Introduction To The Skeleton of Hummingbirds

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Introduction to the Skeleton of Hummingbirds (Aves:

Apodiformes, Trochilidae) in Functional and Phylogenetic
Contexts
Author: Zusi, Richard L., Division of Birds, National Museum of Natural
History, P.O. Box 3 7 012, Smithsonian Institution, Washington, D.C. 2 0 013,
USA
Source: Ornithological Monographs No. 77
Published By: American Ornithological Society
URL: https://doi.org/10.1525/om .2013.77.L1
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O rn ith o lo g ic a l M o n o g r a p h s
Volume (2013), No. 77, 1-94
© The American Ornithologists' Union, 2013.
Printed in USA.
INTRODUCTION TO THE SKELETON OF HUMMINGBIRDS

(AVES: APODIFORMES, TROCHILIDAE) IN FUNCTIONAL
AND PHYLOGENETIC CONTEXTS
R ic h a r d L. Z u s i 1
D iv isio n o f B ird s, N a tio n a l M u s e u m o f N a tu ra l H isto ry , P.O . B o x 3 7 0 1 2 , S m ith s o n ia n In s titu tio n ,
W a s h in g to n , D .C . 2 0 0 1 3 , U S A
A bstract.— Historically, comparative study of the skeleton of hummingbirds has focused

on systematics, emphasizing differences between hummingbirds and other birds and only
rarely addressing differences within Trochilidae. This monograph covers both approaches, and
comparisons within Trochilidae are framed within recently published, plausible phylogenetic
hypotheses. The data are derived mainly from museum collections of anatomical specimens,
covering ~256 species of 102 genera of hummingbirds, and 11 genera of other Apodiformes.
Although the syringeal skeleton is included, emphasis is on the axial and appendicular skeletons.
The first section deals with the syrinx and with skeletal features mainly associated with
nectarivory and hovering, emphasizing characters that are unique to hummingbirds within
Apodiformes. The syrinx of hummingbirds lies in the neck rather than the thorax and displays
a unique bony knob on the surface of the tympanic membrane. During posthatching devel
opment, the upper jaw of hummingbirds undergoes metamorphic changes that produce a
morphology uniquely adapted for nectarivory within Aves. The ventral bars of the upper jaw
lengthen and rotate to become lateral walls of an incompletely tubular bill that is completed by
the closed mandibula, and lateral bowing (streptognathism) of the mandibula helps to seal the
tube while a bird drinks nectar. Streptognathism of the opened jaw is used in display by some
Hermits. The lamellar tip of the tongue required for nectar uptake also develops after fledging,
while young are still fed by the parent. In Trochilines the nasal region changes from its configu
ration by bone resorption during posthatching development. Cranial kinesis in hummingbirds
is poorly documented, but structural differences in the upper jaw of Hermits and Trochilines
imply differences in cranial kinesis. The palatum of hummingbirds is distinguished from that of
other apodiforms by extreme reduction of the lateral part of the palatinum, greater width of the
ventral choanal region, and by a median spine on the vomer. Otherwise the vomer is variable in
shape and not compatible with aegithognathism. Among cranial features, the basipterygoid pro
cess, lacrimale, and jugale are absent, and the interorbital septum is complete. The hyobranchial
apparatus differs from that of other apodiforms in having an epibranchiale that is longer than
the ceratobranchiale, and variably elongate in relation to body size. I hypothesize two modes
of hyobranchial function—one applicable to moderate protrusion of the tongue (typical nectar
eating), and another to extreme protrusion. The pelvis is less strongly supported by the synsa-
crum, and the proximal portion of the hind limb is more reduced than in other Apodiformes. By
contrast, the tarsometatarsus and flexor muscles of the toes are well developed in association
with perching and clinging. In the flight mechanism, features uniquely pertinent to hovering
are distinguished from those that support stiff-winged flight— the latter common to both swifts
and hummingbirds. Hovering is especially dependent on adaptations for axial rotation of the
wing at all major joints, and on extreme development in hummingbirds of the unusual wing
proportions (short humerus and forearm, and long hand) and enlarged breast muscles found in
swifts. Osteological characters of the Oligocene fossil E u r o tro c h ilu s that can be compared with
modern hummingbirds do not indicate nectarivory or sustained hovering in that taxon.
Present address: 802 NE 62nd Avenue, Apt. F, Hillsboro, Oregon 97124, USA. E-mail: [email protected]
Ornithological Monographs, Number 77, pages 1-94. ISBN: 978-0-943610-96-2. © 2013 by The American Ornithologists' Union.
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1

2 ORNITHOLOGICAL MONOGRAPHS NO. 77
In the second section, variations within Trochilidae are described and their distributions within
the major clades (Hermits, Topazes, Mangoes, Brilliants, Coquettes, Patagona, Mountain Gems,
Bees, and Emeralds) are specified. Most diverse are the jaw mechanism, nasal region and con-
chae, hyobranchial apparatus, cranial proportions, crests, and pneumatic inflation, structure of
the ribcage based on number of ribs attached to the sternum, pectoral girdle, and various humeral
characters. Other noteworthy but largely unexplained variation characterizes the hyobranchial
apparatus of H elio d o x a , the humerus of the " P y g m o rn is group" of P h aeth o rn is, sexual dimorphism
in numbers of thoracic ribs, and synostosis of phalanges of the foot. Although Hermits display
distinctive characters, their subfamily status is uncertain for lack of informative outgroups. Major
trochilid clades are either weakly supported or unsupported by uniquely derived characters, but
apomorphic variation within Mangoes suggests recognition of an A n th ra c o th o ra x group of genera,
and within Emeralds, a large A m a z ilia group. Each of the major trochilid clades displays con
siderable diversity in body size and skeletal characters, and numerous characters show parallel
evolution within the family. Intraspecific variation is widespread, and selected examples are high
lighted. Patterns of skeletal variations at multiple levels of phylogeny suggest that some varia
tions characterizing higher levels had their origins at the intraspecific level.
A list of unsolved problems of functional morphology of the skeleton in hummingbirds is offered.
Especially intriguing are the many posthatching changes in development of the feeding mechanism
and the challenge of incorporating morphological data and their implications into models of evolu
tion of hummingbird communities. R eceiv ed 1 7 S eptem ber 2012, accepted 8 F ebru a ry 2013.
Key words: Trochilidae, Apodiformes, comparative osteology, myology, inter- and intraspecific
variation, nectarivory, hovering, E u ro tro ch ilu s.
Introducción al Esqueleto de los Colibríes (Aves: Apodiformes: Trochilidae) en

