic circulation transports blood to and from all the heart between the ventricle and distributing vessels of
other body tissues. the systemic and pulmonary circulations. This structure
clade. A monophyletic lineage of organisms. A single species is not present in reptiles.
and its descendants, representing a distinct branch on a convection. The mass transfer of heat or matter due to
phylogenetic tree. bulk transport in a moving fluid (gas or liquid).
clear layer. A term given to the innermost living cells of convergence, convergent character. Reference to
an outer epidermal generation during skin shedding of homoplasy or the independent evolution of similar
squamates. character states in unrelated lineages, usually attrib-
cloaca. The common chamber and passageway where re- utable to similar selection pressures associated with
productive, urinary, and digestive ducts or canals re- similarity of one or more common features of the
lease their contents. This chamber receives feces from environment.
the large intestine and voids its contents to the exterior copulatory plug. See seminal plug.
through the vent or cloacal opening.
cornea. The transparent surface covering the iris and pupil,
cloacal pop, popping. Rapid extrusion and retraction of through which light passes as it enters the eye.
the cloaca, which results in the rapid expulsion of air
corneous, cornified. Descriptive of keratinized epithe-
from the vent in certain North American snakes. The ac-
lium, as the stratum corneum of the epidermis.
tion produces a clearly audible popping sound while the
tail is held aloft as a defensive action. corpus luteum (pl. corpora lutea). The remnants of a
ruptured egg follicle following ovulation, which secrete
clutch size. The collective number of eggs that are ovu-
relatively large volumes of progesterone until late preg-
lated and laid by a single female at one time. Cf. litter
nancy in viviparous reptiles.
size.
costocutaneous muscles. The muscles that run between
coefficient of friction. A dimensionless value that de-
the ribs and overlying skin of snakes.
scribes the ratio of the force of friction between two bodies
and the force pressing them together. This value is an em- cranial kinesis. Movements between parts of the skull,
pirical measurement that is determined experimentally. usually in contexts related to feeding of snakes.
Glossary of Terms | 215
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critical thermal maximum (pl. -a) (CTMax). The tem- the relative movement of fluid and opposite to the direc-
perature at which a species, when heated gradually, be- tion of movement.
comes incapacitated such that long-term survival is not ecdysis. The shedding or sloughing of the stratum corneum
possible at this or higher temperatures. of the epidermis, which periodically renews the outer
critical thermal minimum (pl. -a) (CTMin). The tem- covering of the skin.
perature at which a species, when cooled gradually, be- ectothermy (adj. ectothermic). Reference to an animal
comes incapacitated such that long-term survival is not that depends on external heat sources to regulate body
possible at this or lower temperatures. temperature. Cf. endothermy.
crypsis, cryptic. A condition of being camouflaged; eggshell. The shell or outer covering of an egg, consist-
concealed. ing of fibers and variable amounts of calcium carbonate
defensive strike. A strike made by a snake as a defensive crystals.
movement to thwart a potential predator. Cf. predatory electromyography. The recording (and study) of electrical
strike. activity of muscles.
derived, or derived character. Reference to a more re- endocrine (adj. or n.) Secreting (chemical messengers)
cent character or feature that departs from the ancestral into the blood circulation. See hormone.
condition in a lineage. Opposite to primitive.
endothermy (adj. endothermic). Reference to organisms
dermis. The inner layer of skin beneath the epidermis, (e.g., birds, mammals) wherein regulated body tempera-
containing fibrous connective tissue, blood vessels, ture is attributable largely to internal heat production
nerves, and chromatophores. arising from relatively high rates of energy metabolism.
diagnostic character. A specific character state that dis- Cf. ectothermy.
tinguishes unambiguously one species or clade of organ- endurance. The ability of an organism to exert itself and to
isms from another. move or remain active for a long period of time.
diapsid. Reference to a reptilian skull in which there are epaxial muscles. Muscles of the trunk that lie, or origi-
two temporal, or postorbital, openings. nate, dorsal to the vertebral column or body axis.
diastole. Relaxation of muscles of the ventricle while fill- epidermal generation. A unit of lepidosaurian epidermis
ing with blood from the atria, prior to contraction. Cf. that is periodically formed and shed in ecdysis. A com-
systole. plete, mature generation of epidermis when superficial
dietary water. Preformed water that is present in the food in position just before it is shed to the environment is
that an animal consumes. called an outer epidermal generation. During renewal
of the epidermis during the shedding cycle, the newly
diffusion. Movement of atoms, molecules, or ions as a re-
forming unit, lying beneath the outer generation that is
sult of random thermal motion from a region of higher
about to be shed, is called the inner epidermal generation.
to lower concentration.
epidermis. The outer layer of skin of a vertebrate, overly-
digesta. See chyme.
ing the dermis. The epidermis contains the stratum cor-
digestive tract. See gastrointestinal tract. neum and living cells having the capacity to form keratin.
diverticulum (pl. -a). A circumscribed pouch or sac. epididymis. The largely convoluted tubule that drains the
dorsal aorta. The principal systemic blood vessel that con- efferent ducts of the testis into the urethra. This struc-
veys blood to the body tissues posterior to the heart, ture lies at the surface of the testis and functions to store
formed by the union of the right and left aortic arches. sperm until they are released to the exterior.
epinephrine. See catecholamines.
down-regulation. Control of a physiological activity by a
decrease in receptor density in a target cell membrane. esophagus. The region of the gut located between the
Cf. up-regulation. mouth and stomach, functioning to transport ingested
food to the region of digestion.
drag. The resistance to movement of an object through a
fluid, which increases with the viscosity and density of estrogens. A family of sex steroids synthesized primarily
the medium and varies with the shape and surface area in the ovary, but some are produced in the adrenal cor-
and properties of an object. A drag force acts parallel to tex, brain, and testis. These hormones play a central role
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in stimulating the female system during reproductive Sliding friction is the force that has to be overcome in or-
cycles and the development of secondary sexual charac- der to keep one of two contacting objects moving at a
teristics. They also function to prepare the reproductive constant velocity.
system for fertilization, and are essential for vitellogen- frontal. Of, or pertaining to, the front of the head or skull
esis and egg development. of an animal, especially the large and prominent dermal
evaporative cooling. Removal of body heat attributable bone on the dorsal roof of the skull, lying between the
to evaporation of water, whether passive or actively en- eye orbits.
hanced by panting. fusiform. Spindle-shaped, with tapering toward each end.
exhalation. See expiration. gas exchange. In context of physiology, the exchange of
expiration. Active or passive movement of air out of respiratory gases (O2 and CO2) between an organism and
the lung (to the external environment). Exhalation. Cf. its environment.
Inspiration. gas exchanger. Any permeable organ that exchanges res-
external respiration. See ventilation. piratory gases with the environment: lung, gills, or skin.
extraembryonic membranes. Structures formed around gastric glands. Glands in the wall of the stomach that se-
the embryo that eliminate wastes (allantois), provide crete mucus, acid, and proteolytic enzymes.
food (yolk sac) and oxygen, and protect the embryo (am- gastrointestinal tract. A hollow, tubular cavity extending
nion and chorion). through an animal and open at both ends. This structure
eyecap. See spectacle. functions in ingestion, digestion, and absorption of food
materials. Also called alimentary canal, digestive tract, or
facial pit. See pit organ. simply gut.
facultative endothermy. Endothermic heat production genetic drift. Evolutionary change due to random fluctua-
by an animal that is not obligatory, but may or may not tions of gene frequencies, independent of selection and
occur depending on circumstances. most evident in small populations.
fang. A grooved or tubular tooth that is used to inject genotype. The genetic makeup of an individual, which
venom. along with other factors such as the environment deter-
fascia. A band of connective tissue that forms a sheath, as mines the organism’s phenotype. Cf. phenotype.
around a muscle or blood vessel. gliding. A form of aerial locomotion involving largely pas-
faveolus (pl.-i). A functional unit of reptilian lung parenchy- sive but controlled movement through air. In snakes, a
ma, consisting of an individual membranous compartment flattened body is used as an airfoil to reduce the angle of
bounded by neighboring units in the form of a honeycomb. descent after launching from an elevated site.
fenestra (pl.-ae). A large opening, usually within or be- glottis. The opening from the pharynx (throat) to the tra-
tween bones. chea or larynx.
fitness. The ability of an organism to contribute its genes glycolysis (adj. glycolytic). Pertaining to the enzymatic con-
to the next generation; roughly expressed as the number version of glucose to the simpler compound of lactate (or
of offspring contributed to the next generation weighted pyruvate), resulting in production of energy as ATP with-
by the probability of surviving to reproduce. out a requirement for oxygen. This constitutes the princi-
pal route of carbohydrate breakdown and oxidation and is
flow. Movement of fluid, or the quantity of fluid moving,
an important aspect of activity metabolism in snakes (and
usually expressed as volume per time.
other reptiles) that utilize glycolysis for ATP production in
footplate. The expanded base of the columella providing muscle during short but intense bursts of activity.
contact with the oval window of the inner ear.
gonad. A reproductive organ in which either eggs (ovary)
foramen. A hole or opening that allows passage through a or sperm (testis) are produced. The ovary or testis is a pri-
tissue wall. mary sexual character.
friction. Mechanical resistance to relative motion between gonadotropin, gonadotropic hormone. Hormones that
two solid surfaces that are in contact. Static friction is the influence the activity of the gonads, particularly those
force that has to be overcome in order to induce forward secreted by the anterior pituitary-follicle stimulating
motion of an object along a surface that it contacts. hormone and luteinizing hormone.
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gonadotropin-releasing hormone. A hormone secreted horizontal undulatory progression. See lateral undulation.
from the hypothalamus and which stimulates the release hormone. A chemical messenger that is secreted into the
of gonadotropins from the pituitary. blood circulation or intercellular space and affects target
gravitational pressure. The component of pressure in tissues. Cf. endocrine.
a fluid that is attributable to gravity. Also called hydro- hydrophobic. Repelling water; nonwettable.
static pressure.
hydrostatic indifferent point. That point in a con-
gut. See gastrointestinal tract. tained horizontal fluid where the pressure does not
hair cells. Mechanosensory epithelial cells bearing minute change when the contained volume (say a tube) is tilted
hairlike structures that are bent by sound or vibrational upright.
stimuli, which alters the membrane properties and creates hydrostatic pressure. See gravitational pressure.
bioelectric “signals” that are transmitted to the auditory
nerve. These cells are arrayed along the basilar membrane hypothalamus. That part of the brain that forms the floor
of the inner ear. of the median (third) ventricle.
harmonic. In bioacoustics, an overtone whose frequency inertia. The tendency of an object to remain at rest or in
is an integral multiple of a fundamental frequency. uniform motion in a straight line unless acted upon by
external forces.
head pits. Structures similar to apical pits and having vari-
inhalation. See inspiration.
able appearances and distribution on the head scales of
snakes. Also called parietal pits. inner ear. The internal part of the ear, comprising a senso-
ry organ responsible for balance and equilibrium sense
heart. The central muscular pump of the cardiovascular
in addition to the sense of hearing.
system, consisting of two atria and a single ventricle in
snakes. inner epidermal generation. See epidermal generation.
heart rate. The frequency of heart contractions that pro- inspiration. Active movement of air into the lung. Inhala-
vide the force to move blood through the circulation. tion. Cf. expiration.
Heart rate is typically measured as the number of heart- integument. A covering. The skin and its derivatives.
beats (or contraction cycles) per time.
interaortic foramen. A small opening between the left
hematocrit. The percentage of total blood volume occu- and right aortic arches, located at their base near the
pied by red blood cells, typically measured in a sample ventricle.
of whole blood.
interstitial fluid. Liquid within the spaces surrounding
heme. The ringlike molecular component of hemoglobin (outside of) cells, generally similar to blood plasma but
containing iron that is responsible for binding oxygen with lower content of protein.
within a structural surrounding of carrier protein.
interventricular canal. A space within the ventricle of non-
hemipenis (pl.-es). Either of paired copulatory organs ly- crocodilian reptiles that allows communication (flow of
ing in a cavity at the base of the tail in squamate reptiles. blood) between the cavum arteriosum and cavum venosum.
hemoglobin. The pigment inside red blood cells responsi- intracardiac shunt. See shunt.
ble for the reversible binding and transport of oxygen.
iridescent color. Bright and changing color attributable to
hemotoxic. A property of snake venoms that impairs blood reflection due to structural properties of a surface (and
vessels and lymphatic vessels. not due to pigments).
hertz (Hz). Cycles per second (a derived unit of frequency). iris. A muscular disc with a contractile hole situated in
hinge. The softer, pliable region of skin between overlap- front of the eye lens that acts as an adjustable aperture.
ping scales of reptiles, especially squamates. Jacobson’s organ. See vomeronasal organ.
homology. Similarity of characters due to common ancestry. keeled scale. A scale that bears a prominent central keel
homoplasy, homoplastic. Reference to similarity of char- or protruding midline, detectable by touch or by eye. Cf.
acter states, or function, attributable to convergent or smooth scale.
parallel evolution and not due directly to inheritance keratin. A hard or tough, fibrous, nonsoluble protein
from common ancestry. produced by the epidermis and forming the outermost
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stratum corneum. Alpha (α) keratin consists of helical, litter size. The collective number of animals that are born
hairlike molecules, whereas beta (β) keratin is a pleated at one time in a viviparous species. Cf. clutch size.
sheet and feather-like. The latter is more rigid and gener- loreal pit. See pit organ.
ally tougher than is alpha keratin.
lymph, lymphatic fluid. Clear plasma-like fluid that is
keratinocyte. An epidermal cell that has capacity to syn- carried in lymphatic vessels.
thesize keratins.
mandibular raking. An unusual feeding mechanism in
kinematics. The study of animal motion, its course and which the tooth-bearing elements of the lower jaw rotate
patterns. synchronously in and out of the mouth, thereby drag-
kinesis. Generally, reference to physical movement. This ging prey into the esophagus. This has been described in
word is descriptive of movements between parts of the small, burrowing thread snakes.
skull (cranial kinesis), usually in contexts related to feed- mating ball. A mating phenomenon seen in some snake
ing of snakes. species, especially garter snakes, in which males out-
labial pit. See pit organ. number females in breeding aggregations; from 10 to
100 or more males surround and simultaneously court a
lactate, lactic acid. A product of the incomplete oxidation
single receptive female.
of carbohydrate via the pathway of glycolysis in the ab-
sence of oxygen. Lactate is a salt of lactic acid, typically mean selected temperature. See preferred body tempera-
produced in muscle during very intense activity. ture.
lacunar cells. A cell type present in the epidermis of sq- melanin. A dark pigment derived from oxidation products
uamates during the shedding cycle, located between α- of tyrosine and dihydroxyphenol compounds, present in
keratin above and the clear layer below, and characterized skin and internal peritoneum.
by misshapen nuclei that appear to lie in a vacuole. melanism. Excessive pigmentation or blackening of the
lamellar granules. Discreet lipid-enriched secretory or- skin or other tissues, usually of genetic origin.
ganelles that are present in the epidermis and from melanophore. A chromatophore that contains melanin,
which lipids are released to the extracellular spaces which is generally dark brown to black in color.
where they become part of the epidermal permeability
barrier. melanophore stimulating hormone (MSH). A hormone
formed in, and secreted from, the pituitary gland and
large intestine. The posterior segment of the intestine, which acts on melanocytes to stimulate the dispersion
usually a comparatively straight tube of large diameter of melanin granules within these cells and thereby cause
passing to the cloaca. darkening of the skin.
larynx. A complex of cartilaginous elements, fibers, and melatonin. A predominant hormone associated with the
muscles at the pharyngeal opening of the trachea that pineal gland, but also found in the brain and eyes of ec-
functions to protect the opening and, in some species of tothermic vertebrates. Synthesis of melatonin is largely
reptiles, permits vocalization. under light control, and levels fluctuate rhythmically
lateral undulation (or horizontal undulatory pro- with light cycles. Melatonin is an important communi-
gression). The most commonly used mode of terres- cator between environmental cues of light and tempera-
trial locomotion in snakes, involving horizontal waves ture and affects both physiology and behavior, including
that travel down alternate sides of the body axis and reproduction in snakes.
generate a reaction force at fixed points in the animal’s mesos layer. A stratum of differentiated cells within the
physical environment—usually surface irregularities in stratum corneum, consisting of α-keratinized cells that
the substrate. are alternately sandwiched between lamellar lipids in
left aortic arch. See aortic arches. many species. This layer comprises the permeability bar-
rier to flux of water across the skin.
left-to-right (L-R) shunt. See shunt.
metabolic water. Water that is formed during oxidative
lepidosaur. Any member of a clade of reptiles (Lepidosau-
cellular metabolism.
ria) inclusive of snakes, lizards, amphisbaenians, and
tuatara. microarchitecture. See microsculpture.
lens. The principal light-focusing structure in the eye. microdermatoglyphics. See microsculpture.
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microornamentation. See microsculpture. neuromodulator. A chemical messenger that alters the
microsculpture, microsculpturing. Reference to micro- function or actions of neurons.
scopic features of surface morphology that are present neuron. An individual nerve cell and fundamental unit of
on scales of squamate reptiles. Also called microarchitec- the nervous system. Cf. nerve.
ture, microdermatoglyphics, and microornamentation.
neurotoxic. A property of snake venoms that is destruc-
microstructure. In context of scale morphology, see mi- tive to the nervous system, including neuromuscular
crosculpture. junctions.
microvasculature. The small peripheral blood vessels that neurotransmitter. A “chemical messenger” that is re-
distribute blood within tissues, including arterioles, cap- leased from nerve terminals to affect other nerves or
illaries, and venules. cells on which the nerve terminals act.
microvillus (pl.-i). A minute, cylindrical projection of a node. A branching point in a phylogenetic tree.
cell membrane that increases the surface area of absorp-
norepinephrine. See catecholamines.
tive epithelia, as in the intestine.
oberhautchen. The outermost layer of β-keratin that
mimicry. The phenomenon where organisms resemble one forms the external microsculpturing overlying the epider-
another in context of gaining an advantage in avoiding mis of lepidosaurs. The original spelling of this term is
predators. Öberhautchen. However, Ernest Williams pointed out in
modality. The state or quality of a stimulus or sensation 1988 that the term was now appearing in the English lit-
(light, sound, etc.). erature so frequently that capitalization with an umlaut
was unnecessary.
molecular clock. Reference to a constant rate of nu-
cleotide substitutions in DNA when averaged across ontogeny (adj.ontogenetic). Reference to complete de-
the entire genome of a species. A phylogenetic tree velopment of an organism, from fertilized egg to adult.
that is constructed on the assumption of a molecular opisthoglyph (adj.-ous). A condition in venomous
clock has all the terminal taxa equidistant from the snakes where the posterior pair of teeth on each maxilla
root. are enlarged or grooved to function as fangs.
monophyletic, monophyletic lineage. Reference to a outer epidermal generation. See epidermal generation.
condition in which a group of species have all been de-
rived from a single common ancestor. oval window. The membranous area on the lateral or ven-
tral wall of the inner ear, adjoining the footplate of the
morphological color change. Color changes that occur
columella.
over days, weeks, or longer due to developmental, on-
togenetic, or seasonal changes in chromatophore pat- ovarian follicle. The structure of the ovary that contains
terns. Cf. physiological color change. the developing egg.
MSH. See melanophore stimulating hormone. ovary (pl.–ies). The female reproductive organ (gonad)
that produces ova or eggs.
muscular ridge. A muscular septum in the ventricle of
noncrocodilian reptiles that partially divides the ventri- oviduct. The tube that conveys eggs from the ovary to the
cle by separating the cavum pulmonale from the cavum uterus or to the exterior via the cloaca.