Contextos Funcionales y Filogenéticos
Resumen .—El estudio comparativo del esqueleto de los colibríes históricamente se ha enfo
cado en la sistemática, enfatizando las diferencias entre los colibríes y otras aves, y rara vez se
han evaluado las diferencias dentro de Trochilidae. Esta monografía cubre ambas aproximacio
nes y las comparaciones dentro de Trochilidae se enmarcan en hipótesis filogenéticas plausibles
y publicadas recientemente. Los datos se derivan principalmente de colecciones de museo de
especímenes anatómicos, abarcando ~256 especies de 102 géneros de colibríes y 11 géneros
de otros Apodiformes. Aunque se considera el esqueleto de la siringe, se hace énfasis en el
esqueleto axial y el apendicular.
La primera sección trata de la siringe y de las características del esqueleto asociadas prin
cipalmente con la nectarivoría y el revoloteo, con énfasis en caracteres que son únicos de los
colibríes al interior de Apodiformes. La siringe de los colibríes se ubica en el cuello en vez de en
el tórax y muestra una protuberancia ósea en la superficie de la membrana timpánica. Durante
el desarrollo posterior a la eclosión, la maxila de los colibríes pasa por una metamorfosis que
resulta en una morfología adaptada para la nectarivoría que es única entre las aves. Las bar
ras ventrales de la maxila se elongan y rotan para convertirse en las paredes laterales de un
pico tubular incompleto que se completa por la mandíbula cerrada, y el arqueo lateral de la
mandíbula (estreptognatismo) ayuda a sellar el tubo mientras el ave toma néctar. El estrep-
tognatismo de la mandíbula abierta es usado en despliegues por algunos colibríes ermitaños.
La punta lamelar de la lengua que se requiere para recoger el néctar también se desarrolla
después del emplumamiento, mientras los pichones aún son alimentados por sus padres. En
los Trochilinae, la región nasal cambia su configuración por reabsorción del hueso durante el
desarrollo posterior a la eclosión. La quinesis craneal en los colibríes ha sido pobremente doc
umentada, pero las diferencias estructurales en la maxila de los ermitaños y los troquilinos
implican diferencias en la quinesis craneal. El paladar de los colibríes se distingue de el de otros
Apodiformes por la reducción extrema de la parte lateral del palatino, una región ventral coanal
más ancha y una espina medial en el vómer. Por lo demás, el vómer es variable en forma y no
es compatible con el aegitognatismo. Entre las características del cráneo, el proceso basipteri-
goides, el lacrimal y el yugal están ausentes, y el septo interorbital está completo. El aparato
hiobranquial difiere de el de otros Apodiformes en que presenta un epibranquial más largo que
el ceratobranquial y elongado de manera variable en relación con el tamaño corporal. Yo pro
pongo dos hipótesis sobre la función del hiobranquial - una aplicable a la protrusión moderada
de la lengua (consumo típico de néctar) y otra a la protrusión extrema. La pelvis está menos

SKELETON OF HUMMINGBIRDS 3
fuertemente soportada por el sinsacro y la porción proximal de la extremidad posterior está más
reducida que en otros Apodiformes. En contraste, el tarsometatarso y los músculos flexores de
los dedos están bien desarrollados en asociación con las actividades de percharse y aferrarse.
En el mecanismo del vuelo, las características que son pertinentes únicamente para el revoloteo
se distinguen de aquellas que soportan el vuelo con alas rígidas, el cual es común a vencejos y
colibríes. El revoloteo es especialmente dependiente de las adaptaciones para la rotación axial
del ala en todas las articulaciones importantes, y del desarrollo extremo en los colibríes de las
proporciones inusuales de las alas (húmero y antebrazo corto, y mano larga) y de los músculos
pectorales agrandados que se encuentran en los vencejos. Los caracteres osteológicos del fósil
del Oligoceno E u r o tro c h ilu s que pueden ser comparados con los colibríes modernos no indican
nectarivoría o revoloteo sostenido en ese taxón.
En la segunda sección, se describen las variaciones que existen dentro de Trochilidae y se
especifica su distribución en los clados principales (Ermitaños - H er m its , Topacios - T opazes,
Mangos - M a n g o e s, Brillantes - B rillia n ts , P a ta g o n a , Gemas de Montaña - M o u n ta in G em s, Abejas -
B ees y Esmeraldas - E m e ra ld s ). Los más diversos son los mecanismos de la mandíbula, la región
nasal y los cornetes, el aparato hiobranquial, las proporciones del cráneo, las crestas, la inflación
neumática, la estructura de la caja torácica basada en el número de costillas unidas al esternón,
la cintura pectoral y varios caracteres del húmero. Otra variación notable pero no explicada en
gran medida caracteriza el aparato hiobranquial de H elio d o x a , el húmero del "grupo P y g m o rn is"
de P h a eth o rn is , el dimorfismo sexual en el número de costillas del tórax, y la sinostosis de las
falanges de la pata. Aunque los ermitaños muestran caracteres particulares, su estatus como
subfamilia es incierto debido a la falta de grupos externos informativos. Los clados principales
de colibríes están pobremente apoyados o no están apoyados por caracteres únicos derivados,
pero la variación apomórfica dentro de los Mangos sugiere el reconocimiento de un grupo
genérico A n th ra c o th o r a x , y, dentro de las Esmeraldas, de un gran grupo del género A m a z ilia .
Cada uno de los principales clados de colibríes muestra una diversidad considerable en el
tamaño corporal y en los caracteres del esqueleto, y muchos caracteres presentan evolución
en paralelo en la familia. La variación intraespecífica está ampliamente difundida y se resaltan
algunos ejemplos. Los patrones de variación en el esqueleto en múltiples niveles de la filogenia
sugieren que algunas de las variaciones que caracterizan los niveles profundos tienen sus orí
genes en el nivel intraespecífico.
Se ofrece una lista de problemas sin resolver sobre la morfología funcional del esqueleto de
los colibríes. Resultan especialmente intrigantes los muchos cambios posteriores al nacimiento
en el desarrollo de los mecanismos de alimentación y el desafío de incorporar los datos mor
fológicos y sus implicaciones en modelos sobre la evolución de las comunidades de colibríes.
The skeletal system is composed of bone, cartilage, and ligaments. (Campbell and Lack
1985:543)
Frequently a distinction is made between the Axial and the Appendicular Skeleton—the
former being restricted to the Vertebral Column and the Cranium proper, while the latter
comprises the Ribs, Breastbone ... Limbs and their arches, the Hyoid apparatus and the
Jaws. (Newton and Gadow 1893-1896:848)
S y rin x .. The essential features.. .are, first, membranes stretched between the several parts
of a cartilaginous or bony framework, and next, special muscles which by their action
vary and regulate the tension of the membranes. (Newton and Gadow 1893-1896:937)
Introduction here were not obtained for this study, but were
accumulated in museums over the years as an ar
Prologue.—This monograph summarizes data chive of the diversity of birds. The number of in
from private and institutional collections housed dividuals of each species in anatomical collections
in museums of natural history—the ultimate usually is low, sometimes only one or zero, and
sources for comparative anatomical studies. In data on older specimen labels are often minimal.
particular, it is based on specimens prepared as These deficiencies are balanced by the taxonomic
skeletons and spirit specimens, preparations that, richness now available in collections. Because the
traditionally, were neglected in favor of the study skeleton consists of more than bones, spirit speci
skin. With few exceptions, the specimens studied mens are important adjuncts to the exposition of

major skeletal variation. The syringeal skeleton is of comparative osteology in which higher-level
included here with the more commonly studied grouping was inferred from enumeration of sim
axial and appendicular skeletons. ilarities or differences, produced a heated and
Hummingbirds comprise some 330 extant colorful controversy concerning the relationships
species restricted to the Western Hemisphere of hummingbirds to swifts and of swifts to swal
and are the most speciose of non-passeriform lows (reviewed by Sibley and Ahlquist 1972).
families (Bock and Farrand 1980). Linnaeus (1758) In the late 19 th century, Robert W. Shufeldt and
described 18 species, but by the late 1800s ninety William K. Parker maintained their convictions
percent of the species now recognized had been that swifts and swallows were closely allied and
described (Graves 1993). However, monographic that hummingbirds had no special relationship
treatments of the family based on variations in with swifts.
the integument produced little agreement on the Until recently, most anatomical studies were
composition of genera and higher categories, and minimally comparative within Trochilidae; in
major classifications lacked higher-level group the late 19th century, Shufeldt stated that the
ings (Cory 1918, Peters 1945, Morony et al. 1975). U.S. National Museum's (USNM) anatomical
Striking elaborations of plumage associated with collections included no Apodiformes (Shufeldt
sexual selection rendered generic allocation diffi 1885). The monographic works on avian anatomy
cult and resulted in a proliferation of genera. Nev and systematics by Huxley (1867), Furbringer
ertheless, the rapid development of hummingbird (1888), and Gadow and Selenka (1891) included
taxonomy has provided a basis for meaningful, only one or a few species of hummingbird repre
anatomical comparisons. sented by few, sometimes damaged, specimens.
Within this monograph, "variation" includes Even the most detailed treatment of the hum
differences between individuals of a species, spe mingbird skeleton (Shufeldt 1885) described
cies of a genus, genera within higher categories, only a single species. A survey of myology of
higher categories up to subfamily, and families of the avian hindlimb by Hudson (1937) did not
an order. Some characters that show little varia include a hummingbird, and Zusi and Bentz
tion within Trochilidae but that differ from other (1984) covered only six species in their description
Apodiformes are discussed as variation within of hummingbird myology. Major anatomical col
Apodiformes rather than within Trochilidae. The lections have greatly increased their taxonomic
variation in morphological states presented here coverage of hummingbirds in recent years (Zusi
is essentially qualitative, involving differences in et al. 1982, Livezey 2003). Thus, analysis of varia
shape, presence or absence, and relations to other tion in a single wing muscle by Zusi and Bentz
characters, and a few characters are meristic (e.g., (1982) covered 19 species of swift, 88 species
counts of vertebrae). Proportions, based on small of hummingbird, and many non-apodiform
samples, are usually expressed in words rather species, whereas the present monograph includes
than numbers, and, as a result, this monograph almost 75% of the extant species and 92% of
is only an introduction. Most of the data on os- extant genera of hummingbirds (Appendix 1).
teological variation within Trochilidae presented To summarize, within 200 years, anatomists
here were originally amassed for phylogenetic had identified ostensibly unique aspects of hum
analysis. mingbird anatomy and fostered a majority view
Comparative anatomy.—Most early anatomical of the close relationship between hummingbirds
work on hummingbirds comprised interordinal and swifts, but had left the subject of compara
surveys of selected anatomical structures (e.g., tive osteology within the Trochilidae largely
sternum and shoulder girdle, L'Herminier 1827; unexplored. More recently, interest has shifted
pterylosis, Sclater 1867; syrinx, Müller 1878; to many other aspects of hummingbird biology
palate, Huxley 1867, Parker 1878; pelvic muscu and ecology, and phylogenetic inference has been
lature, Garrod 1873a). The growing data base of based largely on molecular data.
comparative anatomy, as enlarged and analyzed Uniqueness, parallelism, and convergence.— Most
by Fürbringer (1888), Gadow and Selenka (1891), purportedly unique skeletal characters of hum
Beddard (1898), and others, supported a general mingbirds have pertained to the shoulder girdle,
consensus on the monophyly of Trochilidae and sternum, and forelimb. Demonstration of unique
a close relationship of swifts and humming ness in the hummingbird skeleton is complicated
birds. Nevertheless, additional studies, largely by the uniquely specialized structure of the