arteriosum and cavum venosum. oviparity (adj. oviparous). A mode of reproduction
nanoscale. Reference to a scale of measurement on the in which underdeveloped eggs are laid by the female. De-
order of a billionth (10−9) of a meter. veloping embryos are encased within membranes over-
lain by a shell, and these are deposited in the environment
naris (pl.-es). The nostril or nasal opening, usually paired. outside the body before hatching. Cf. viviparity, viparous.
neck sacs. See tracheal air sac. oviposition, oviposit. The act of laying or depositing eggs
nerve. A bundle of neurons, or processes of neurons that in the environment. Cf. ovulation.
are enveloped by connective tissue. Cf. neuron. ovulation. The release of an ovum or egg from the ovary.
net cost of transport. The amount of energy that is used Cf. oviposition.
to transport a given mass of an animal a given distance. pant, panting. Increased breathing frequency that in-
neuro-. A prefix meaning nerve or neuron. creases the rate of ventilated air movement and hence
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evaporation of water and removal of heat from mem- pheromone. A chemical substance produced by an individ-
branes associated with the upper respiratory airways, ual and released into the environment for the purpose
throat, and mouth. of signaling a social response between (among) individu-
parenchyma. The essential and distinctive functional tis- als of the same species.
sue of an organ. photoperiod. The period of light in 24 h.
parietal. Either of a pair of dermal bones forming a prin- phylogeny, or phylogenetic tree. A diagram that depicts
cipal part of the braincase at the roof of the skull (lo- the relationships of groups of organisms according to
cated between the frontals and occipitals). Generally, their evolutionary history. The diagrammatic tree repre-
this term is used in reference to the dorsal part of the sents hypothesized genealogical ties and sequence of his-
head. torical, ancestor-dependent relationships that link taxa.
parietal pits. See head pits. physiological color change. Color changes that occur
quickly due to nervous, hormonal, or local control mech-
parthenogenesis (adj. parthenogenetic). Reproduction
anisms. Cf. morphological color change.
in which an egg develops into an embryo without fertili-
zation by a sperm. pigment. In biological usage, a molecular substance in cells
or tissues that imparts color.
passage time. With reference to the gut, the time elapsed
from ingestion to defecation pineal gland. An organ formed from the roof of the fore-
brain that acts to measure light, produces melatonin,
PBT. See preferred body temperature.
and regulates the hormonal output of other endocrine
performance. The relative measure of key tasks or func- structures.
tions such as feeding, digesting, moving, growing, etc.,
pit organ. Specialized infrared receptors having evolved
that are important for survival and reproduction.
independently several times within the Boidae and once
performance breadth. Reference to some measure of the within Colubroidea (Crotalinae). Boid pit organs are
thermal range over which performance has some subjec- located in upper and lower labial scales (and/or rostral
tive value to the organism. scales) and called labial pits, whereas crotaline pit organs
peripheral resistance. The resistance to blood flow attrib- are present as single structures between the eye and
utable to the smaller peripheral blood vessels. nostril on either side of the head and called facial pits
or sometimes loreal pits. Pit organs consist of a thin, in-
peristalsis. A traveling wave of constriction (followed by nervated membrane stretched across an open cavity in
relaxation) in tubular tissue such as the gut, produced by pit vipers, permitting rapid and sensitive detection of
constriction of circular muscle. In the gut, these move- changes in infrared radiation. The labial pits of boids are
ments serve to move objects through the lumen. similar except the membrane lines the inner recess of a
peritoneum. A membrane that lines the body cavity and labial pocket.
invests internal organs therein. placenta. A vascular, nutritive connection between fetal
perivascular lymphatic. A lymphatic vessel that sur- and maternal tissues, through which the developing em-
rounds and is concentric with a blood vessel. These bryo exchanges nutrients, respiratory gases, and meta-
structures are common in snakes. bolic waste products. The wall of the uterus is typically
the maternal connection in placental reptiles.
permeability barrier. In this book, reference to the spe-
cialized layer of lipids that is located in the stratum cor- pleurodont. Reference to an anchoring condition of teeth
neum of the epidermis, limiting the flux of water across in which rootless teeth are attached to the inner side of
the skin. the jawbone, set in a shelf-like inner, lingual wall. This is
a common mode of ankylosis in lizards and snakes.
phenotype. The physical characteristics of an organism, re-
lated to its genetic expression and sometimes modified polymorphism. The sustained occurrence of two or more
by environment. Cf. genotype. distinct and genetically determined forms (e.g., color
pattern) in a single species. This usually represents two
phenotypic plasticity. Variation of phenotype attrib-
or more genetically distinct classes in the same inter-
utable to environmental influence on the phenotype,
breeding population.
caused by environment interaction with genetic expres-
sion related to the particular phenotype in question. See postprandial calorigenic response, metabolic response,
also reaction norm. or thermogenesis. See specific dynamic action.
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power. The rate of doing work, equal to work per time. push point. See resistance site.
prebutton. The small, first segment on the tip of the tail of pyloris. The distal aperture of the stomach, opening into
rattlesnakes, present at birth and lost at the first ecdysis. the small intestine.
Cf. button. radio telemetry. Study of the location, movements, be-
predatory strike. A strike by a snake that is made with havior, or physiology of animals using remote detection
intention of capturing prey. Cf. defensive strike. and transmission equipment involving radio signals.
preferred body temperature (PBT). The mean selected RCM. See relative clutch mass.
temperature that is maintained by an ectothermic ani- reaction force. See thrust and propulsive force.
mal in a gradient or mosaic of thermal environments.
reaction norm. The variability of phenotypic traits exhib-
pressure. Force per unit area. ited by a given genotype under a range of natural con-
pressure shunting. See shunt. ditions common to the habitat of the species, or under
standard experimental conditions. See also phenotypic
prey transport. Reference to swallowing a prey item, in-
plasticity.
cluding manipulation by various active elements of the
jaws and mouth. reaction zone. See resistance site.
prezygapophyses. See zygapophysis. receptor. A nerve or modified sensory cell that receives
and transduces a stimulus.
primitive, or primitive character. Reference to a char-
acter or feature that is basal or of ancient evolutionary rectilinear locomotion. A mode of snake locomotion in
origin. Opposite to derived. which the animal moves forward in a straight line, with
no lateral movement. Muscles act bilaterally to pull the
progesterone. A steroid hormone secreted from the ovary
skin forward relative to the ribs, following which the
and corpus luteum, essential for egg retention and preg-
ventral scales anchor the body to the substrate. Other
nancy in viviparous species. It has many effects that sup-
muscles then pull the ribs and vertebral column forward
port egg and embryo development.
relative to the stationary ventral skin.
prokinesis. A condition of cranial kinesis in which the line
refraction. The bending of light rays when they pass be-
of movement is located between the nasal and frontal
tween two media of differing density (e.g., air to water).
elements, anterior to the orbit.
relative clutch mass (RCM). The ratio of the total mass
proprioceptors. Sensory receptors located primarily in
of a clutch to the body mass of the associated female,
muscles, tendons, or joints that sense tension and pro-
expressed as a decimal fraction or a percentage. Cf.
vide information about the position and relative motion
clutch size.
of body parts.
resistance. Generally, a property or aggregate properties
propulsive force. A force exerted against the environment
that impede the movement or flow of something in a cir-
that results in a reaction force that is equal and opposite
cuit or flow system. In context of locomotion, the forces
in direction. The reaction force is equal to thrust and ena-
that resist forward movement.
bles forward movement of the object or animal exerting
the propulsive force. resistance site (site of resistance). In context of snake
locomotion, any physical point in the environment
proteroglyph (adj.-ous). A snake or condition in which
against which the body can apply force either to “an-
a relatively long maxilla bears a single, hollow, venom-
chor” a position, or to enable forward movement. Also
conducting fang on its anterior end. The fang is fixed and
called contact zone, reaction zone, push point.
followed posteriorly by non-venom-conducting teeth
(characteristic of elapids). resonance (resonate, resonating). A physical process
whereby an oscillating phenomenon is amplified.
pulmonary. Reference to the lung.
respiration. Strictly, the intracellular oxidation of or-
pulmonary circulation. See circulation.
ganic substrates by molecular oxygen, resulting in the
punctuated equilibrium or evolution. Reference to rela- generation of ATP energy and the by-products of CO2
tively brief episodes of speciation, followed by long peri- and H2O.
ods of stability of species.
retina. The innermost, light-sensitive, multimembrane
pupil. The aperture in the center of the iris through which layer of the eye, containing the sensory cells that trans-
light enters the eye. duce light into vision.
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rhinokinesis. A condition of cranial kinesis in which mo- of blood vessels, and biochemical properties that confer
bility of the nasal elements (four snout bones) enables rapid twitch cycles.
unusual rotations of the snout tip during swallowing shedding, skin shedding. See ecdysis.
movements made by natricine snakes.
shunt. An alternate pathway. With respect to intracardiac
right aortic arch. See aortic arches. shunts (within the heart), a right-to-left shunt (R-L shunt)
right-to-left (R-L) shunt. See shunt. results in partial or complete pulmonary bypass (blood
normally intended for the pulmonary artery enters the
rod. A photoreceptor cell of the retina that is sensitive to
systemic vessels), and a left-to-right shunt (L-R shunt) re-
light because of cellular properties responding to low
sults in partial or complete systemic bypass (blood nor-
light intensities. Cf. cone.
mally intended for the systemic vessels instead enters
ruga (pl.-ae). A ridge or fold. the pulmonary artery). Increases in pressure within ei-
saccular lung. The segment of lung that consists of thin, ther of these circuits (whether active or passive) can cre-
membranous tissue with only nutritive blood supply and ate shunting, and these mechanisms are called pressure
nonfunctional in gas exchange. Typically, this segment shunting. Alternatively, a passive mechanism that also
terminates at the blind posterior end of the lung. Cf. creates shunting occurs when blood that is located in a
vascular lung. space of the ventricle common to both pulmonary and
systemic circulations at different phases of the heart cy-
sacculus. The smaller and more ventral of two saclike divi- cle is subsequently “washed” into the “wrong” circulation
sions of the fluid system of the inner ear, and part of the by inflowing or outflowing blood moving in the “correct”
vestibular apparatus. direction. This mechanism is called washout shunting.
salt glands. Extrarenal glands that secrete highly concen- shuttling. A thermoregulatory behavior, which involves
trated solutions of salt. In snakes, these are located in active movement between contrasting warm and cooler
sublingual or premaxillary locations in marine species. parts of the environment.
sand swimming. Reference to rapid burial and burrowing sidewinding locomotion. A mode of locomotion in
movements of sand-dwelling snakes. snakes while moving over low-friction or shifting sub-
scansorial. Proclivity, or adaptation, for climbing. strates such as desert sands. The movement is character-
ized by alternate lifting of sections of the body, which
sclera. The tough, fibrous outer coat of the eye.
are moved forward and then placed down to “roll out”
scutes. The ventral scales of a snake. on the substrate, producing a series of separate, paral-
SDA. See specific dynamic action. lel tracks, each oriented at an angle to the direction of
travel. During these movements the snake is in static
secondary sexual characteristics. Reference to pheno- contact with the ground at two points.
typic differences between sexes other than the reproduc-
tive organs. sinus venosus. The first heart chamber to receive blood
from systemic veins and convey it to the atrium.
semicircular canals. One of the equilibrium organs in the
inner ear, which functions to sense acceleration of the sister taxon. Reference to two taxa having the same im-
head with respect to the gravitational field. See vestibu- mediate common ancestor. These appear on a phyloge-
lar system. netic tree as lineages or branches that arise from a single
divergence node.
seminal plug (also copulatory plug). Dried semen that
site of resistance. See resistance site.
obstructs the female’s reproductive tract or genitalia.
slide-pushing. See slipping undulation.
seminal receptacle. In general, a cavity or structure for
storage of sperm. In snakes this is a branched glandular sliding friction. See friction.
sac in the lumen of the oviduct. slipping undulation (also slide pushing). A mode of snake
seminiferous tubules. Long, convoluted structures with- locomotion employed on low-friction substrates, whereon
in the testis that support developing sperm. backward moving body waves (undulations) are propa-
gated rapidly and generate a sliding friction sufficient to
septum (pl.-a). A dividing wall or partition.
produce a reaction force that propels the snake forward.
shaker muscle. Specialized muscle in the tail of rattle- Alternating waves of body motion are similar to those in
snakes, used to shake the rattle. This muscle is charac- lateral undulation, but the forward reaction forces are gen-
terized by having numerous mitochondria, a rich supply erated without the use of fixed points on the substrate.
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small intestine. The anterior segment of intestine and the structures are innervated and possibly function as heat
principal site of digestion, extending between the stom- detectors, similarly to the facial pits of pit vipers.
ach and large intestine.
systemic circulation. See circulation.
smooth scale. Reference to a scale of squamate reptiles
systole. Contraction of the ventricle to eject blood into the
that lacks prominent keels or central ridges, detectable
arterial system. Cf. diastole.
by touch or by eye. Cf. keeled scale.
temporal arches. Reference to the upper or lower arch-
snakebot. A robot modeled or fashioned after a snake.
es or bars formed by skull bones as a consequence of
solenoglyph (adj.-ous). A snake, or condition, in which fenestration.
each fang is erected by rotation of a reduced maxilla
tendon. A band or cord of fibrous connective tissue that
on the prefrontal bone, characteristic of viperid and
is continuous with muscle fibers and attaches muscle to
atractaspidid snakes.
bone or cartilage.
specific dynamic action (SDA). Increase of metabolic
testis (pl.-es). The male gonad in which sperm are
rate that follows ingestion of a meal.
produced.
spectacle. The fixed and transparent eye covering of a
testosterone. A steroid androgen synthesized in the testes
snake, consisting of epidermis that is fused with the
and responsible for the appearance and maintenance of
sclera of the eye. Also called brille or eyecap.
male secondary characteristics.
spermatogenesis. The development of mature spermato-
thermal intertia. A tendency to slow the gain or loss of
zoa in the male testis.
heat due to the contribution of an animal’s mass to its
spur. A corneous spine projecting from either side of the capacity for heat. Larger objects (or animals) heat and
cloacal opening in certain species of snakes representing cool more slowly than do smaller objects (or animals),
basal lineages. and they are said to exhibit greater thermal inertia.
static friction. See friction. thermal preferendum. See preferred body temperature.
stimulus. A quality of the environment that stimulates a thermoreceptor. A sensory nerve ending specifically re-
receptor. sponsive to temperature changes.
stratum corneum. The keratinized, outermost layers of thermoregulation. Regulation of temperature. See behav-
the epidermis. ioral thermoregulation.
stratum germinativum. The basal or innermost layer of thrust. A forward-acting force that produces forward mo-
living cells of the epidermis, which by means of cell divi- tion. Cf. propulsive force.
sion gives rise to the cell layers of the epidermis above it.
topology. The branching order of a phylogenetic tree.
streptostyly. A condition of cranial kinesis in which the
trachea. A membranous and cartilaginous tube that con-
quadrate forms a mobile joint with the squamosal ele-
ducts air between the throat and lung. See also tracheal
ment, resulting from the evolutionary loss of the lower
lung, tracheal air sac.
temporal arch.
tracheal air sac. Membranous diverticula that are acces-
structural color. A color seen on the surface of an animal,
sory outgrowths of the tracheal airway and function in
attributable to physical or structural attributes that dif-
defensive displays or sound production in various Asian
ferentially reflect light in various ways, not due to the
species of snakes.
presence of pigment.
tracheal chambers or diverticula. See tracheal air sac.
supercooling. Reference to cooling below the physical
freezing (= melting) point of body fluids without forma- tracheal lung. Vascular, functional lung that arises along
tion of ice crystals. an expanded tracheal membrane, anterior to the heart in
certain species of snakes. See vascular lung.
supranasal sac. A recess formed by invaginated skin be-
neath the supranasal scale, having an inconspicuous slit- trailing behavior. Reference to one individual following
like opening between the supranasal and nasal scales. another (usually conspecific) individual, largely by means
This structure is present in many snake species of the of a chemical trail that results from adherence of skin
subfamily Viperinae and the related Causinae. These pheromones to the substrate over which a snake moves.
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transducer. A device that changes the form of energy that and the ambient medium (= breathing and sometimes
impinges on it or is an input signal. called external respiration).
truncus arteriosus. Literally arterial trunk, with refer- ventricle. The muscular chamber of the heart that receives
ence to the three outflow tracts (right and left aortic blood from the two atria and pumps it via outflow tracts
arches, and pulmonary artery) where they are joined by to tissues of the body.
common elements of fibrous fascia near their origins at venule. A smaller blood vessel that connects a capillary bed
the ventricle of the heart. with a vein.
undulation. Reference to movement in waves, or sinusoi- vertebral column. The spinal skeleton consisting of a se-
dal movement from side to side. ries of articulating vertebrae extending from the skull to
up-regulation. Control of a physiological activity by an in- the tip of the tail.
crease in receptor density in a target cell membrane. Cf. vertical septum. An incomplete septum in the ventricle
down-regulation. of noncrocodilian reptiles that partially separates the
urates, uric acid. The crystalline waste product of nitro- cavum arteriosum from the cavum venosum.
gen metabolism. Urates are salts of uric acid, which is vestibular system. The collective organs of equilibrium in
poorly soluble in water and can be excreted in a precipi- the inner ear.
tated form with minimal loss of water.
villus (pl.-i). One of numerous small, fingerlike projec-
uterus. A glandular part of the oviduct (middle region in tions of tissue that function as absorptive structures in
snakes) responsible for the production of fibrous and the intestine.
calcium components of the eggshell in reptiles.
viscosity. A physical property of a fluid that impedes the
utriculus. The larger of two saclike divisions of the fluid tendency for adjacent layers of the fluid to move past
system of the inner ear, associated with the sense of each other. The internal friction of a fluid causing resist-
equilibrium. See vestibular system. ance to flow.
vascular lung. The functional segment of the lung, char- vitellogenesis. The production of yolk, or “yolking” of an
acterized by a spongy appearance and rich blood supply. egg in the ovary.
Cf. saccular lung.
viviparity (adj. viviparous). The retention of embryos
vasoconstriction. Constriction of smooth muscle in blood within the oviduct until development is complete, thus
vessels, usually smaller arteries. giving birth to developed young instead of laying eggs.
vasodilation. Relaxation of smooth muscle in blood ves- Cf. oviparity, oviparous.
sels, usually smaller arteries, which results in dilation of vomeronasal organ. A specialized chemosensory cham-
the vessel(s) in question. ber that forms a major sense organ above the roof of
vein. A blood vessel that returns blood from tissue capil- the mouth in snakes (and other reptiles). It is lined with
lary beds toward the heart. Cf. artery. sensory epithelium that detects odorant particles that
are brought into the mouth on the tongue. Also called
venom. A toxic or potentially toxic substance normally
Jacobson’s organ.
secreted by an animal and injected by a stinger, fang,
or bite. washout shunt. See shunt.
venom delivery system. With reference to snakes, this zygapophysis (pl.-es). Each of four processes on the bor-
term refers to venom, associated glands for production der of the neural arch, which articulates with its oppo-
and storage, and the muscles and specialized teeth that site member on adjacent vertebrae, providing additional
are used for delivery. strength to the articulation and preventing undue tor-
sion. Anterior zygapophyses (called prezygapophyses) are
vent. The cloacal opening from cloaca to exterior.
directed upward and somewhat inward, whereas poste-
ventilation. In respiration physiology, the process of mov- rior zygapophyses (called postzygapophyses) are directed
ing air or water between the gas exchanger (lung or gill) downward and slightly outward.
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INDEX
abdominal cavity, 192 African Bush Viper, fig. 1.27 amplitude