flight mechanism found in both swifts and hum hummingbird flight in both laboratory and field,
mingbirds, reflecting their commonality of stiff but insights concerning other anatomical com
winged flight and a strongly powered upstroke plexes (nasal region, hyoid apparatus, syrinx)
of the wing (Savile 1950). Similarities in the flight are essentially lacking.
mechanisms of the two families have been in Phylogenetic contexts.— Recent evidence from
terpreted either as derivations from a common morphological data (Livezey and Zusi 2007) and
ancestor or as convergent evolution. Probably molecular data (McGuire et al. 2007) supports
both processes were involved, and separate, par monophyly of Apodiformes—Hemiprocnidae,
allel morphoclines of specialization in the wings Apodidae, and Trochilidae. Molecular studies of
also occur within both modern swifts and hum phylogeny have employed increasing taxonomic
mingbirds (Zusi and Bentz 1982, Bleiweiss 2002). representation of Trochilidae (Gill and Gerwin
Given this high level of parallel evolution, gross 1989, Sibley and Ahlquist 1990, Bleiweiss et al.
anatomical features of the flight apparatus that 1997, Gerwin and Zink 1998, Altshuler et al.
are unique to hummingbirds and significant for 2004, McGuire et al. 2007). These studies present
hovering are often subtle. No such parallelism plausible hypotheses concerning the phylogeny
exists in the feeding mechanisms of swifts and of major clades within Trochilidae as shown in
hummingbirds. However, functional comparison Figure 1. The results from molecular analysis
of hummingbirds with long-billed, nectar-eating were broadly supported by exploratory cladistic
passeriforms reveals convergence related to nec- analyses of morphological data (R. L. Zusi un-
tarivory (Paton and Collins 1989). publ. data). Nevertheless, basal polarities of vari
Functional osteology.—In contrast to static, an ous anatomical character-state variations within
atomical description of the skeleton, a functional Trochilidae are uncertain because closely related
approach may involve structural complexes sister taxa of Trochilidae are unrepresented by
and kinematics of movable parts. The role of living species or fossils. The most intriguing
ligaments in osteological kinematics (e.g., Sy fossil, Eurotrochilus, is too distant (Oligocene) to
1936, Bock 1964, Zusi 1967) is critical, but of serve that purpose. Therefore, questions about
ten neglected. Papers by Moller (1930, 1931), modern hummingbirds persist: for example, are
Scharnke (1930, 1931b), Steinbacher (1935a), the Hermits a sister clade to all other humming
Weymouth et al. (1964), Wolf and Hainsworth birds (Trochilines) or are they a specialized clade
(1977), Ewald and Williams (1982), Kingsolver within the Trochilines?
and Daniel (1983), Montgomerie (1984), Paton Objectives of this monograph.—This study sup
and Collins (1989), Rico-Guevara and Rubega plements current, experimental approaches by
(2 0 1 1 ), and others explored the functional basis presenting species-rich description of variation in
of nectar eating. Similarly, Lorenz (1933), Stolpe the skeleton of adult hummingbirds. In Section I,
and Zimmer (1939), Cohn (1968), Karhu (1992, I emphasize the uniqueness of the syrinx and of
1999), and others clarified the mechanism of feeding and flight anatomy by comparison with
stiff-winged flight in swifts and hummingbirds, a sample of other Apodiformes and with Aegothe-
and of hovering in hummingbirds. In addition, les, thus highlighting characters of low variability
many more recent studies on muscle physiology within Trochilidae that may represent anatomical
(electromyography) in relation to wing stroke, correlates of hovering and nectarivory. In addition,
aerodynamics of the wing, energetics of hover comparison of modern hummingbirds with fossils
ing, physiological limits of hovering in different assigned to Eurotrochilus (Mayr 2004) prompted
environments (hypoxic, hypodense), mechanics reevaluation of levels of behavioral specialization
of nectar uptake, coevolution of bill and flower in the Oligocene taxa. In Section II, I present major
structure, and other topics have provided a new variation within Trochilidae and indicate distribu
understanding of the functional, ecological, and tion of such variation within and among the major
evolutionary aspects of hovering and nectar- clades of hummingbirds. Examples of intraspecific
ivory. Several explanations for hovering, rather variation are presented, and patterns of diversity
than perching, when feeding at flowers were of and possible adaptation at various phylogenetic
fered by Pyke (1981), Miller (1985), Hainsworth levels are identified. Throughout this study, and
(1986, 1991), and Gill (1985), and each explana especially under headings in all-capital italics, I
tion may be relevant in a particular context. Cur offer speculations on function that could be profit
rently predominant are physiological studies of ably tested by other methods.

A P O D IF O R M E S
PRIMARY
TROCHILIDAE
OUTGROUP
H ER TROCHILINES
TO P MAN NEOTROCHILINES
ANDEAN
HUMMINGBIRDS
Fig. 1. Branching diagram of a higher-level phylogenetic framework of hummingbirds and outgroups fol
lowed in this monograph. Branch lengths are arbitrary. Dashed lines show other plausible arrangements (see
text). If Topazes are considered sister to all other hummingbirds, one could recognize Topazinae for Topazes,
Phaethornthinae for Hermits, and Trochilinae for all other hummingbirds (see Chesser et al. 2012). This diagram
is modified from McGuire et al. (2007), not based on a new phylogenetic analysis. Abbreviations: HER. = Hermits,
MAN. = Mangoes, TOP. = Topazes.
M ethods and M aterials families if the character in question is thought to be

similar throughout the family, and English names
Taxonomic nomenclature.—I follow the American when referring to a subset of species in the fam
Ornithologists' Union (1998) Check-list of North ily. Bleiweiss et al. (1997) and McGuire et al. (2007)
American Birds, seventh edition, and Remsen et proposed informal names for major clades within
al. (2007) for nomenclature of generic and specific Trochilidae. I employ the vernacular names "Her
level taxa of South American birds. For Old World mits," "Topazes," "Mangoes," "Brilliants," "Co
birds, I follow Dickinson (2003), and names of fos quettes," "Patagona," "Mountain Gems," "Bees,"
sils are from Mayr (2004). I use Hemiprocnidae and "Emeralds" used for the major clades by
(crested swifts) and Apodidae (swifts) as primary McGuire et al. (2007), but for convenience in sum
outgroups, and Aegothelidae (owlet frogmouths) marizing distribution of anatomical characters I
as a more distant outgroup to Trochilidae (hum place Topazes next to Mangoes within Trochilines
mingbirds). I use the scientific names of outgroup (Fig. 1). I follow the placement of Patagona as sister

to Mountain Gems, Bees, and Emeralds, although "prepalatal upper jaw" for the osseous portion of
some anatomical characters support its inclusion the upper jaw that is covered by ramphotheca in
in Brilliants. modern birds.
Scientific names for the nine major clades Within the palatum, the maxillary process of
informally named above are presented by McGuire the palatinum fuses with the palatine process of
et al. (2009), but formal names to represent a the maxillare in adult birds. I refer to the result
hierarchy of those clades were not proposed. ing structure as the "rostral bar," connecting the
If Topazes are considered as sister to all other palatum with the prepalatal upper jaw.
hummingbirds, one could recognize Topazinae, In Sections I and II, I use English anatomical
Phaethornithinae, and Trochilinae (Chesser et al. terms in text and figures, with the singular form
2012). Throughout, I use the capitalized informal of Latin equivalents in parentheses at first use
terms "Hermit" and "Trochiline" (i.e., non (e.g., "dorsal bars (pila supranasalis)"). When
Hermit) without necessarily accepting the validity English and Latin names are identical or nearly
of the traditional subfamilies Phaethornithinae so, I use only the Latin name (e.g., mandibula
and Trochilinae. Within Trochilines, I separate for mandible). Latin names of bones that include
Mangoes and Topazes from a clade that con "os," as in "os palatinum," are Anglicized in
tains all other non-Hermits, and term the latter, many other works by the single adjectival form,
unnamed clade "Neotrochilines." Names are for example "palatine." Here, I omit "os" and use
needed to represent the Brilliants and Coquettes the Latin noun (e.g., palatinum) in place of the
(sometimes called "Andean Hummingbirds"), English name (palatine bone). Conventionally,
the clade comprising Mountain Gems plus Bees, Latin names of muscles are preceded by "m ." or
and the clade that includes Mountain Gems, Bees, "musculus" but are otherwise identical to Eng
and Emeralds (Fig. 1). Within Apodidae, I include lish names. For this reason, I use either English or
species representing major clades hypothesized Latin names for muscles.
by Price et al. (2005). Taxonomic coverage and sample sizes.—Species
Anatomical nomenclature.—With few exceptions, studied as skeletons and spirit specimens and
anatomical nomenclature follows Baumel et al. the museum collections consulted for each are
(1993)—specifically Clark (1993), Baumel and Wit- listed in Appendix 1. Of 330 extant species, 256
mer (1993), Baumel and Raikow (1993), Vanden (about 75%) were studied. Of 111 extant genera,
Berge and Zweers (1993), and King (1993). Addi 102 (92%) were examined. The frequency matrix
tional names follow Zusi and Livezey (2006) and in Appendix 2 contains 33% of extant species and
Livezey and Zusi (2006). Terms of orientation are 90% of extant genera. In the matrix, I usually re
those proposed and explained by Clark (1993). corded data from four specimens of each species,
Nevertheless, difficulties persist. For example, but for some anatomical characters fewer speci
the upper jaw of vertebrates includes not only the mens were available, and for others more than
primary tooth-bearing bones but also those of the four specimens were coded. Unossified struc
palate, linked by the quadrates to the lower jaw. tures (nasal cartilage, muscles, and ligaments)
In external topography of birds, the mandibles usually were scored from a single spirit specimen
covered by rhamphotheca constitute the beak or per species and were thus unavailable for discus
bill and are termed "rostrum maxillare" and "ros sion of intraspecific variation. Species listed in
trum mandibulare" by Clark (1993:1-2). However, Appendix 1 but not included in the matrix were
under "Osteologia" (Baumel and Witmer 1993), examined for selected characters in the course of
the term "rostrum maxillae" refers only to the the study.
symphysial portion of the paired premaxillary Sources o f error and missing data.—A potential
bones, which forms the anterior tip of the upper source of error in skeletal specimens of humming
jaw, and "rostrum mandibulae" refers only to the birds is the misidentification of some specimens
symphysial portion of the paired dentary bones, (especially females or immatures) before prepa
which form the anterior tip of the lower jaw. No ration. In general, I found that most skeletons
term is offered to represent the entire bony portion were identifiable to genus from skeletal charac
of the upper jaw that excludes the palate. Livezey ters alone. I believe that few uncorrected errors
and Zusi (2006) used the term "rostrum maxillae" of species identification occurred in the present
not only for this portion of the bony upper jaw but study and that any such errors would have per
also for the entire maxilla. Here, I propose the term tained to congeners. A more prevalent problem