abduction, 186 African egg-eating snake, 30 of flexions or undulations, 81, 83,
absorption (digestive), 65, 68 African garter snakes, 26 85–86, 90, 98
Acalyptophis peronii, fig. 3.8 African Horned Adder, 95 of sound, 185, 188
Acanthophis, 57, 188 African house snakes, 200 anaconda, 14, 16, 169
Acanthophis antarcticus, 48, 189, African Rock Python, 16 Green Anaconda, 14, figs. 1.18–1.19,
figs. 1.42, 8.7 age, aging , 62, 110, 210 2.1, 2.12
Acanthophis rugosus, fig. 6.18 aggregation, See behavior ancestral trait or lineage, See basal trait or
acceleration, 81, 84, 85, 99, fig. 3.12 Agkistrodon, 22 lineage
accelerometer, 85 Agkistrodon contortrix, 135, fig. 1.32 androgens, See hormone: sex steroids
accessory venom gland, 60–61, fig. 2.27 Agkistrodon piscivorus, 21, 48, 53, 135, anguilliform swimming, 81
acclimation, 110, 114, fig. 4.14 182, fig. 3.2 angular bone, 41
acclimatization, 110, fig. 4.14 Agkistrodon piscivorus conanti, 46, 137, Aniliidae, 13–14
accommodation, 165 208, figs. 1.3, 1.5, 1.32, 2.2, 2.13, Anilius scytale, 13, fig. 1.14
acetylcholine, 58, 149 2.33, 2.35, 2.38, 5.24, 6.2, 6.13, ankylosis, 54
acetylcholinesterase, 58 7.11, 7.13, 9.3, 9.18–9.19 Anomalepididae, 11
acoustic signal or profile, 182–183 aglyphous, 57, 60 Anomochilidae, 13
Acrantophis dumerili, figs. 2.34, 5.4–5.5 Ahaetulla, 167 Anomochilus, 13, fig. 1.13
acrochordid (Acrochordidae), 13, 17, 18, 34, Ahaetulla prasina, 167, figs. 3.3, 7.5 antifreeze proteins, 113
47, 71, fig. 1.23 Aipysurus laevis, 177 antivenin, 62
Acrochordoidea, 17, 34 air sac, See tracheal air sac aortic arch, 143–146, figs. 6.3, 6.5
Acrochordus, 44, 85, 120, 147–148, 155, 157, albino, 137 Aparallactinae, 19–20
159, 167, 177 alethinophidian (Alethinophidia), 12–13, 34 Aparallactus, 19
Acrochordus arafurae, 18, 108, 195, 209, algae, fig. 2.38 Aparallactus jacksoni, 19
fig. 1.23 alimentary canal, See gastrointestinal Aparallactus modestus, 57
Acrochordus granulatus, 18, 42, 71, 124, tract apical pit, 177, figs. 7.11, 7.13
145, 155, 157, 169, 177, figs. 1.23, allele, 137 Aplopeltura, 33, 42
5.15, 6.8, 6.10 “all-or-none,” 183 apnea, 156
Acrochordus javanicus, 18 alpha (α) keratin, See keratin aposematism, 131–132
action potential, 58, 117, 127, 149, 164, 168, altitude, See high altitude aquatic, See habitat, habits
171, 175, 181 Amazon Tree Boa, fig. 2.16 aquatic locomotion, See behavior:
active foraging, forager, See behavior ambush foraging, forager, See behavior locomotion: swimming
adaptive radiation, See evolution amelanistic partial albinism, 137 Arafura File Snake, 195
adder, 20–21, 169, 182 ammonium, 70 arboreal, See habitat, habits
adduction, 186 amniote, 51 Arizona Black Rattlesnake, 134, fig. 5.22
adrenal gland, 149 amphibian, 5, 113, 148 arteriole, 146, 148–149
advanced snakes or lineage, 42, 46, amphibious, See aquatic artery, 145–146, 148
See also Alethinophidia and amphisbaenian, amphisbaenid, 4, 10, 34, arthropod, 99
Caenophidia 99, fig. 1.4 Aruba Island Rattlesnake, fig. 1.29
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Asclepius, rod of, fig. 5.1 cannibalization, fig. 2.33 rectilinear, 90–91, 96, fig. 3.12
Asian coral snake, 26, fig. 1.41 cantilever, 88, 96–97, fig. 3.17 sidewinding, 89–90, 92–93, 99,
Asian flying snake, 30 caudocephalic waves, 206 figs. 3.13–3.14
Asian pipe snakes, See pipe snakes cloacal popping, 188 slide-pushing, 92–94
Asian sunbeam snakes, 13 coil, coiling, 95, 108, 111, 129, 131, 135, “sprint,” 89
Aspidites, 17 158, 182, 185, 208, figs. 5.15, 9.14 swimming, 18, 77–78, 80–86, 92, 132,
Aspidites melanocephalus, fig. 7.8 combat behavior or dance, 205–206, figs. 3.1, 3.5, 3.8–3.9, 5.7
Aspis, 182 fig. 9.19 anguilliform swimming, 81
assimilation, 69 communal nesting, 198 nest attendance, 198, fig. 9.14
Asthenodipsas, 33 constriction, 13, 37–38, 45–46, 49, 50, nocturnal, 19–20, 26, 33, 107, 109,
Astrotia stokesii, 27, fig. 1.45 78–79, 149, figs. 2.3, 2.7, 2.12 114–115, 135, 165–166, fig. 1.5
Atheris, 21, 155 cratering , 95, fig. 3.16 pair bonding, 209
Atheris squamigera, figs. 1.27, 5.8 crepuscular, 165–166 parental care, 208
ATP, 141, 184 defensive behavior, display, or posture, posture, postural control, 98, 108–109,
Atractaspididae, 19 11, 13, 20, 22, 48, 61, 160, 185, 151–152, fig. 6.18
atractaspidine (Atractaspidinae), 19–20, 188, figs. 1.48, 1.50, 6.19, 7.10 predator, predation, predatory
56, 60–61 den, denning, 94, 108, 112, 118, 189, behavior, 95–96, 115, 129–132,
Atractaspis, 19–20, 56, fig. 1.24 200, 205, fig. 4.7 134–135, 138, 167, 173, 177, 184,
Atractaspis microlepidota, fig 1.24 dispersal, 208 209–210
atrioventricular valves, 143–144 diurnal, 114, 166–167 reproductive behavior, 200, 203–204,
atrium, atria, 143–144, 147, figs. 6.2–6.3, 6.5 diving , 29, 77, 145, 147–148, 156, 159, 206
Atropoides, 22, 95 fig. 6.14 courtship, 123–124, 173, 201–202,
Atropoides mexicanus, fig. 1.36 drinking , 66, 70, 72 204–208
auditory nerve, 168–169, fig. 7.7 incidental drinking, 70 mating, coitus, copulation, 173,
auditory system, 175 “sponge model” of drinking, 72 192–195, 200–201, 203–204, 206,
Australian Red-bellied Black Snake, 25 escape behavior, 95–96, 130, 135 208, fig. 9.17
axial muscle, See epaxial muscle feeding , 37–62, 66–67, 69–70, 72, 111, mating “ball,” 208
axial skeleton, See skeleton 173, 196, fig. 2.4, postmating behavior, 208–209
Azemiopinae, 24 periodic (discontinuous, precourtship behavior, 204–205
Azemiops feae, 22, fig. 1.37 intermittent) feeding, 66 rubbing scales, 182
flattening or compression (of body), 13, sand swimming, 94
background color match, See color 18, 29, 78, 85, 96–98, 107–108, spitting venom, See venom
bacteria, 65–66, 68 159, figs. 3.1, 3.6, 3.19, 4.2, 5.7, strike, striking, 20–21, 48–53, 62, 69,
ballast, 69 5.20, 6.18 95–96, 129, 169–170, 173, 175,
Ball Python, 16, 166, 168, 210 hood, 26, 78 177–178, 184–185, 187, figs. 1.36,
Barbados Threadsnake, fig. 1.12 neck, figs. 1.48, 5.20 2.16, 2.20
barnacle, fig. 5.16 tail, See tail tail
baroreceptor, See receptor foraging , 48, 53, 66, 69, 96, 115, 173, 176, caudal luring, 26, 188–189
basal trait or lineage, 9, 12–13, 24, 38, 210 curling or elevated, 26, 129, 132, 188,
41–42, 46, 55, 58, 143, 155, 166, active foraging, 46, 47, 67 fig. 1.50
204, fig. 2.4 ambush foraging, 26, 47, 66–67, 95, prehensile, 53, 78, fig. 2.20
basement membrane, 118, figs. 5.3–5.4 170, figs. 1.28, 1.42, 3.16 rattling, shaking, vibration, 22, 158,
basilar membrane, 168–169, fig. 7.7 caudal luring, 26 181–185, fig. 8.4
bask, basking, See behavior: “float-and-wait,” 44, figs. 1.44, 2.8 thermoregulation (behavioral), 105–110,
thermoregulation gaping , See gape 134, 136, 173, 176, 196, 203, 210
bat, 186 growling , 187 basking, 96, 109, 111, 173, 196, figs.
Bearded Dragon lizard, fig. 2.5 head swaying, 167 4.2, 4.8–4.9
behavioral thermoregulation, See hiss, hissing, 22, 26, 48, 61, 158, 160, “set point” (for regulation), 110
behavior: thermoregulation 181, 185–187 shuttling, 107–108
behavior, 10 nasal hissing, 187, fig. 8.6 tongue flicking, See tongue
activity (general), 203, fig. 4.15 inflating neck or body, 61, 155, 158–160, trailing behavior, 49, 60, 173, 205–206
aggregation, 11, 94, 108, 112, 173, 198, figs. 6.17, 6.19 chemical trails, 118
208, fig. 4.7 jumping , 95–96, 98 bellowing, See behavior
aggressive behavior, 26, 129, 136, 204 knotting , 124, fig. 5.15 belly plates, See scale
“blocked-flight aggression,” 96 locomotion, 29, 69, 77–101, 114, 147, bends, See decompression illness
bellowing, 187 149, 210, fig. 3.3 beta (β) keratin, See keratin
biting, bite force, 49, 51, 206 climbing, scansorial, 16, 96–98, bicarbonate, 157
brooding, 12, 16, 110–112, 208, fig. 4.12 149–153, figs. 3.4, 3.18 bile (from liver), 65
burrow, burrowing, 7, 11–13, 19–21, 26, 47, concertina, 88–90, 94, 96, 99, fig. 3.11 binocular vision, See vision
55–56, 78, 90, 94–95, 107–108, 110, gliding , 77, 98 biochemical reaction rate, 114
121–122, 157, 164, 166–167, 189, lateral undulation, 86–90, 92–93, 96, bird, 5, 10, 26, 66, 71, 80, 103, 106, 112, 132,
210, figs. 1.4, 1.24, 3.15, 1.49, 3.11 98–99, figs. 3.9–3.10 138, 143, 200–201, 209
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birth (and hatching), 126, 198, fig. 9.15 body cavity, 78, 147, 156, 159, caduceus, fig. 5.1
Bitia hydroides, 33 figs. 6.12, 9.5, See also caecilian, 3, 19
biting, bite force, See behavior abdominal cavity caenophidian (Caenophidia), 12–13, 15, 17,
Bitis, 21, 22 body fluids, 71, fig. 6.8 146, 205
Bitis arietans, 21, 176, 186–187 body size, length or mass, 78, 88, 91, Caisson disease, See decompression illness
Bitis caudalis, 95 92–93, 98, 163, 186, 192, 196, 199, calcium, 193, 195
Bitis gabonica, 21, 69, 170, figs. 1.6, 1.28, 205, 209 calcium carbonate, 197
2.25, 8.6 body temperature, See temperature California King Snake, 111, 126, 138, figs.
Bitis nasicornis, 21, figs. 1.28, 2.25 flattening, compression, See behavior 2.7, 5.26
Black-headed Python, fig. 7.8 trunk, 86, 88, 92–93, 95, fig. 3.3 Calliophis, 26
Black-headed Sea Snake, fig. 3.6 Bogertophis subocularis, fig. 9.15 Calliophis sauteri, fig. 1.41
Black Mamba, fig. 2.6 boid (Boidae), 16, 68, 123, 136, 155, 175, 177, Calloselasma rhodostoma, 22, 62
Black Milk Snake, fig. 5.19 199, 205 camouflage, See crypsis
black peritoneum, 135 Boiga, 30, 57 cannibalization, See behavior
Black Racer, fig. 5.8 Boiga irregularis, 30, 60, 96 cantilever, See behavior
Black Rat Snake, figs. 1.48, 2.37, 9.13, 9.15 Bolyeria multocarinata, 16 capillary, 141–143, 145–148, 155–157, 183,
Blacktail Cribo, 45, fig. 1.48 bolyeriid (Bolyeriidae), 15, 136 figs. 5.3, 6.4, 6.12, 6.15
Black-tailed Rattlesnake, fig. 1.29 bone, 54, fig. 2.23 capitulum, fig. 3.2
Black Threadsnake, fig. 1.12 Booidea, 12 captive breeding, 200–201, fig. 5.25
Black Tiger Snake, fig. 4.15 Boomslang , 58 carbohydrates, 66
blind snakes, 4, 13, 90, 127, 192 Bothriechis, 22 carbon dioxide, See respiratory gases
Braminy Blind Snake, fig. 1.11 Bothriechis supraciliaris, fig. 1.34 Carboniferous period, 5, figs. 1.7–1.8
dawn blind snakes, 11 Bothriopsis, 22 cardiac muscle, See muscle
“Blocked-flight aggression,” See behavior Bothrochilus boa, fig. 4.12 cardiac output , 149, 151
blood, 59, 70, 127, 142–144, 147–148, 155–157, Bothrops, 22 Caretta caretta, fig. 2.14
160, 202, figs. 2.26, 6.1, 6.6, 6.15 Bothrops asper, fig. 5.11 carotene, See pigment
blood circulation, 63, 65–66, 97, 113, Bothrops jararaca, 62 carotid artery, 146, 151, fig. 6.5
141–153, 156, 203, figs. 6.1, 6.9 Boulengerina, 26 Carphophiinae, 32
pulmonary circulation, 143 boundary layer, 84–85, 123, fig. 3.7 Carphophis, 32
systemic circulation, 143 Brahminy Blind Snake, 195, fig. 1.11 carrion, See prey
blood flow, 46, 113, 147, 149, 151, 159, branch (of phylogenetic tree), 9, 12, 34, cartilage, fig. 6.11
175, 184 fig. 1.9 Casarea dussumieri, 15
blood oxygen capacity, See oxygen brain, braincase, 38, 40–41, 46, 50, 51, catecholamines, 149
capacity 57, 78, 112, 117, 149, 151–152, Cat-eyed Snake, figs. 2.17, 3.3
blood plasma, 70, 113, 142, 147, 151, 163–164, 169–170, 172, 175, 178, cat snake, 30
156–157 202, 205, fig. 2.6 caudal luring, See behavior
“blood pooling,” See pooling Brazilian Coral Snake, fig. 5.19 caudocephalic waves, See behavior
blood pressure (arterial), 58, 145, Brazilian Hawkmoth caterpillar, fig. 5.21 causine (Causinae), 176
147–153 Brazilian Rattlesnake, 203 Causus, 21, 155
diastolic pressure, 149 breathing , See ventilation Causus maculatus, fig. 1.26
systolic pressure, 149 brille, See spectacle caval vein, 147, fig. 6.5
venous pressures, 149 Broghammerus reticulatus, 14, 16, figs. 1.17, cavum arteriosum, 144, figs. 6.2–6.3
blood supply, See vasculature 2.23, 9.6 cavum pulmonale, 144, figs. 6.2–6.3
blood vessel, 58, 143, 145–149, 151–152, bronchus, bronchial airway, 153, figs. 6.4, cavum venosum, 144, figs. 6.2–6.3
197–198, fig. 6.5 6.11 Central American Coral
blood volume, 147–148, 157 brooding , See behavior Snake, fig. 5.19
Blotched Palm Viper, See palm viper brown snake, 26, 89 Central American Indigo Snake, fig. 1.48
Blue-banded Sea Krait, fig. 1.43 Brown Tree Snake, 30, 96 Central American Jumping Pit Viper, See
Bluestriped Garter Snake, fig. 1.46 Brown Vine Snake, figs. 1.48, 2.18, 5.18 jumping pit viper
Blunt-headed vine snake, 32 buffer, buffering, 157 Central American Rattlesnake, fig. 2.39
Blunt-headed Tree Snake, fig. 1.51 Bull Snake, 47, 111, 182, 186 Central American Speckled Racer,
boa, 5, 12, 15–16, 34, 50, 55, 67, 78, 91, 97, Bungarus, 26 fig. 1.48
107, 120, 173–174, 176 Bungarus multicinctus, fig. 1.40 central nervous system, See nervous
Boa Constrictor, Boa constrictor, 16, 53, 96, buoyancy, 84, 86, 155, 159, fig. 6.14 system
107, 136, figs. 1.21, 2.31, 9.11 Burmese Python, 16, 67, 69, 111, 175, 199, centrifugal acceleration, 84
body, body wall, 19–20, 26, 37, 48, 77–78, figs. 2.36, 4.10, 6.4 Cerastes cerastes, 169
81, 83, 85, 87–95, 97, 99, 103, burrow, burrowing, See behavior Cerberus rhynchops, 34, 167
106–109, 112, 123, 152, 155–156, Burton’s Snake Lizard, fig. 1.4 chameleon, 117
158, 168, 174, 181, 185–186, 193, bushmaster, 22, 47 character, character state, 9–11
196, 199, 206, 210, figs. 1.20, South American Bushmaster, fig. 1.33 character evolution, 9–10
1.22, 1.30, 1.31, 1.36, 1.42, 2.32, bush vipers, 21 Charina, 16
3.1, 3.6, 3.11–3.13, 4.10, 5.15 button (of rattle), 182, fig. 8.3 Charina bottae, 110
Index | 229
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chemical cues or signals, See color vision, 166 Cottonmouth, 21–22, 48, 50–51, 53, 95,
chemoreception genetics, 136–139 135–136, 182, fig. 3.2
chemoreception, 49, 118, 169–173, structural color, 123, 127–128, fig. 5.12 Florida Cottonmouth, 46, 53, 66, 137,
205 Coluber, 30 208–209, figs. 1.3, 1.5, 1.32, 2.2,
chemosensory receptors, See receptor Coluber constrictor, 99, 135, fig. 5.8 2.13, 2.33, 2.35, 2.38, 5.24, 6.2,
Chinese Cobra, fig. 2.26 Coluber constrictor constrictor, 137 6.13, 7.11, 7.13, 9.3, 9.18–9.19
Chinese Green Tree Viper, 115, figs. 1.31, Coluber constrictor flaviventris, 208 cotylosaur, 5, fig. 1.8
5.6 colubrid (Colubridae), 10, 12, 17, 19, 26, countercurrent heat exchanger, 110