was over-cleaned skeletal specimens that were upper jaw, (3) verifying presence of bones often
damaged or incomplete, and under-cleaned spec lost in skeleton preparation (e.g., sesamoids of
imens in which parts of the skeleton were not the tail, free ribs, phalanges), and (4) clarifying
visible. The number of fully useful, skeletal speci syringeal structure. A juvenile specimen (nest
mens in museums was thus less than the totals ling) and an adult specimen of C. swainsonii, both
listed in skeleton inventories (Wood and Schnell cleared and stained, provided the only direct
1986). In addition, incorrect sexing of specimens contrast between juvenile and adult features and
that were ultimately prepared as skeletons oc served as a basis for discussion of ontological
curred at rates that probably differed among metamorphosis of the jaws, a phenomenon that
species. Skeletal specimens of juveniles young I have assumed to be widely applicable within
enough to retain sutures of the cranium were not Trochilidae.
found, and all specimens discussed here were of Functional anatomy and adaptation.—Functional
adult size with the exception of one nestling of properties of osteological entities include resistance
Chlorostilbon swainsonii—a spirit specimen that to and propagation of forces, and contributions to
was cleared and stained. kinetic systems that usually involve joints, liga
Each skeletal specimen in museums is routinely ments, and muscles. Here, I inferred such prop
identified before preparation and labeled with erties from examination and manipulation of
the prevailing scientific name. Especially during specimens rather than from measurements on live
historical periods of taxonomic lumping, two or birds. For example, to obtain qualitative informa
more subsequently recognized species may have tion on flexibility within the upper jaw during
received the same name on skeleton boxes. This cranial kinesis, I manipulated freshly dead indi
problem probably was most troublesome for me viduals of three species of Hermits and three of
with regard to skeletal variation among speci Trochilines. Rostrodorsal pressure on the articu
mens commonly labeled "Phaethornis longuema- lar-quadrate region simulated contraction of m.
reus," now thought to represent at least three depressor mandibulae and m. protractor quadrati
species (see Section II under "Humerus"). et pterygoidei during cranial kinesis. The same tac
Anatomical specimens.—Description of most tic was employed on hydrated skeletons of addi
individual skeletal elements of hummingbirds tional species. Manipulation of cleared and stained
required magnification with a dissecting micro specimens clarified motion at some articulations,
scope, thus limiting simultaneous comparisons to and actions of several muscles of the forelimb
a few species. Using a camera lucida, I made line were noted while tensing their tendons. I inferred
drawings of the cranium, palatum, humerus, and interrelations of bones and muscles during exten
sternum of many species to permit broad, synop sion and retraction of the tongue from superficial
tic comparisons for the initial discovery of major dissection of spirit specimens that had been fixed
variations. Skeletons with articulated vertebrae, with the tongue conveniently positioned in ran
trunks, and digits of the foot were indispensible domly different stages of protrusion.
for counts of vertebrae, ribs, and phalanges. When structures or functions are associated
Spirit specimens listed in Appendix 1 were with behaviors such as foraging, locomotion,
used for determining gross morphology of the or social interactions, their biological role may
(cartilaginous) nasal region, conformation and become evident. A structural complex can serve
asymmetry of the epibranchiales, and variation more than one biological role within or between
in muscles and ligaments. Although not central species. Structural adaptation requires a phyloge
to the present study, data that supplement the netic perspective and demonstration of a change
widely cited information on the tendons of m. from the ancestral condition (inferred from
tensor propatagialis brevis (Zusi and Bentz 1982) outgroups); the change may increase efficiency of
are presented in Appendix 3. the structure in the same biological role or may
Selected specimens of 44 species (35 genera) enable its use in a new biological role.
from the USNM spirit collection were cleared The bulk of this monograph concerns descrip
and stained for bone, or cartilage and bone. These tive anatomy, thus filling gaps in the record of
specimens were especially useful for (1 ) deter hummingbird osteology and raising new ques
mining the nature of cartilaginous structures in tions. Functions and biological roles are inferred
the nasal region and patterns of ossification, (2 ) throughout, and evidence is presented for
verifying delicate ossifications in the prepalatal adaptations related to nectarivory or sustained

hovering in all hummingbirds. Still unexplored, Powdermill, Pennsylvania. Birds captured in mist
however, are the biological roles, ecological nets for banding were retained briefly in restrain
significance, and adaptation of many variations ing tubes and allowed to feed on sugar water from
of the skeleton within Trochilidae. an inverted tube feeder. A dissecting microscope
Histology.—Histological transverse sections of was oriented to allow observation at 6 x magnifi
the prepalatal upper jaw of Glaucis hirsutus and cation of the bill and tongue in either ventral or
Heliodoxa xanthogonys, nasal region of Eulampis lateral view during feeding. Additional species
jugularis and Phaethornis malaris, and syrinx of (Eulampis jugularis, Orthorhynchus cristatus, and
G. hirsutus and E. holocericeus provided informa Cyanophaia bicolor) were netted inadvertently in
tion on tissue structure and details of anatomical the course of other studies in Dominica (Lesser
relationships not evident under low magnifica Antilles), March 1990. These birds were held
tion. These specimens were decalcified, sectioned briefly in the field and observed in ventral view
at 8 microns, and stained with haematoxylin and with the aid of a flashlight and mirror while they
eosin or Masson trichrome stain. fed on sugar water from a vial. Other details of bill
Fossils.— Fossils of Cypseli from Early Eocene movement and hovering were obtained from vid
to Middle Oligocene—predominantly isolated eos and published photographs or descriptions.
humeri and coracoids—include a few partially Size comparisons.—I relied on data in Dunning
articulated skeletons of swift-like birds, several of (2008) for broad comparisons of body weight
which have well-preserved feather impressions. within Apodiformes. Within Trochilidae, cora
Three fossil families have been proposed (Mayr coid length is highly correlated with cube root of
2003b). The most interesting find for the present body weight, and the two measures vary isomet
study is Eurotrochilus inexpectatus from the Oli rically (R. L. Zusi unpubl. data). Within a single
gocene of Germany (Mayr 2004, 2007) and other species (Trochilus citulus), Graves (2009) found
fossils referred to that genus (Louchart et al. 2007, sternal length to be most highly correlated with
Bochenski and Bochenski 2008). My knowledge body weight. Whether this result applies within
of the osteology of these fossils is based solely on all interspecific comparisons is unknown. In the
published illustrations and descriptions. text, I made some comparisons between species
Intraspecific variation.—The anatomical varia of similar body size (based on body weight or on
tions discussed under Section II represent coracoideum length) to highlight proportional
phenotypes that differed qualitatively or meristi- differences or similarities; in the figures, scale
cally and were coded originally as two or more bars are not included, but individual skeletal ele
states of each morphological character. Coded ments are sometimes scaled to a similar length or
states that applied to each species were either width to emphasize proportional differences.
constant (monomorphic) or variable (polymor Phylogeny.—Phylogenetic hypotheses derived
phic) within the sample of specimens, as de from morphological or molecular evidence (Sib
tailed in the frequency matrix (Appendix 2). ley and Ahlquist 1990; Bleiweiss et al. 1994;
For interspecific comparison, each species was Johansson et al. 2001; Mayr 2002, 2003a; Chubb
characterized by its modal (majority) state, or if 2004; Cracraft et al. 2004; Livezey and Zusi 2006,
two character states were equally represented 2007; Hackett et al. 2008) agree on the monophyly
in a sample, I chose the state that was typical of of Apodiformes (Hemiprocnidae, Apodidae, and
congeners; in monotypic genera, I used the state Trochilidae), but differ in the proposed sister-group
that appeared to be derived. Sample sizes (1 to 4, relationship of Apodidae (i.e., to Trochilidae or to
sometimes more) were mostly too small to permit Hemiprocnidae). Here, I accept the monophyly
a comprehensive representation of intraspecific of Apodiformes and the sister-group relationship
variation here. Nevertheless, I describe selected of Hemiprocnidae and Apodidae. Aegothelidae
examples of such variation. With the exception of provides a more distant outgroup, either as an
sexual dimorphism in numbers of ribs attached early branch of Apodiformes (Mayr 2002) or as a
to the sternum, I did not undertake analysis of basal branch of the sister order Caprimulgiformes
sexual dimorphism in the skeleton. (Livezey and Zusi 2007). The phylogenetic context
Behavioral data.—I observed nectar-drinking is presented in Figure 1.
behavior of Ruby-throated Hummingbirds (Ar The two most comprehensive molecular stud
chilochus colubris) on 20 May 1986, at the Carnegie ies (Bleiweiss et al. 1997, McGuire et al. 2007)
Museum of Natural History's banding station at largely agree on the constitution and sister

relationships of major clades within Trochilidae. are associated with incomplete bronchial rings,
Other studies have addressed relationships at and an ossified drum (tympanum) is formed from
various levels using molecular or morphological modified tracheal and bronchial rings.
data—groups of clades (Zusi and Bentz 1982), He- Location.— In all birds except hummingbirds
liodoxa (Gerwin and Zink 1989), Hermits (Gill and (and one species of spoonbill, Plataleinae: Ajaia
Gerwin 1989), and some Brilliants and Coquettes ajaja; Garrod 1875) the syrinx and bronchi lie
(Roy et al. 1998). within the thoracic cavity (cavitas thoracica) cau
dal to the furcula and interclavicular membrane
Section I. The U niqueness of H ummingbirds (saccus clavicularis; hereafter ICM). The syrinx
and a major portion of each bronchus of hum
Except for the syrinx, this section is based on mingbirds are situated in the neck rostral to the
intensive taxonomic sampling within Trochili level of the furcula (Müller 1878, Cannell 1986).
dae and limited sampling of outgroups repre However, the ICM includes an evagination ros
sented by one or a few species each of Apodidae, tral to the furcula that encloses the syrinx and the
Hemiprocnidae, and Aegothelidae (Appendix 1). rostral portion of each bronchus (Fig. 2). Between
I describe the syrinx, on the basis of limited tax
onomic sampling that included both Hermits
and Trochilines, to characterize probable syn-
apomorphies of Trochilidae. With respect to the
tongue and hyobranchial apparatus (apparatus
hyobranchialis), I make some comparisons also
with long-billed, nectariverous Passeriformes
(Nectariniidae). The data in this section are or
ganized topographically to emphasize structural
complexes that may support functional capabili
ties unique to hummingbirds.
Syrinx
The larynx, trachea, syrinx, and bronchi of birds