Chinese Moccasin, 22, figs. 7.11–7.12 29, 32, 34, 42, 47, 54–55, 57, 61, courtship, See behavior: reproductive
Chinese Sea Krait, figs. 1.43, 6.14, 6.16 67, 85, 98, 113, 120, 131, 136, 151, behavior
Chionactis occipitalis, 94 159, 166–167, 173, 199, 205–206, cranial kinesis, See streptostyly
chorioallantoic placenta, See placenta 208–209, fig. 31 cratering, See behavior
chorioallantois, See extraembryonic Colubrinae, 29, 32, fig. 1.48 Crayfish Snake, 29, fig. 2.22
membranes colubroid, (Colubroidea), 12–13, 17, 29, 34, Cretaceous period, 6, 12
chromatophore, See pigments 56–58, 60 cricoid cartilage, 186
Chrysopelea, 30, 98 columella, 168–169, 181, fig. 7.7 critical thermal maximum (CTMax), 113
Chrysopelea paradisi, 98, fig. 3.19 combat behavior or dance, See behavior critical thermal minimum (CTMin), 113
chyme, 64–65, 67 Common Death Adder, 48, 189, figs. 1.42, crocodile, crocodilian, 5, 10, 80, 118, 143,
ciliary muscle, See muscle 8.7 145, 197
circadian rhythm, 110, 202 Common Garter Snake, 201, 203 Cross-barred Tree Snake, fig. 5.12
circannual cycle, 201 communal nesting, See behavior crotaline (Crotalinae), 20, 22, 24, 50,
circulatory system, 142–153, 160 compound bone, 51 173–176
clade, 10, 27 compression (body or tail), See behavior Crotalus, 22, 49, 173, 182–185
cladogram, See phylogenetic tree compressor glandulae, See muscle Crotalus adamanteus, 22, 80, 187, 211,
classification (taxonomic), 4–5, 10, 27 compressor muscle, See muscle figs. 1.29, 2.5, 5.9, 5.17, 8.3
clear layer (of skin), 126, fig. 5.4 concertina locomotion, See behavior: Crotalus atrox, 22, 66, 176, 182–183, 187,
climatic change, 210 locomotion figs. 6.17, 8.3–8.4
climbing, See behavior cones (of eye), See receptor: visual Crotalus catalinensis, 22
cloaca, See gastrointestinal tract receptors Crotalus cerastes, 67, 92, 99,
cloacal gland, See gland connective tissue, 54, 78, 118, 155, 173 figs. 3.13–3.14, 3.16, 7.10
cloacal popping , See behavior constriction, See behavior Crotalus cerberus, 134, fig. 5.22
clock (season or rhythm), 201 constrictor laryngis, See muscle Crotalus durissus, 111, 208, figs. 4.1,
Cloudy Snail Sucker, fig. 2.8 contact zone, See resistance site 4.13, 7.12
clutch, clutch and litter size, 199–200, Contia, 32 Crotalus durissus unicolor, fig. 1.29
210, figs. 9.8, 9.12 conus arteriosus, 143 Crotalus durissus terrificus, 203
CO2, See respiratory gases convection, 141–142, 158, fig. 6.1 Crotalus horridus, 50, 66, figs. 1.29,
Coachwhip, 67 convergence 2.32, 7.2
coagulation, 58 convergent evolution, 10, 26, 33, Crotalus lepidus, fig. 1.29
cobra, 19, 24–26, 46, 56, 59, 61, 96, 108, 48, 132, 195, figs. 1.22, 1.53, 1.42, Crotalus mitchellii, 136
187, 191, figs. 1.39, 2.26 3.8 Crotalus mitchellii pyrrhus, 134,
King Cobra, 26, 159–160, 187, 198, convergence in neural circuits, 173 fig. 5.23
figs. 1.39, 2.11, 4.5, 9.1, 9.14 copperhead, 22, 49 Crotalus molossus, fig. 1.29
cochlear duct, 168, fig. 7.7 Northern Copperhead, fig. 1.32 Crotalus oreganus, 173
coefficient of friction, See friction copulation, See behavior: reproductive Crotalus oreganus helleri, 134,
coelomic cavity, See body behavior figs. 2.25, 4.6
coil, coiling, See behavior copulatory organ, See hemipenes Crotalus ruber, 80, 185
coitus, See behavior: reproductive copulatory plug, See seminal plug Crotalus ruber lorenzoensis, 22
behavior coral snake, 24–26, 46, 131–132, 188, Crotalus simus, fig. 2.39
collagen, 118–119, 155 fig. 5.19 Crotalus viridis nuntius, fig. 1.29
Collared Lizard, fig. 4.2 Corallus Crotaphytus collaris, fig. 4.2
color, coloration, 3, 5, 10, 12, 16, 19, 22, 26, Corallus caninus, 17, figs. 1.22, 7.4 crypsis, cryptic, 22, 26, 129–132, 134–136,
61, 117, 127–140, 167, 192, figs. Corallus grenadensis, figs. 2.20, 3.17 167, 204, figs. 1.25, 1.28, 1.31,
1.22, 1.31, 1.34, 5.24–5.25, 6.18, Corallus hortulanus, fig. 2.16 1.36, 3.16, 5.17, 5.22–5.23, See also
See also pigments “corkscrew,” (of portal vein), 147, fig. 6.6 background color match
background color match, fig. 6.18 cornea, See eye CTMax, See critical thermal maximum
color change, 135–136 corneous, cornified, 119 CTMin, See critical thermal minimum
morphological color change, 136 Corn Snake, 96, fig. 9.5 cutaneous evaporative water loss, See
ontogenetic color change, 136, 138 coronary arteries, fig. 6.2 evaporation
physiological color change, 136 corpus luteum, 193 cutaneous gas exchange, See gas exchange
color polymorphism, 138, “costal pump,” 186 cutaneous receptor, See receptor
figs. 5.26–5.27 costocutaneous muscle, See muscle Cylindrophiidae, 13
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Daboia Display (defensive), See behavior avian egg, 197
Daboia palaestinae, fig. 7.2 “dissociated reproductive cycle,” 203, fig. egg follicle, 193, 203, 210, fig. 9.6,
Daboia russelli, 176, 187, fig. 5.10 9.17 See also vitellogenic follicle
Dasypeltis, 30, 54, 56, 182 Disteria major, fig. 5.16 eggshell, 193, 195, 197–199,
dawn blind snakes, 11 dive, diving , See behavior figs. 9.12–9.13, 9.15
death adder, 26, 57, 188 diversity (of characters or species), 11–12, “flexible-shelled egg,” 197
decline (of snakes), See extinction 20, 22, 29, 58, 129, 136, 150, 166 “rigid-shelled egg,” 197
decompression illness, 29, 145 DNA , 5, 7, 9, 59, 191–192 egg yolk, See yolk
defecation, 67–69 Dog-faced Water Snake, 34 egg-eating snakes, 56, 182
defense, See behavior dormancy, 66, 200, 202, 204, 208 African egg-eating snakes, 30
degenerated, 13, 165–166, fig. 1.4 dorsal aorta, 146, fig. 6.5 egg tooth, 199, fig. 9.15
dehydration, 66, 70–72, 113, 197, 209 down-regulation, 67, 70 Elachistodon, 54
Deinagkistrodon acutus, 22, figs. 6.1, 7.11–7.12 drag force, See resistance Elachistodon westermani, fig. 2.1
den, denning, See behavior drink, drinking, See behavior Elaphe, 30, 151, fig. 6.5
Dendrelaphis, 30 drought, 201 Elaphe quadrivirgata, 169, 173
Dendroaspis, 26, 55 Drymarchon, 30 elapid (Elapidae), 12, 17, 19–20, 24–25,
Dendroaspis jamesoni, fig. 1.38 Drymarchon corais corais, fig. 9.12 27, 30, 34, 46, 54–58, 60–61, 67,
Dendroaspis polylepis, fig. 2.6 Drymarchon melanurus, 45, fig. 1.48 109, 113, 120, 131, 151, 166, 199,
dendrogram, See phylogenetic tree Drymobius, 30 208–209
dentary bone, 51, 55–56, fig. 2.23 Drymobius margaritiferus, figs. 1.5, 1.48 Elapsoidea, 26
dentition, See teeth Dryophis, 167 elastin, 155
deoxygenated blood, 143–144 Duberria, 42 elastic fibers or tissue, 145, 197
derived trait or lineage, 4, 9, 55 duct, 60, 192, 195, See also efferent duct electromagnetic radiation, See radiation
dermal melanophore process, 136 Dumeril’s Ground Boa, figs. 2.34, 5.4–5.5 electromyography (EMG), 88, fig. 3.9
dermis, See skin duplex retina, 166 electroreception, electric field, 177
Desert Horned Viper, 169 Dusky Pygmy Rattlesnake, fig. 4.3 elephant trunk snakes, 18, fig. 1.23
development, 7, 111, 115, 135, 158, 170, Duvernoy’s gland, 60 embryo, embryogenesis, 8, 54, 71, 109,
192–193, 196–198, 210 dwarf boas, 15 120, 192–193, 195–198, 201, 203,
developmental plasticity, See plasticity dwarf pipe snakes, 12–13 figs. 9.8, 9.10
Diadophis, 32 embryonic membranes, 25, 195, 197
Diadophis punctatus, fig. 1.50 ear, 3, 7, 34, 167–169, 181, 189, fig. 7.7 chorioallantois, 195, fig. 9.10
diagnostic character, 3, 121, 192 Eastern Coachwhip, 47, 77, fig. 2.14 Emerald Tree Boa, 17, figs. 1.22, 7.4
Diamondback rattlesnake, 22 Eastern Coral Snake, 188, fig. 5.19 emergence, 107, 200–201, 204–205,
Eastern Diamondback Rattlesnake, 80, Eastern Corn Snake, fig. 7.9 fig. 9.17
187, 211, figs. 1.29, 2.5, 5.9, 5.17, 8.3 Eastern Diamondback Rattlesnake, See EMG, See electromyography
Western Diamondbacked Rattlesnake, diamondback rattlesnake Emydocephalus, 56
176, 182, 187, figs. 6.17, 8.3–8.4 Eastern Glass Lizard, fig. 1.4 Emydocephalus annulatus, 205, fig. 2.15
Diamond Python, 111, fig. 6.12 Eastern Garter Snake, 137 endocrine, endocrines, See hormone
diapsid, 39, fig. 2.4 Eastern Hognose Snake, 137, 187 endotherm, endothermy, 20, 103
Diard’s Blindsnake, 12 Eastern Racer, See Black Racer facultative, 111
diastole, 144, 149, fig. 6.2 Eastern Rat Snake, figs. 2.19, 2.30 thermogenesis, 111, fig. 4.13
dichromatic color vision, See vision Eastern Yellow-bellied Racer, 208 endurance, 90, 97, 99
diet, See prey ecdysis, 4, 11, 22, 72, 110, 115, 117, 122–127, energy, 66–70, 89–90, 92, 99, 103, 114–115,
dietary water, See water 166, 182, 205, 208, figs. 1.6, 148, 164, 168, 181, 183–185, 199,
diffraction, diffraction grating , 123, 128 5.3–5.4, 5.12, 5.15, 5.24, 7.4, 9.18 209–210, fig. 3.10
diffusion, 141, 156–158, fig. 6.1, 6.15 frequency, 126 Enhydris, 34
digesta, See chyme “renewal stage,” 125 Enhydris jagorii, fig. 7.6
digestion, 59, 62–70, 109, 111, 114–115, “resting stage,” 125 Enhydris plumbea, fig. 7.6
209, figs. 2.31, 2.37, 4.13 Echis, 182, fig. 8.1 envenomation, See venom
digestive efficiency, 68–69 Echis carinatus, fig. 8.1 enzyme, enzymatic activity, 58, 61, 63–67,
rate of, 67–68, fig. 2.37 ecomorph, 138 110, 113, 126
digestive tract, See gastrointestinal tract ectoparasite, figs. 5.15–5.16 Eocene epoch, 20
digging, See burrow ectopterygoid bone, 40, 50 epaxial muscle, 78
Dinodon semicarinatum, 47 ectotherm, ectothermy, 10, 103–116, 173 Epicrates cenchria, fig. 5.12
dinosaur, 5, fig. 2.4, edema, 58, 151 epidermal appendage, 182, fig. 8.7
Dipsadaboa flavida, fig. 5.12 eel, 3, 86, fig. 1.4 epidermal generation, 124
dipsadine (Dipsadinae), 32, 56 efferent duct (of testis), 192 inner epidermal generation, 125–126,
Dipsas, 32, 42 efficiency, 51, 63, 67–68, 85, 93, 138, 184 figs. 5.3–5.4
discontinuous feeding, See periodic feeding egg , 16, 32, 71, 111, 126, 193–200, 203, outer epidermal generation, 11, 125,
disintegrin, 58 208, 210, figs. 4.12, 5.25, 9.7, figs. 5.3–5.4
Dispholidus typus, 58 9.12, 9.13 epidermis, See skin, epidermal generation
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epididymis, 192 False Fer-de-Lance, fig. 7.8 fossorial, See habitat
epiglottal keel, 186–187 fang , 19–22, 24, 26–27, 33, 49–51, 53–57, 61, fovea centralis, 167
epinephrine, 149 170, figs. 1.24, 1.28, 1.42, 2.5–2.6, free nerve ending, See nerve
epithelium, epithelial cells, 54, 64, 2.17, 2.24, 2.25, 2.27 free stream velocity, 84, fig. 3.7
67, 153, 169–173, 176, figs. 2.34, fang sheath, 61 freeze tolerance, 113
7.9 rear-fang , 29, 30 freezing, 113
equilibrium sense, 167, 169 Farancia abacura, 32, fig. 1.50 frequency (of sound), 181, 183–186, 188
Erpeton tentaculatum, 34, 44, 177–178, figs. fasting , 67, 69–70 frequency modulation, 187
2.10, 7.14 fat, See lipids friction, 85–86, 88–90, 92–93, 123, See also
Erycidae (Erycinae), 16 fatigue, 184 resistance
erythrophore, See pigment faveolus, faveoli (of lung), 155, 158, figs. frog, 113, 135, 186, 210, See also prey
Eryx, 16 6.4, 6.11, 6.13, 6.15 frontal bone, 40, 50, fig. 2.6
Eryx colubrinus, fig. 1.20 Fea’s Viper, 22, fig. 1.37
escape behavior, See behavior feces, 63, 65–70, 72 Gaboon Adder or Viper, 21, 69, 170,
esophagus, See gastrointestinal tract blockage or compaction, 66, 69–70 figs. 1.6, 1.28, 2.25, 8.6
estrogens, See hormone: sex steroids feeding (discontinuous, intermittent or gall bladder, 65, 192–193
estuarine, See habitat, habits periodic), See behavior gape, 38, 41, 48–53, 61, 96, figs. 2.9, 2.16,
Eunectes, 16 fenestra, 39, fig. 2.4 2.18, 2.25, 2.28
Eunectes murinus, 14, figs. 1.18–1.19, Fer-de-Lance, 199, fig. 5.11 garter snake, 29, 45, 56, 66, 89, 109, 113,
2.1, 2.12 fertilization, 194–195 118, 134, 166, 199–202, 204–205,
European Adder or Viper, 131–132, 134, fetal membranes, See embryo 208
200, fig. 1.25 Ficimia, 188 gas exchange (respiratory), 123, 141, 153,
evaporation, 70–71, 112, 121–122, 158 file snakes, 18, 42, 85, 108, 120, 124, 145, 159, figs. 6.1, 6.11, 6.16
evaporative cooling, See heat exchange 147–148, 152, 155, 157, 167, 169, cutaneous gas exchange, 123, 145
evaporative water loss, 70–72, 115, 126, 177, 209, figs. 1.23, 6.8 gas exchanger, 141
208 filtration (at capillaries), 147, 151 gas transport, See respiratory gas
resistance to, See resistance fish, 77–78, 135, 177, 181, See also prey transport
evolution, evolutionary history, 4–5, 7–11, fitness, 114, 199 gastric, 64
34, 63, 67, 132, 136, 139, 163, 185, flattening (of body), See behavior gastrointestinal tract, 37, 62, 66–68, 70,
188 flexible-shelled egg, See egg: eggshell 109, 111, 210, figs. 2.2, 2.35
evolutionary (adaptive) radiation or float, 80, 84 cloaca, 63, 65–66, 70, 188, 192–193, 195,
shifts, 7, 16, 20, 26–27, 38, 55, 59, “float-and-wait” foraging, See behavior 208, figs. 2.35, 9.3, 9.7
85–86 Florida Banded Water Snake, fig. 1.47 esophagus, 38, 62–64, 72, fig. 6.12
excretion, 65, 70–71 Florida Cottonmouth, See cottonmouth intestine (small, large), 62, 64–67, 70,
exhalation, 94, 185–186, fig. 6.14 Florida Green Water Snake, figs. 4.8, 5.8 202, figs. 2.33–2.37, 9.5
expiration, See exhalation Florida Redbelly Snake, fig. 1.48 stomach, 38, 62–64, figs. 2.31–2.34, 2.37
extinction and decline, 11, 138, 191 Florida Worm Lizard, fig. 1.4 gene, 113, 132, 137, 138, 170, 191, 199
extracellular fluid, 113 flow (of blood), See blood generation, 191
extraembryonic membranes, See embryo Flowerpot Blind Snake, Flowerpot Snake, genetic drift, 62
eye, 3, 7, 11, 16, 19, 22, 33, 122, 127, 164–167, 12, 195, fig. 1.11 genetics and genomics, 9, 132, 136–138,
175, figs. 1.4, 1.11, 1.14, 1.20, fluorescence, 127 See also color
1.23, 3.16, 7.1–7.6, 7.12 flying snake, 30, 98 genotype, 114
color, fig. 1.53 “focal point” (of eye), 165 geologic table or time scale, fig. 1.7
cornea, 164–165 folklore, 59, 124, 169, 184, 191 Gerarda, 33
eyelid, 7, 35 follicle, See egg Gerarda prevostiana, 38
iris, 164–165 follicle stimulating hormone, See Gerard’s Water Snake, 38
lens, 164–165, 167, fig. 7.3 hormone gland, 11, 58, 193, 195
pigment, fig. 7.1 food, See prey gastric gland, 64
pupil, 21, 164–166, figs. 1.5, 7.1–7.2 food supplementation, 66 postcloacal, cloacal, or musk gland, 13,
horizontal pupil, 167, fig. 7.5 foraging , See behavior 205
“keyhole,” 167, fig. 7.5 foramen, 159, fig. 6.19 venom, See venom
retina, 164–167, 202, fig. 7.3 force, 183–184, fig. 8.4 gliding, 30
sclera, 164 propulsive force, 51, 78, 81, 83, 85–87, glossary, 213
vitreous fluid, 165, fig. 7.3 89, 93, figs. 2.16, 3.4–3.5 glottis, 153, 156, 185, 187, figs. 2.18–2.19, 8.5
eyecap, See spectacle reaction force, 87, 89, figs. 2.16, 3.4–3.5, Gloydius blomhoffi, 22
Eyelash Pitviper, fig. 1.34 3.10 glucose, 113
thrust, 83–85, 87, fig. 3.5 glycolysis, 184
facial pit, 16, 22, 173–176, figs. 1.5, 7.4, force vector, See vector goanna, See lizard: varanid
7.11–7.12 Fordonia, 33 gonad, 192–193, 201, 203–204
facultative endothermy, See endothermy forest pit viper, 22 ovary, ovaries, 192, fig. 9.6
False Coral Snake, 32, fig. 1.14 fossil, fossil record, 5–7, 11, 185, fig. 1.19 testis, testes, 78, 192, 195, fig. 9.5
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gonadotropic hormones, See hormone head, 11, 13, 19–20, 22, 26, 33, 37–38, horizontal undulatory progression, See
gonadotropin, gonadotropins, See 42, 50–51, 53–54, 60, 85, 87, behavior: locomotion: lateral
hormone : gonadotropic 92–95, 98, 109–110, 112, 124, undulation
hormones 146, 151–152, 163, 167–168, 181, hormone, 136, 142, 149, 193
gonadotropin-releasing hormones, See figs. 1.11, 1.15, 1.24, 1.30, 1.42, gastrointestinal hormones, 66
hormone 2.16, 3.5–3.6, 7.4, 7.6, 8.6 gonadotropic hormones,
Gonyosoma oxycephalum, 132, 159, 187, head swaying, See behavior gonadotropins, 203
figs. 5.18, 6.19 head pit, See parietal pit follicle stimulating hormone, 203
Gopher Snake, 182, 186 hearing , 167–169, 183, 189 leutinizing hormone, 203
granular scales, See scale heart, 78, 113, 142–145, 147–148, 150–152, gonadotropin releasing hormones,
gravid, 109, 208 155, figs. 6.1–6.3, 6.5, 6.9 203
gravitational pressure, 150–152, heart rate, 149 reproductive hormones, 201
figs. 6.7–6.8 heat, 22, 103, 106, 108–109, 111, 142, 173, sex steroids, 204
gravity, 86, 96, 99, 147, 150–153, 175, 209 androgens, 204, 208, fig. 9.17
figs. 6.6–6.9 heat exchange, 108–109, 122, 129, 158, testosterone, 203
Green Anaconda, See anaconda figs. 4.1, 4.6 estrogens, 203, 208
Green Tree Python, 17, figs. 1.22, 7.1 conduction, 103, 158, 173, fig. 4.1 progesterone, 203
Grenada Bank Tree Boa, figs. 2.20, 3.17 convection, 103, fig. 4.1 horn (over eyes), fig. 3.16
ground snake, 26 evaporative cooling, 112, 158, house snakes, 20
growling , See behavior figs. 4.1, 4.13 Hox genes, 7–8
growth, 66, 114–115, 126, 135, 182, 193, 198, radiation, 103, 107, 121–123, 158, humans, 78, 80, 127
209–210 173–175, figs. 4.1, 4.9 humming bird, 103
growth rate, 210 heat stress, 112 hump-nosed pit vipers, 22
guanine, 128 hematocrit, 148 hyaluronic acid, 58
Gulf Salt Marsh Snake, 44 heme, 156 hyaluronidase, 58, 63
gut, See gastrointestinal tract Hemeroplanes ornatus, fig. 5.21 hydration, 121
gut passage time, See passage time hemipenis, hemipenes, 192, 208, hydrochloric acid, 64
Gyalopion, 188 figs. 9.3, 9.4 hydrophiine (Hydrophiini), 27, 29, 71, 85,
Gyalopion canum, 188 hemodynamics, 148–149 170
hemoglobin, 127, 142–143, 148, 156 Hydrophis, 27, 29, 85
habitat, habits, hemorrhage, 147 Hydrophis donaldi, fig. 8.8
aquatic, 6, 18, 19, 29, 32–33, 44, 71, 78, hemotoxic, 58 Hydrophis elegans, fig. 3.6
80, 84–86, 108, 117, 122, 124, 141, henophidian (Henophidia), 12–13, 34, 166 Hydrophis melanocephalus, fig. 3.6
145, 147–148, 150–153, 155–158, hepatic portal vein, 147, figs. 6.5–6.6, Hydrophis ornatus, fig. 1.45
160, 164, 166–168, 170, 177–178, 6.16 hydrophobic, 121–122, 136, fig. 5.11
189, 196, 199, 205, 210, figs. 6.8, herpetoculture, 191, 200 hydrostatic indifferent point, 150
7.14 hertz (Hz), 181 hydrostatic pressure, See gravitational
amphibious or semi-aquatic, 29, 83, Heterodon, 32, 132 pressure
86, 122, 158, fig. 3.8 Heterodon nasicus, fig. 1.49 Hypnale, 22
estuarine, 34, fig. 8.8 Heterodon platyrhinos, 187 hypothalamus, 112, 202–203
freshwater, 34 Heterodon platyrhinos platyrhinos, Hz, See Hertz
marine, 7, 18, 29, 34, 71–72, 84, 86, 137
108, 120, 123, 126, 148, 159, 196, hibernation, See dormancy ice-nucleating proteins, 113
199, 205, figs. 1.43, 3.8, 6.8 high altitude, 196 iconography, fig. 5.14
arboreal, semiarboreal, 16–17, 22, 26, 30, Hill Death Adder, fig. 6.18 iliocostalis, See muscle
32, 33, 50, 53, 56, 69, 78, 89–90, hinge (of scale), See scale Imantodes, 32
95–98, 132, 150–153, 159, 164, hinged teeth, 54 Imantodes cenchoa, fig. 1.51
166–167, 199, figs. 1.22, 1.31, hiss, hissing , See behavior immune response, 115
1.34, 1.38, 3.18–3.19, 6.19, 7.5 H2O, See water incidental drinking, See behavior:
fossorial, 12, 32, 90, 108–109, 166, 168, hog-nosed pit viper, 22, fig. 1.35 drinking
188, 199, 204, See also behavior: hognose snake, 32, 132 incubation (of eggs), 198, figs. 9.13, 9.14
burrowing homalopsid (Homalopsidae), 12, 17, Indian Egg-eating Snake, fig. 2.1
pelagic, 27, 84, 124 33–34, 44, 47, 70, 92, 167, indigo snake, 30, 45
terrestrial, 6, 86, 89–90, 97, 108, 123, figs. 7.6, 7.14 inertial force, See resistance
143, 151–153, 156, 160, 166, 170, Homalopsis buccata, fig. 1.54 inflammation, 58
199, 205 homology, 10 inflation, 159–160
Habu, 22, fig. 1.30 homoplasy, 10 infraorder, 11
hair cell receptors, See receptor hood, See behavior infrared receptor, See receptor
harmonic, 186, 188 hook-nosed snakes, 188 infrared radiation, See radiation
hatching (of eggs), See birth Hopi Rattlesnake, fig. 1.29 infrared thermometer, fig. 4.4
hatchling, See neonate horizontal pupil, See eye ingestion, See prey transport
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inhalaton, 94, 156, 185–187 labyrinthodont, 5 limb, limb girdle, 5–8
inheritance, 192 Lachesis muta, fig. 1.33 forelimb, 8
inner ear, See ear lactate, lactic acid, 184 limbless lizard, 89
inner ear cells, See hair cells lacunar cells or tissue, 125–126, fig. 5.4 lingual, 54, fig. 2.21
inner generation (of epidermis), See lamellar granules, 71 lipids, 65–66, 71, 118–119, 124, 126, 205,
epidermal generation Lampropeltis, 30 fig. 5.4
insect, 184, See also prey Lampropeltis californiae, 126, 138, lamellar lipids (of permeability barrier),
inspiration, See inhalation figs. 2.7, 5.26 125
integration (sensory), 173 Lampropeltis elapsoides, fig. 5.19 reserves, 193
integrin, 58 Lampropeltis getula, fig. 6.11 litter, litter size, See clutch
integument, See skin Lampropeltis campbelli, fig. 9.7 Little File Snake, 42, 157, 177, figs. 5.15,
interaortic foramen, 143 Lampropeltis triangulum gaigeae, 6.10
intercostal muscle, 156 fig. 5.19 liver, 65, 67, 78, 147, 193, figs. 6.6, 6.12, 6.16
intermittent feeding, See behavior: lamphrophiid (Lamprophiidae), 12, 17, 19, lizard, 3–7, 10, 34, 39, 40, 54, 58, 77, 80, 89,
feeding 20, 34 99, 104–105, 110, 112, 134–135,
internal organs, See viscera Lamprophis, 20, 200 145, 158, 195–197, 199, 202, 209,
interstitial fluid, 145, 147 Lamprophis fulginosus, 200 figs. 1.4, 2.4, See also prey
interventricular canal, 144 lancehead, 22 Earless monitor, 7
intestine, See gastrointestinal tract Lanthanotus borneensis, 7 Gila Monster, 4
intracardiac shunt, See shunt Lapemis curtus, 169, figs. 5.9, 6.10 legless lizard, fig. 1.4
invasive (wildlife), 210 large intestine, See gastrointestinal tract skink, 7
ions, 117 larynx, 185–186 varanid, 4, 7, 211, fig. 1.8
iridescence, 13, 123, 127, fig. 5.12 laryngeal septum, 186–187 locomotion, See behavior
iridophore, 128 lateral resistance, 80 Loggerhead Sea Turtle, fig. 2.14
iris, See eye lateral undulation locomotion, See longevity, 210
island, insular, 48, 53, 62, 210 behavior longissimus dorsi, See muscle
Laticauda, 71, 85, 198, 210 loreal pit, See facial pit
Jacobson’s organ, See vomeronasal organ Laticauda colubrina, 48, 50, figs. 1.43, Loxocemidae, 13
Jagor’s Water Snake, fig. 7.6 2.15, 3.8, 6.8, 7.8 Loxocemus bicolor, 13, figs. 1.16, 3.15
Jameson’s Mamba, See mamba Laticauda laticaudata, figs. 1.43, 3.8 lubrication, 124
jaw, 4, 11, 16, 19, 35, 37–42, 50–51, 54, 57, Laticauda semifasciata, 85, figs. 1.43, 3.8, lumen, 60, 65
168, figs. 1.8, 1.20, 2.1, 2.7–2.9, 5.11, 6.14, 6.16, 9.4 lung, 78, 80, 141–145, 147–148, 153–160,
2.16, 2.23, 3.15 laticaudine (Laticaudini), 27, 29, 71, 170, 185–186, figs. 6.1, 6.4–6.5, 6.9,
Jerdon’s Pit Viper, fig. 1.30 fig. 1.43 6.11–6.13, 6.15–6.17, See also
joints, 169 “Law of Pascal,” 150, fig. 6.7 tracheal lung
jugular vein, 147, fig. 6.5 Left-to-right shunt (L-R shunt), See shunt volume of, 155, 158–159, 185
jump, jumping, See behavior leg , 6 Lycodon omorphus, 20
jumping pit viper, 22, 95 length (body length), See body lymph, lymphatic fluid, 147–148
Central American Jumping Pit Viper, lens, See eye lymphatic vessel, 147
fig. 1.36 lepidosaur (Lepidosauria), 4, 34, 119, 124,
Jurassic period, 6 fig. 1.10 malacophagy, See prey: gastropods
Leptodeira Malayan Pit Viper, 22, 62
keel, 13, 120, 186, figs. 3.1, 5.7, 5.10 Leptodeira annulata, fig. 3.4 mamba, 24–26, 55, 89, 96
Keel-bellied Watersnake, 33 Leptodeira nigrofasciata, fig. 3.4 Jameson’s Mamba, fig. 1.38
keeled scale, See scale Leptodeira septentrionalis, fig. 2.17 mammal, 5, 26, 62, 64, 66, 70, 78, 81, 99,
keratin, 4, 22, 71, 119, 126–128, 182 Leptotyphlopidae, 11, 41, fig. 1.11 103, 106, 111–112, 137, 143, 145,
alpha (α), 4, 71, 119–120, 125–126, Leptotyphlops, 55, 192 149, 151, 155, 158, 167–169, 177,
figs. 5.3–5.5 Leptotyphlops ater, 90, fig. 1.12 192–193, 201, 209
beta (β), 4, 119, 124–126, figs. 5.3–5.5 Leptotyphlops carlae, 11, fig. 1.12 Mamushi, 22
keratinization, 125 Leptotyphlops dulcis, 12 mandible, 42, 50, 51, figs. 2.8, 2.18–2.19,
keratinocyte, 119, 128 Leptotyphlops humilis, 127 2.23
kidney, 65, 70–71, 78, 192, figs. 2.2, 2.35 Leucorampha ornatus, See Hemeroplanes mandibular raking, 41, 42
kinematics, 88 ornatus mangrove snake, 30
kinesis, 38–40, 42, 51 leutinizing hormone, See hormone Many-banded Krait, fig. 1.40
kinetic skull, See streptostyly Lialis burtonis, fig. 1.4 marine (form or habits), See habitat,
King Cobra, See cobra Liasis fuscus, 111 habits
king snake, 30, fig. 6.11 Lichanura trivirgata, 16 mass (of snake), See body
krait, 24, 26, See also sea krait “lie-and-wait” foraging, See behavior Masticophis, 30
Kukulkan, fig. 5.14 lift, 98 Masticophis flagellum, 47, 67, fig. 2.14
ligament, 40 Maticora, 26
labial pits, See facial pit light, See radiation: visible mating, See behavior: reproductive
labial scales, fig. 7.4 light receptor, See receptor: photoreceptor behavior
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mating “ball,” See behavior: reproductive Micrurus, 131, 188 M. spinalis-semispinalis, 78, 183, fig. 3.3
behavior Micrurus decoratus, fig. 5.19 M. supracostalis lateralis, 183
maxilla, maxillary bone, 16, 19, 40–42, Micrurus fulvius, 188, fig. 5.19 smooth muscle, 65–66, 145, 149,
50, 51, 54–57, 61, figs. 2.5–2.6, Micrurus nigrocinctus, fig. 5.19 158, 175, 187, 192–193,
2.24 midbrain, 169 figs. 2.34, 6.11
mean selected temperature, See preferred milk snake, 30 tension, 111
body temperature mimicry, 132, 189, figs. 5.19, 5.21 twitch, 183–184
measurement of temperature, fig. 4.4 mineralized shell, See egg: eggshell: muscular ridge, fig. 6.3
mechanical cues or signals, See “rigid-shelled egg” musk, 182
mechanoreception mitochondria, 141, 156, 182 musk gland, See gland
mechanical work, 183–184 mobility of jaw or joints, 78, See also mutation (genetic), 9, 62, 138, 189, 191
mechanoreception, 49, 123, 177–178, 189, behavior, kinesis, streptostyly Myrichthys colubrinus, fig. 1.4
206 modality (of stimulus), 163 mythology, 117, 124, 191, figs. 5.1, 5.14,
mechanoreceptor, See receptor “mode,” of locomotion, See behavior 9.1–9.2
melanin, See pigment “mode,” reproductive, See reproduction
melanism, 132, 134–135, 138 moisture, 198 Naja
melanocyte, See pigment molecular data, methods, properties, or Naja atra, figs. 1.39, 2.26
melanophore, See pigment studies, 4, 9, 13, 24, 34, 62, 166, Naja shrionegrina, 6
melanophore stimulating hormone fig. 1.9 nanopit, 174
(MSH), 136 mole vipers, 19–20, fig. 1.24 nanoscale, See microsculpture
melatonin, 136, 202–203 momentum, 95, fig. 3.12 narial or nasal valve, See valve
membrane, 22, 65, 70, 163, 168, 173, 175, monitor lizard, See lizard: varanid naris, nares, See nostril
185, 193–195, fig. 7.11 monophyletic lineage, 7, 10, 11, 17, 32, 34 nasal bone, 40
eggshell membrane, 195, fig. 9.11 monotypic, 27, fig. 1.14 nasal cavity or passages, 169–170, 187,
mesos layer (of skin), 119, 125, Morelia fig. 7.9
figs. 5.3–5.5 Morelia amethystine, 17 nasal hissing, See behavior
metabolic water, See water Morelia spilota, 111, fig. 6.12 “nasal pore,” 176
metabolism, 70, 209 Morelia viridis, 17, figs. 1.22, 7.1 nasal receptors, See receptor
rate of (metabolic rate), 46, 66–67, 69, morphology, 34 natricine (Natricinae), 29, 40, 42, 46–47,
103, 106, 114–115, 135, 157, 200, morphological color change, See color: 122, 199, fig. 9.10
fig. 2.36 color change Natrix, 29
metabolic heat production, 105–107, mortality, 196 natural history, 204
111–112, fig. 4.1, 4.13 mosasaur, 7, fig. 1.8 natural selection, 10, 59, 62–63, 130, 136,
metabolic wastes, 197 motor sensory system, 175 152, 189
methyl ketone, 118, 205 mouth, 11, 20, 37, 49, 51, 56, 61–62, 72, neck, 62, 87, 92–93, figs. 3.5–3.6
Mexican Burrowing Python, 13, 172–173, figs. 2.16, 2.19, 2.25, neck sac, See tracheal air sac
figs. 1.16, 3.15 5.18, 8.5 necrosis, 58
Mexican Vine Snake, See Brown Vine MSH, See melanophore stimulating neonate or hatchling, 126, 198, 201, 208–
Snake hormone 209, figs. 9.9, 9.11–9.12, 9.15
microarchitecture, See microsculpturing mucosa, mucosal cells, 60, 65, 67, 72, Neotropical Bird Snake, See Puffing Snake
microbe, 117 fig. 2.34 Neotropical racer, fig. 1.48
microdermatoglyphics, See mucus, 56, 64, 176 Nerodia, 29, 40, figs. 1.3, 1.47
microsculpturing mucous cells, glands or secretions, 62, Nerodia clarkii, 44
“microfacets,” 172 172, 193 Nerodia fasciata, 85
microfibril, See microsculpturing Mud Snake, 32, fig. 1.50 Nerodia fasciata pictiventris, fig. 1.47
microgravity, 169 muscle, musculature, 13, 22, 40, 51, 57–58, Nerodia floridana, figs. 1.47, 4.8, 5.8
“micro-hairs,” See microsculpturing 60–62, 72, 77–78, 80, 85, 87–91, Nerodia sipedon, 48, 205
microornamentation, See 96, 111, 113–114, 118, 143, 146, nerve or neuron, 66, 111, 113, 117, 127, 163,
microsculpturing 156, 158, 160, 165, 169, 182, 183, 168, 172, 175–177, 201
micropit, 174–175 185–186, 188, 195, figs. 3.5, 6.16, free nerve ending, 173, 177
micropore, 124 7.10 nerve growth factor, 58
microsculpturing (of scales), axial muscle, 78–79, 87, 92, figs. 3.3, 3.9 nerve signal, See action potential
121–125, 127, 136, 177, cardiac muscle, 143–144, 148–149 nervous control, 145, 201, fig. 6.9
figs. 5.10, 5.13 ciliary muscle, 165 nervous system, 149, 177, 201
microfibril, 123 costocutaneous muscle, 91, fig. 3.12 central nervous system, 78, 110, 149,
“micro-hairs,” 123 compressor glandulae, 60 163, 173, 177, 181, 203
nanoscale structure, 123 compressor muscle, 60 nest, 198, fig. 9.14
microstructure, See microsculpturing constrictor laryngis, 186 net cost of transport, 99
microvasculature, 148 epaxial muscle, 78, 88, 97 neural arch, fig. 3.2
microvilli, 172 M. iliocostalis, 78, 183, fig. 3.3 neuroendocrine regulation, 201–202,
Micruroides, 131, 188 M. longissimus dorsi, 78, 183, fig. 3.3 fig. 9.16
Micruroides euryxanthus, 188 M. sphincter cloacae, 188 neuromodulator, 201, 203
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neuromuscular control, 98 ovary, ovaries, See gonad Pelamis, 71
neuron, See nerve overwintering, 94, 108, 118, 122, fig. 4.7, Pelamis platurus, 27, 44, 81, 84, 124, 138,
neurotoxic, 58 See also behavior 159, 169, 177, figs. 1.44, 2.9, 2.24,
neurotransmitter, 149 oviduct, 192–195, 197, 203, fig. 2.35 3.1, 3.5, 5.7, 5.9, 5.15, 5.27, 6.10,
night adders, 21, 176 oviparity, oviparous, 12–13, 16, 19, 21, 7.1, 9.8–9.9
Nina sebae, fig. 5.20 25, 27, 29, 32–33, 71, 195, 197, pelvis, pelvic girdle, 5, 6, 11, fig. 1.14
nitrogen, 145 199–200 pelvic spur, 5, 11, 206, fig. 1.14
nitrogenous wastes, See urates, uric acid oviposit, oviposition, 195, 197–198, 208, peptide, 58
nocturnal, See behavior figs. 9.7, 9.12 performance, 85–86, 96, 110, 114–115, 151,
node (of phylogenetic tree), 9, 34 ovulation, 193–194 173
norepinephrine, 149 oxidation, 127, 141 performance breadth, 114, fig. 4.14
Northern Black Racer, 137 Oxybelis aeneus, figs. 1.48, 2.18, 5.18 performance curve, 110, 114, fig. 4.14
Northern Copperhead, See copperhead oxygen, See respiratory gases periodic feeding, See behavior: feeding
Northern Rubber Boa, 110 oxygen affinity, 148, 157 peripheral resistance, See resistance
Northern Water Snake, 199, 205 oxygen capacity (of blood), 148, 156 peristalsis, 38, 65, figs. 2.14, 2.30
Northwestern Garter Snake, 130 Oxyuranus, 26 peritoneum, 135
Nose-horned Viper, fig. 1.25 permeability, 117, 121, 197
nostril, 16, 19, 22, 33, 94, 153, 176, 187, “pacemaker,” 143 of capillaries, 147
figs. 1.23, 6.10, 7.4, 7.11, 8.6 Pacific Rattlesnake, See Southern Pacific permeability barrier (to water), 71–72,
Notechis, 27, 53 Rattlesnake 126, figs. 5.3–5.4
Notechis ater niger, fig. 4.15 paddle, See tail Permian period, 5, figs. 1.7, 1.8
Notechis scutatus, 85–86 pair bonding , See behavior pH, 61, 64, 157–158
nutrient, 62, 66–67, 69, 142, 145, 195, 197 palate, palatine bone, 41, 51, 55–56, 171, pharynx, 62, 153
nutritional status, 62, 148 173, fig. 2.6 phenogram, See phylogenetic tree
palatomaxillary bones (arch or bar), 40, phenotype, 5
oberhautchen, 119, 121, 123–124, 126, 50, 61 phenotypic plasticity, See plasticity
figs. 5.3–5.5, 5.10 palatopterygoid bar, bones, 41 phenotypic trait, 9, 114
odor, 11, 49, 170, 172–173, fig. 2.38 Paleozoic era, 5 pheromone, 118, 205, 208
olfaction, 169–173, 205 Palestine Viper, fig. 7.2 “sexual attractiveness pheromone,” 205,
olfactory bulb (of brain), 171 palm viper, 22 fig. 9.18
olfactory epithelium, 169–171 Blotched Palm Viper, fig. 1.34 phospholipase, 58
olfactory receptors, See receptor pancreas, 65 photoperiod, 200, 202
Olive-headed Sea Snake, fig. 5.16 Pantherophis, 30, 151, fig. 6.5 photoreceptor, See receptor
Olive Sea Snake, 177, 210 Pantherophis alleghaniensis, figs. 2.19, phylogeny, phylogenetic tree, 4–5, 8, 9–10,
omphalallantoic placenta, See placenta 2.30 19, 34, 55, figs. 1.8–1.10, 1.55
ontogeny, ontogenetic, 48, 53, 136, Pantherophis guttatus, 86, 96, figs. 7.9, physiological color change, See color
148 9.5 physiological thermoregulation, 110–112
ontogenetic color change, See color Pantherophis obsoletus, 111, figs. 1.48, panting, 112, 158
Opheodrys, 30 2.37, 3.3, 3.18, 9.13, 9.15 pigments, 11, 122, 127, 136, 142, See also
Ophidia, 11, 34, 35 panting , See physiological hemoglobin and iridophore (not
ophiophagous, 45 thermoregulation a true pigment)
Ophiophagus hannah, 26, 159, 187, 198, papilla, papillae (sensory), 172–173 carotenes, 128
figs. 2.11, 4.5, 9.14 Paradise Tree Snake, 98, fig. 3.19 chromatophores, 127–128, 136
Ophisaurus ventralis, fig. 1.4 Pareas, 33, 42 erythrophore, 128
opisthoglyphous, 57, 61 Pareas formosensis, fig. 1.53 melanin, 127–128, 135, 137
opossum, 62 pareatid (Pareatidae), 12, 17, 33–34, 42, 56, melanocytes, melanophores, 127–128, 136
opsin, 166 fig. 1.53 pteridine, 128
optic tectum, 175 parenchyma, 153, 155–158 xanthophores, 128
oral secretions or tissues, 172 parental care, See behavior pineal gland, 202–203
Oriental Coral Snake, fig. 1.41 parietal bone, 40, 60, fig. 2.6 Pine Snake, 186
Oriental Whipsnake, fig. 7.5 parietal (head) pit, 177 pipe snakes, 12, 13, fig. 1.13
orientation, 169 parthenogenesis, 12, 195 Asian pipe snakes, 13
Orsini’s Viper, 21 partial pressure (of gas), 141, 145, 149, Red Pipe Snake, 13, fig. 1.14
oscillator, 183 156–157, fig. 6.15 piscivorus, See prey: fish
osmosis, osmotic flux, 70–71 parturition, See birth pit (of scale surface), 177
osmotic concentration, 113 passage time (ingestion to defecation), pit organs, See facial pit
osteoderm, 54 68–69 pituitary gland, 136, 203
outer generation (of epidermis), See PBT, See preferred body temperature pituitary hormones, 136
epidermal generation peg (as resistance site), 88–89, Pituophis
oval window, 168 figs. 3.9–3.10 Pituophis catenifer, 182, 186
ovarian follicles, 193 pelagic, See habitat, habits Pituophis melanoleucus, 111, 186–187
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pit viper, 20, 22, 24, 47–48, 56, 120, 126, 158, prey, 3, 20, 22, 25, 33, 37–38, 40–41, 46, 48– Pseudonaja
173, 175–176, 208, figs. 1.33, 7.11 51, 53–54, 56, 59, 61–63, 66–68, Pseudonaja nuchalis, 26–27
placenta, placentation , 195, 197, figs. 9.8, 95–96, 115, 120, 152, 167, 173, 175, Pseudonaja textilis, 27
9.10 188, 200, 209–210, fig. 1.24 Pseustes poecilonotus, figs. 1.48, 2.18
chorioallantoic placenta, fig. 9.10 amphibians, 33, 48 pteridine, See pigment
omphalallantoic placenta, fig. 9.10 anurans (frogs, toads), 21, 32, 38, pterygoid bone, 41, 42, 50, 55, fig. 2.5
placental membranes, fig. 9.10 45–46, 48, 50, 53, 62, 66–67 Pueblan Milksnake, fig. 9.7
Plains Gartersnake, 199 birds, 16, 20, 38, 45–46, 48, 50, 53, Puff Adder, 21–22, 176, 186–187
plants, 68 67–68, 97, fig. 2.37 Puff-faced Water Snake, fig. 1.54
plasma, See blood plasma caecilians, 19 Puffing Snake, figs. 1.48, 2.18, 8.5
plasticity (developmental, ontogenetic, carrion, 21, 45 pulmonary artery or trunk, 143–147,
physiological, phenotypic), 53, eggs, 37, 45, 47, 97, figs. 2.1, 2.14, 2.19, figs. 6.3, 6.5, 6.16
86, 114, fig. 4.14 2.30, 3.15 pulmonary circulation, 147
pleurodont, 54, fig. 2.21 fish or fish eggs, 13, 19, 26–27, 33, 38, pulmonary vein, 147, fig. 6.5
“Plumed Serpent,” fig. 5.14 45–48, 50–51, 54, 56, 64, 67, 84, pupil, See eye
Pogona vitticeps, fig. 2.5 178, figs. 1.44, 2.10, 2.13, 7.14 purine, 128
point of force application, See resistance eel, 13, 27, 46, 50 push point, See resistance site
site invertebrates, 33, 38, 45, 189 pygmy rattlesnake, 22
poison, 57–58 crabs, 33, 38 pylorus, 64
polymorphism, 132, See also color centipedes, 19–20 pyloric valve, 64
polypeptide, 58 crustaceans, 19, 33, 67, fig. 2.22 python, 5, 8, 12–16, 34, 50, 55, 67, 69,
polyphyletic, 34 earthworms, 13, 20, 32, 38 91, 108–111, 120, 172–174, 176,
pooling (of blood), 151–152, figs. 6.7–6.8 gastropods (slugs, snails), 32–33, 42, 208–210
pore, 172, 174, 176, figs. 5.13, 9.13 56, fig. 2.8 Python brongersmai, fig. 5.25
portal vein, See hepatic portal vein insects, 12, 21, 37–38, 45, 67, 167 Python curtis, 69
Porthidium, 22 larvae or pupae, 41 Python molurus, 16, 67, 69, 111, 175,
Porthidium nasutum, fig. 1.35 mammals, 13, 16, 20, 38, 46, 48, 50, figs. 2.36, 4.10, 6.4
postcloacal musk gland, See gland 67–68, fig. 2.32 Python regius, 16, 166, 168
postmating behavior, See behavior: deer, fig. 2.1 Python reticulatus, 14, 16, fig. 1.17
reproductive behavior rodents, 20, 49–50, 176, figs. 2.36, 3.16 Python sebae, 16
postprandial calorigenic response, See mice, 13, 38, 45, 50, 53, 63, 169, pythonid (Pythonidae), 16, 205
specific dynamic action figs. 2.7, 2.16, 4.13
postprandial metabolic response, See shrews, 20 quadrate bone, 6, 39–40, 51, 168–169,
specific dynamic action reptiles, 13, 20–21, 25 figs. 2.5–2.6
postprandial thermogenesis, See specific lizards, 13, 32, 45–46, 48, 62, 167, 189, quadratojugal bone, 6
dynamic action fig. 3.16 quadrupedal, 77
posture, See behavior geckos, 16 Queen Snake, 29
power, 80, 85 skinks, 16, 19, 54
power spectrum, 187 snakes, 13, 19, fig. 2.11 racer, 26, 30, 45–46, 77, 89, 96, 99, 135,
Prairie Rattlesnake, fig. 1.29 turtles, 47, figs 2.12, 2.14 181, 205
Prairie Ringneck Snake, fig. 1.50 vertebrates, 20 radiation (electromagnetic)
prebutton (of rattle), 182 prey handling time, 59 infrared, 22, 173–176
precourtship behavior, See behavior: prey transport, 38–42, 45, 66–70, figs. solar, 107, 117, 158, fig. 4.11
reproductive behavior 2.11. 2.13–2.14, 2.19, 2.37–2.38 ultraviolet, 135, 174–175
predator, predation, See behavior primitive trait or lineage, See basal visible, 163–165, 174–175, 201
preferred body temperature (PBT), progesterone, See hormone: sex steroids radiation (evolutionary), See evolution
109–110, 113, 148 prokinesis, 40 radiotelemetry, radio transmitter, 47, 105,
preferred range, See preferred body proprioceptors, 169 109, figs. 4.4–4.5, 4.9
temperature propulsive force, See force Rainbow Boa, fig. 5.12
prefrontal bone, 40, 50, 56 protease, 58, 65 “Rainbow Serpent” (of mythology), 191
prehensile tail, See behavior protein, 4, 62, 65–67, 69–70, 113, 166, 182 Ramphotyphlops braminus, fig. 1.11
premaxilla, premaxillary bone, 55, 71, 198 proteolytic enzymes, 58, 64 rat snake, 30, 46–47, 78, 96–97, 111, 151,
pressure proteroglyph, 57, 61 169, figs. 2.26, 3.3, 6.5, 6.9, 6.19
blood pressure, See blood Protobothrops rattle (of rattlesnake), 182–185, 188–189,
in fluids, 150, 169, fig. 6.7 Protobothrops flavoviridis, 22, fig. 1.30 figs. 5.14, 8.2–8.4
in lung, 156, 186 Protobothrops jerdoni, fig. 1.30 rattling, See behavior
oxygen, See partial pressure protraction , 41 rattlesnake, 22, 47–49, 51, 56, 63, 66, 80,
transmural pressure, fig. 6.7 Psammophis, 20 112, 136, 173, 175–176, 182–185,
water vapor, See water Psammophis subtaeniatus, figs. 5.10, 5.13 187–189, 200, 208, figs. 1.29,
pressure shunting, See shunt: intracardiac Pseudechis porphyriacus, 25, 27, 108, 211, 5.14, 6.9, 8.2
shunt fig. 4.9 RCM, See relative clutch mass
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reabsorption, 54 friction, 87, 93, 99 Saw-scaled Viper, 182, fig. 8.1
reaction force, See force gravitational vertical force, 84 scale, 3, 10–11, 13, 51, 54, 89, 93, 117,
reaction norm, 114 inertial, 84–85, 89 119–124, 126–127, 175, 177, 188,
reaction site, See resistance site viscosity, 84 figs. 1.6, 1.23, 5.6, 5.8–5.12, 7.11
rear-fanged, 50 resistance site, 80, 87–88, 93–94, 96, granular, 18–19, 120
receptor, 58, 127, 149, 163, 168, 172–175, figs. 3.4, 3.9, 3.12 head plates or scales, 11, 21–22, 51, 120,
177, fig. 1.5 resources, 200–201 177, fig. 1.15
baroreceptor, 149 respiration , 114, 141, 143, 156, 158 hinge, 120
chemosensory receptors, 173 respiratory gases 117, 145, 148, 153, keeled, 19–20, 44, 120, 182,
cutaneous receptors, 177, 189 155–157, 185, 195, 197 figs. 5.9–5.10, 8.1, 8.8
hair cell receptors, 168–169, 177, fig. 7.7 exchange, See gas exchange labial, 16
infrared receptors, 173–175, fig. 1.5, See carbon dioxide, 117, 141, 146, 153, scute or ventral, 11, 18, 78, 87, 89–91, 120,
also facial pits 156–158, 185, fig. 6.1 figs. 3.1, 3.12, 5.6–5.7, 5.9, 5.12, 9.3
mechanoreceptor, 45, 176–178, fig. 2.10 oxygen, 46, 113, 117, 141–142, 145–146, smooth, 11, 13, 19, 21–22 120, figs. 1.11,
nasal receptors, 170 148, 153, 156–158, 160, 185, 195, 5.8
olfactory receptors, 170 197, figs. 6.1, 6.15 spine or spinous, 18, 121, 177,
photoreceptor, 166, 177–178, fig. 7.3 respiratory gas transport, fig. 6.1 fig. 5.8–5.9, 8.8
stretch receptor, 149, See also resting stage (of shedding cycle), See tuberculate, 18, fig. 5.9
baroreceptor ecdysis scanning electron microscopy (SEM), 121,
thermoreceptors, 173–177 Reticulated Python, 14, 16, 199, figs. 1.17, 174, fig. 5.10
visual receptors, 127, 164 2.23, 9.6 scansorial, See behavior: locomotion:
cones, 164, 166–167 retina, See eye climbing
rods, 164, 166 retraction, retractor muscle, 192 scattering (of light), 128
vomeronasal receptors, 172–173 Rhamphotyphlops braminus, 12, 195, Schultheis thermometer, 105, fig. 4.4
rectilinear locomotion, See behavior: fig. 1.11 sclera, See eye
locomotion Rhineura floridana, fig. 1.4 scolecophidian (Scolecophidia), 11, 12, 34,
Red-bellied Black Snake, 25, 27, 108, 211, Rhinoceros Viper, 21, figs. 1.28, 2.25 41, 55, 173
fig. 4.9 rhinokinesis, 40 Scrub Python, 17
red blood cell, 142, 148, 156–157 rib, 3, 6, 78–79, 85, 88, 91, 97–98, 156, 159, scute, See scale
Red Blood Python, fig. 5.25 186, fig. 3.12 SDA , See specific dynamic action
Red Coffee Snake, fig. 5.20 ribbon snake, 29 sea krait, 27, 50, 71, 85, 198, 210, figs. 3.8,
Red Diamond Rattlesnake, 80, 185 Rice Paddy Snake, fig. 7.6 5.11, 6.8, 9.4
Red-sided Garter Snake, figs. 4.2, 4.7, 9.17 right-to-left shunt (R-L shunt), See shunt sea snake, 24–25, 27, 29, 46, 48, 56, 78,
Red-spotted Pit Viper, fig. 1.30 rigid-shelled egg, See egg: eggshell 81, 83–85, 124, 126, 132, 145,
Red-tailed Rat Snake, 132, 159–160, 187, Ringed Python, fig. 4.12 152–153, 157–159, 169–170, 173,
figs. 5.18, 6.19 ringneck snake, 26, 32 177, 189, 208–209, figs. 1.4, 2.15,
reflectance (of light), 128 robotics, 99–100, fig. 3.20 6.9–6.10, 8.8
refraction, 165 Rock Rattlesnake, fig. 1.29 season, seasonality, 114, 193, 201,
Regina, 29 rod (of eye), See receptor: visual receptors figs. 4.15, 9.17
Regina rigida, fig. 2.22 rodent, 94, 103, 210 sea turtle, 47
relative clutch mass (RCM), 199 rostral scale, 11, 94, figs. 1.11, 1.20 secondary sexual characteristics, 203
renal vein, 147 Rosy Boa, 16 secretion, 11, 57, 66, 71
renewal stage (of shedding cycle), See Rough-scaled Bush Viper, figs. 1.27, 5.8 segment (of rattle), fig. 8.2
ecdysis Round Island Boa, 16 selection pressure, See natural selection
replacement (teeth), 55, fig. 2.23 rubber boa, 16 SEM, See scanning electron microscopy
reproduction, 66, 115, 135, 191–212, fig. 9.16 rugae, 64 semiaquatic, See habitat, habits
reproductive cycles, 201, 203–204, Russell’s Viper, 176, 187, fig. 5.10 semicircular canals, 168–169, fig. 7.7
fig. 9.17 seminal or copulatory plug, 208
reproductive mode, 195–197 sacculus, 168–169, fig. 7.7 seminal receptacles, 194
reproductive tract, 65 salamander, 77, 99 Seminatrix pygaea, 29
reptile (Reptilia), 5, 10, 39–40, 71, 80, salivary gland, 59 seminiferous tubules, 192
114, 145, 156, 173, 194, 196, 200, salivary secretions, 62 serous cells or gland, 60
203–204, figs. 1.8, 1.10 salt, 71 “serpent,” 191
non-avian reptile, 10 salt gland, 71 Serpentes, See Ophidia
resistance sand boa, 16 sex, 62, 110, 191–192, 205
forces, 87 Kenya Sand Boa, fig. 1.20 sex steroids, See hormone
to blood flow, 143–145 San Diego Gopher Snake, 104 “sexual attractiveness pheromone,” See
peripheral resistance, 148–149 sand snake, 20 pheromone
to evaporative water loss, 124, 126 sand swimming, See behavior sexual maturation, 209–210
to thrust in locomotion, 84–85, 87 San Lorenzo Island Rattlesnake, 22 shaker muscle (of rattlesnake), 182–185,
drag, 84–85 Santa Catalina Island Rattlesnake, 22 fig. 8.4
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Shaw’s Sea Snake, figs. 5.9, 6.10 smooth scale, See scale subterranean, See behavior: burrow, and
shearing force, 84 snail-eating snake, 32–33, 42, fig. 1.52 habitat: fossorial
shed, shedding , See ecdysis snakebite, 62 sunbeam snakes, 12, 13, 166
shell, See eggshell snakebot, 99–100, fig. 3.20 sunlight, See radiation
shell glands, 195 snout, 11, 16, 21, 40, 50, 94, 124, 167, supercooling, 113
“she-male,” 208 figs. 1.24, 1.49, 6.10, 7.5, 7.14 superfamily, 11
shield-tail snakes, 12–13, fig. 1.15 solenoglyph, 56, 61 supranasal sac, 176
“shivering,” 12, 16, 111, fig. 4.12, See also sound, 183–190 supratemporal bone, 40
endothermy South American Bushmaster, See surface-to-mass ratio, 107
shunt, 110, 143, 145, 157 bushmaster survival, survivorship, 115, 130, 199,
intracardiac shunt, 144–145 South American Rattlesnake, 111, 208, 209–210
“pressure shunting,” 145 figs. 4.1, 4.13, 7.12 swallowing, See prey transport
“washout shunting,” 145 Southern Black Racer, 77 Swamp Snake, 29
shuttling , See behavior Southern Pacific Rattlesnake, 77, 104, 134, swimming, See behavior: locomotion
Sibon, 32, 42, fig. 1.52 figs. 2.25, 4.6, 5.23 sympatric, 26, 42, 132, fig. 5.19
Sibon nebulatus, fig. 2.8 Southwestern Speckled Rattlesnake, 134, synchrony of reproduction, 203
Sibynomorphus, 42 fig. 5.23 systematics, 12
Sidewinder Rattlesnake, 66–67, 77, 92, speciation, 9, 58 systemic circulation, See blood: blood
94, 99, figs. 3.13–3.14, 3.16, 7.10 specific dynamic action (SDA), 69–70, 111, circulation
sidewinding locomotion, See behavior: fig. 4.13 systole, 144, 149, fig. 6.2
locomotion Speckled Racer, fig. 1.5
signaling Speckled Rattlesnake, 134, 136, fig. 5.23 tail, 11, 13, 18–19, 22, 26, 37, 78, 81, 83, 85,
pathway, 8 spectacle (of eye), 3, 7, 122, 165–166, 89, 92, 94, 98, 146, 151–152, 177,
sexual signaling, 136 figs. 1.5, 7.4 182–183, 188–189, 192, figs. 1.4,
sinus venosus, 143 speed, See velocity 1.11, 3.5, 8.7, 9.3, See also behavior
sister taxon (or group), 11–13, 17, 19, 24, sperm , 158, 192, 194–195, 203, 208 paddle-shaped, 10, 29, 85, figs. 1.43,
32, 34, fig. 1.9 spermatogenesis, 192, 203, fig. 9.17 3.5–3.6, 3.8
Sistrurus, 22, 182 sperm storage, 194–195 spine, fig. 1.20
Sistrurus miliarius, fig. 4.3 spinalis-semispinalis, See muscle tail vibration, See behavior
site of resistance, See resistance site spine, 11, 18, 177, fig. 8.7 taipan, 26
size (body size), See body spinule, 177 Taiwan Slug Snake, fig. 1.53
skeleton, skeletal elements, 6, 8, 77–78, spitting cobra, 62, fig. 2.29 Tantilla, 30
80, figs. 1.3, 3.11 spitting (venom), See venom taste buds, 173
skin, 4, 10–11, 13, 18–19, 29, 37, 40, 71–72, splenial bone, 41 taxon, taxa, 10
85, 89–91, 111, 113, 117, 141, Split-jawed Boa, See Round Island Boa taxonomic character, See diagnostic
145–146, 152, 159, 173, 176, “sponge model” (for drinking), See character
205–206, 208, figs. 2.1, 3.1, 3.7, behavior: drinking taxonomy, 34
3.12, 5.2–5.3, 5.9, 5.24, 8.8, 9.18 Spotted Night Adder, fig. 1.26 teeth, 11, 16, 37–38, 40–41, 50–51, 53–61,
dermis, 118–120, 124–125, 128, spreading factor, See hyaluronidase figs. 2.8, 2.17, 2.19, 2.21–2.22, 2.24
figs. 5.3–5.4 sprint, sprint speed, 89 temporal arch, fenestra, or opening,
epidermis, 4, 71, 118–126, 128, 136, 165, spur, See pelvic spur 39–40, figs. 2.4, 4.5
205, figs. 1.6, 5.3–5.4, 5.11, 7.4 squamate (Squamata), 5, 10–11, 34–35, 117, temperature, 65, 66–68, 103–116, 122, 138,
shedding, See ecdysis 120, 138, 143, 196, 201, figs. 1.4, 141, 148, 175, 177, 182, 200–202,
skull, 4, 6–7, 10–11, 19, 38–40, 42, 51, 94, 1.8, 1.10 fig. 4.1, 4.14, 9.17
figs. 1.8, 2.4–2.5, 2.7, 2.23, 2.27 static friction, See friction body temperature, 21, 64, 103–116, 129,
slide-pushing locomotion, See behavior “stem reptiles,” 5, fig. 1.8 134–136, 158–159, 173, 183–184,
sliding friction, See friction sterility, 158 196–198, 200, 202–203, figs. 4.1,
slipping undulation, See behavior: steroids (sex), See hormone 4.2, 4.4, 4.9, 4.11, 4.13, 9.17
locomotion, slide-pushing stiletto snake, 19, 20, 56, fig. 1.24 egg temperature, 111, fig. 4.12
“slithering,” See undulation and behavior: stimulus, 163, 175 gradient, 109, fig. 4.9
lateral undulation Stoke’s Sea Snake, 27, fig. 1.45 lethal limit, 113
slough, See ecdysis stomach, See gastrointestinal tract regulation, See behavior
slug-eating snake (slug-eating snake, Storeria occipitomaculata obscura, fig. 1.48 sensitivity, 114, fig. 4.14
slugsnake, snail-eater), 33, 42 stratum corneum, 71, 119, 174, 182, fig. 5.3 tolerance, 113
slugsnakes, 42 stratum germinativum, 125, figs. 5.3–5.5 temperature or thermal receptors, See
small intestine, See gastrointestinal tract: streptostyly, 40 receptor: thermoreceptors and
intestine stretch receptor, See receptor infrared receptors
Small-scaled Burrowing Asp, fig. 1.24 Stripe-bellied Sand Snake, figs. 5.10, 5.13 tendon, 78–80, 97, 169, fig. 3.3
smell, 169–173 strike, striking, See behavior tension, See muscle
Smilisca baudinii, fig. 2.17 structural color, See color “tentacle,” 45, figs. 2.10, 7.14
smooth muscle, See muscle stump heads, 13 Tentacled Snake, 34, 44, 178, figs. 2.10, 7.14
Index | 239
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Terrestrial, See habitat, habits trade-off, 97, 114–115, 183 “free stream,” 84, fig. 3.7
Terrestrial Snail Sucker, figs. 1.52, 5.19 trailing, trailing behavior, See behavior swimming velocity, 81, 85–86
testis, testes, See gonad transducer, 117, 163, 177 venom, venomous, 20, 25, 32, 38, 46, 48–50,
testosterone, See hormone: sex steroids: transmural pressure, See pressure 56–63, figs. 1.28, 1.30, 2.17, 2.24
androgens Trans-Pecos Rat Snake, fig. 9.15 allocation of venom, 61–62
tetrapod, 5, 71, 151, 168 transporters (molecular), 67 envenomation, 4, 37, 45–46, 49–50, 56,
Texas Blindsnake, 12 “transport system,” See circulatory system 60, 62, fig. 2.17
Thamnophis, 29, 40, 56 tree, See phylogenetic tree spitting, 26, 61
Thamnophis elegans, 67, 109 tree frog, fig. 2.17 venom apparatus or delivery system,
Thamnophis ordinoides, 130 tree snake, 30, 42, 69, 129 19–20, 58–59, 61, 63, 196, fig. 2.27
Thamnophis sirtalis, 21, 113, 134, 166, trichromatic color vision, See vision: color venom composition, 62
201, 208, fig. 4.2 vision venom duct, 55, 60, fig. 2.27
Thamnophis sirtalis sirtalis, 137 trigeminal nerve, 174 venom gland, 21, 26, 59–62, 135,
Thamnophis sirtalis parietalis, Trimeresurus, 22, 176 fig. 2.27, See also accessory
figs. 4.2, 4.7, 9.17 Trimeresurus stejnegeri, 115, figs. 1.31, venom gland.
Thamnophis sirtalis similis, fig. 1.46 5.6 vent (cloacal opening), 66, 188, 192
Thelotornis, 30, 167 Tropidodipsas sartorii, figs. 1.52, 5.19 ventilation (of lung), 58, 94, 113, 141,
thermal conductivity, 175 tropidophiid (Tropidophiidae), 15, 136 156–159, 170, figs. 6.1, 6.15
“thermal inertia,” 103, 111 truncus arteriosus, 146 ventilatory heat exchange, 112
thermal preferendum, See preferred body tuatara, 4–5, 10, 34, fig. 2.4 ventilatory rate, 112
temperature tuberculate scales, See scale ventricle (of heart), 143–146, 148, 150,
thermal radiation, See radiation: infrared tubule, 60, 176, 192 figs. 6.2–6.3, 6.5
thermal sensitivity, 114–115 turtle, 5, 10, 39, 80, 113, 118, 143, 145, 197 venule, 146
thermistor, 105, fig. 4.4 Turtle-headed Sea Snake, 205, fig. 2.15 vertebra, vertebral column, 3, 5–6, 78–79,
thermocouple, 108, fig. 4.4 twitch (of muscle), See muscle 85, 88, 91, 94, 97, 146, figs. 1.3,
thermogenesis, See endothermy and tympanic membrane, 167–168 1.19, 3.2, 3.12
“shivering” Typhlops, 55 vertebral artery, 16, fig. 6.5
thermoreceptor, See receptor Typhlops diardii, 12 vertebrate, 5, 7, 11–12, 77, 85–86, 99, 105,
thermoregulation (temperature typhlopid (Typhlopidae), 11, 94 113, 141, 143, 148, 154, 156–158,
regulation), See behavior 163–166, 168–169, 173, 202–204,
thread snakes, 11–12, 41, fig. 1.12 ultraviolet radiation (UV), See radiation 210, fig. 1.10
throat, See pharynx Ulva lactuca, fig. 2.38 vertical force, 84
thrust, See force: reaction force undulation, 78, 80–81, 83–86, 89, 92–94, vertical septum, 144, fig. 6.3
tiger snake, 27, 53, 85–86 98, 206, figs. 3.4–3.5, See also vestibular system, 169
Timber Rattlesnake, figs. 1.29, 2.32, 7.2 behavior: lateral undulation vestigial (character or trait), 5, 11, 146, 154,
tines (of tongue), 172, fig. 7.10 up-regulation, 67, 69, fig. 4.13 fig. 1.14
Titanoboa cerrejonensis, 15, fig. 1.19 urates, uric acid, 65–66, 70 vibration (mechanical), vibration sense,
tolerance urea, 70 117, 167–169, 181, 185
tolerance to cold, 113, See also “freeze ureter, fig. 2.35 villus, villi, 65, fig. 2.34
tolerance” urine, 70–72, fig. 2.35 vine snake, 78, 89, 96
tolerance to heat, 113 Uromacer oxyrhynchus, 69 viper, See viperid
tongue, tongue flicking, 3, 42, 46, 71, 114, uropeltid (Uropeltidae), 13, 55, 94 Vipera, 21
167, 169–173, 205–206, 208, Uropeltis, 155 Vipera ammodytes, fig. 1.25
figs. 5.18, 7.5, 7.8, 7.10 uterus, 193, 195, fig. 9.10 Vipera aspis, 67
tongue sheath, fig. 8.5 utriculus, 169, fig. 7.7 Vipera berus, 21, 113, 131, 134–135, 200,
topology, 9, fig. 1.9 UV, See ultraviolet radiation fig. 1.25
torsion, 78, 83, 88, 93, 183, figs. 3.2, 8.4 Vipera ursinii, 21
touch receptor, See receptor: vagina, vaginal pouch, 192, fig. 2.35 viperid (Viperidae), viper, 12, 17, 19– 21,
mechanoreceptor valve 24, 26, 34, 48–51, 54–58, 60,
toxicity, 62 narial, 153, figs. 6.10, 7.14 67–69, 91–92, 95, 97, 113–114,
toxin, 20, 57–58, 61–62, 66, 117 intravascular, 147, fig. 6.6 120, 129, 131, 135–136, 155, 173,
trachea, 153, 159, 185–187, fig. 6.13 vasculature, 175, 177 176, 187, 199, 208–209, figs. 1.25,
tracheal air sac, 159, 187, fig. 6.19 vasoconstriction, 149, fig. 6.9 1.42, 2.25
tracheal chamber, See tracheal air sac vasodilation, 149 viperine (Viperinae), 20–21, 176
tracheal diverticulum, See tracheal air vector, of force, 83, 87–90, figs. 3.4, 3.5 Virginia striatula, fig. 9.10
sac vein, 145–146, 148, 152 viscera, 13, 59, 78, 154–156, figs. 2.2, 2.26, 6.8
tracheal lung, 155, 187, figs. 6.9, 6.13 velocity, 84–86, 89, 96 viscosity, See resistance
tracheal membrane, 159, 185–187, air, 186 visible spectrum (of light), 127
fig. 6.19 blood, 148 vision, 11, 45, 49, 164–167, 173, 175, 178,
tracheal rings, fig. 6.19 crawling (terrestrial), 89–93, 130 205–206
tracks, fig. 3.14 gliding , 98 binocular vision, 167, 175, fig. 7.5
240 | Index
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color vision, 166 dietary water, 70, 72 xanthophore, See pigment
dichromatic color vision, 166 drinking , See behavior xenodermatid (Xenodermatidae), 12, 17, 34
trichromatic color vision, 166 metabolic water, 70, 72, 141 Xenodon rabdocephalus, fig. 7.8
visual system, 175 vapor pressure, 197 xenodontine (Xenodontinae), 32, 56,
visual cues or signals, See vision water absorption, 66 fig. 1.50
visual receptor, See receptor water balance, 66, 70–72, 126, xenopeltid (Xenopeltidae), 13, 54, 155
Vitamin D, 117 fig. 2.39 Xenopeltis, 13, 54
vitellogenic follicle, 193, fig. 9.6 water budget, 70 Xenopeltis unicolor, 166
vitellogenesis, 193, 201, 203 water cobra, 26 Xenophidia, 12
vitreous fluid, See eye Water Python, 111
viviparity, viviparous, 12, 16, 19, 21, 25, 29, water snake, 20, 29, 48, figs. 1.3, 1.47 Yellow-bellied Sea Snake, 27, 44, 81, 84,
32, 126, 195–197, 199–200 Western Coral Snake, 188 138, 159, figs. 1.43–1.44, 2.9,
“vocal cord,” 186–187 Western Diamondbacked Rattlesnake, See 2.24, 3.1, 3.5, 5.7, 5.9, 5.15, 5.27,
volume (of lung), See lung diamondback rattlesnake 6.10, 7.1, 9.8–9.9
vomeronasal organ or system, 169–173, Western Hognose Snake, fig. 1.49 Yellow-lipped Sea Krait, 48, figs. 2.15, 7.8
205, fig. 7.9 Western Shovel-nosed Snake, 94 Yellow Rat Snake, fig. 3.18
vomeronasal nerve or receptors, 173, whipsnake, 26, 30, 45–46, 77, 89, 96 Yellow-tail Cribo, fig. 9.12
See receptor wildfire, 134, fig. 5.23 yolk (of egg), 193, 195, 197, 209
work, See mechanical work yolk sac, 197
washout shunting, See shunt worm, 3 YSI Tele-thermometer, fig. 4.4
water, 65–66, 69–72, 84–85, 114, 117, 209, worm snakes, 11–12
fig. 6.7 worship, of snakes, fig. 5.1 zygapophysis, 78, fig. 3.2
Index | 241
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How Snakes Work Structure, Function and Behavior of The World's Snakes

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How Snakes Work

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Library of Congress Cataloging-in-Publication Data

FOREWORD BY RICK SHINE ix CHAPTER 6:

—Malcolm A. Smith, Reptilia and Amphibia, vol. 3, Serpentes (1943), p. 2

4 | How Snakes Work

Fossils and Origins

Evolutionary History and Classiﬁcation of the World’s Snakes | 5

6 | How Snakes Work

Evolutionary History and Classiﬁcation of the World’s Snakes | 7

8 | How Snakes Work

changes, commonly expressed using molecular data as the

Evolutionary History and Classiﬁcation of the World’s Snakes | 9

Classiﬁcation and Phylogeny of the Lepidosauria

10 | How Snakes Work

Evolutionary History and Classiﬁcation of the World’s Snakes | 11

Alethinophidia: The “Modern Lineages”

12 | How Snakes Work

Evolutionary History and Classiﬁcation of the World’s Snakes | 13

14 | How Snakes Work

Figure 1.15. The upper photo shows the underside of a Red-tailed

Evolutionary History and Classiﬁcation of the World’s Snakes | 15

16 | How Snakes Work

reticulatus of earlier nomenclature), which might exceed 10

Caenophidia: Advanced Snakes

Evolutionary History and Classiﬁcation of the World’s Snakes | 17

18 | How Snakes Work

Evolutionary History and Classiﬁcation of the World’s Snakes | 19

Other Lamprophiid African Snakes

20 | How Snakes Work

Figure 1.26. Spotted Night Adder (Causus maculatus),

Figure 1.25. Two species of European viper. The upper photo

Evolutionary History and Classiﬁcation of the World’s Snakes | 21

22 | How Snakes Work

Evolutionary History and Classiﬁcation of the World’s Snakes | 23

Figure 1.30. The often feared Habu (Protobothrops ﬂavoviridis) is a

appears to be closely related to pit vipers, but it was once

Elapids: Cobras, Coral Snakes, Mambas,

24 | How Snakes Work

Figure 1.36. Central American Jumping Pit Viper (Atropoides

Evolutionary History and Classiﬁcation of the World’s Snakes | 25

26 | How Snakes Work

believe this suggestion is adequately sup-

Evolutionary History and Classiﬁcation of the World’s Snakes | 27

Figure 1.41. Oriental Coral Snake (Calliophis sauteri), photographed

Figure 1.43. Upper photo: Yellow-lipped Sea Krait (Laticauda

28 | How Snakes Work

Evolutionary History and Classiﬁcation of the World’s Snakes | 29

include king snakes and milk snakes (Lampropeltis spp.), rat

30 | How Snakes Work

Evolutionary History and Classiﬁcation of the World’s Snakes | 31

Figure 1.50. Two North American xenodontine snake species, both