incorporate cartilaginous or osseus skeletal ele
ments of the respiratory system. Skeletal muscles
interconnect the larynx with the hyobranchial
apparatus, and the trachea with the sternum.
Both interconnections are present in Hemiproc-
nidae and Apodidae but absent in Trochilidae.
Independent movement of the hyobranchial
apparatus, decoupled from the larynx, allows
extreme protrusion of the tongue in humming
birds. Intrinsic muscles, associated only with the
syrinx, are present in hummingbirds and lacking
in outgroups.
The structure of the syrinx of many birds (but not F ig. 2. Location of the syrinx in the neck in hum
hummingbirds) has been reviewed by King (1989). mingbirds. (A) Skinned trunk of a hummingbird in
In Aegotheles and Apodiformes, the membranous right, lateral view, with primary feathers clipped. (B)
trachea and bronchi are supported by cartilaginous Enlarged, semidiagrammatic, dorsal view of syrinx,
trachea, and bronchi. Although the bronchi and syr
rings. The syrinx of Aegotheles consists of bilateral,
inx extend rostrally into the neck within a pouch of
medial tympanic membranes (membrana tym-
the interclavicular membrane, the pouch represents an
panica medialis) that interconnect the third and extension of the thoracic cavity. Abbreviations: bro. =
fourth, and fourth and fifth bronchial rings (car- bronchus, bro. r. 1 = first bronchial ring, med. tym.
tilago bronchialis) caudal to the last tracheal ring mem. = medial tympanic membrane, m. pect. = pec-
(cartilago trachealis) (Beddard 1886). In swifts and toralis muscle, ICM = interclavicular membrane, syr.
hummingbirds the medial tympanic membranes m. = syringeal muscles, tra. = trachea.

the larynx and syrinx, a trachea of Florisuga mel- four pairs are complete in hummingbirds. Unlike
livora comprised 39 rings; and between the syrinx passeriform birds described by Ames (1971), they
and lung (pulmo), the complete bronchial rings are not differentiated into flattened and thick
of each bronchus numbered 35; correspondingly, ened rings. Instead, the cartilage of each ring is
a Campylopterus sp. had 40 tracheal and 41 bron thickened, becoming flatter only in its medial
chial rings. In hummingbirds, the bronchi, both portion. A medial tympaniform membrane closes
rostral and caudal to the clavicles, lie side by side, the gap in the bronchial tubes left by incomplete
diverging only as they approach the lung. The rings. The drum in Apus is shorter than that of
tubular evagination of the ICM binds the bron hummingbirds (Fig. 3A, B).
chi together by contact with their lateral walls At its rostralmost extremity, the ossified drum
and rostrally forms a globular expansion within equals the shape and diameter of the trachea,
which the syrinx is freely suspended. The expan but the drum abruptly widens caudally (Fig. 3B).
sion terminates rostral to the syrinx and is pen The wide portion represents a merging of adja
etrated by the trachea. The limited space between cent bronchi, as demonstrated by the syrinx of
the ICM evagination and the bronchi and syrinx Mellisuga minima (USNM 318954) in which there
is occupied by the bilaterally merged cervical air are six, partly cartilaginous, median partitions
sacs (saccus cervicalis), which originate from the (remains of bronchial rings) within the lumen of
caudal extremity of the primary bronchus in the the drum. Some portions of the bony drum are
lung (Stanislaus 1937). thin and single-layered, whereas others are ex
Structure.—Extrinsic muscles originate outside panded into crests or ridges by addition of a sec
of the syrinx and insert upon it. The only extrinsic ond, external layer of bone that encloses a fatty
muscle in hummingbirds is the paired m. tracheo- marrow cavity and is reinforced by trabeculae.
lateralis, which is represented by flat bands along These ridges are typically on the caudal portion
opposite sides of the trachea. At the intersection of of the drum midventrally and dorsolaterally, but
the ICM and the trachea, this muscle divides into in a few species they extend dorsolaterally along
two branches: one spreads over the rostral surface the full length of the drum. The ridges and crests
of the membrane and inserts on it; the other passes expand the origins of intrinsic muscles. A pillar
through the membrane, curves ventrally, and separates the bronchial openings of the drum
inserts on the caudoventral surface of the drum. caudally (Fig. 3B). This ossified, medial pillar
M. sternotrachealis is absent. In swifts the sterno- (pessulus) is roughly triangular in transverse sec
trachealis and tracheolateralis muscles may rep tion, enclosing a fatty marrow. Its caudolateral
resent an antagonistic pair (Fig. 3A), controlling edges support the two, medial tympaniform
rostrocaudal movement of the syrinx; both mus membranes.
cles have superfast muscle fibers in some Colum- Between the caudolateral rim of the drum and
bidae that are among the fastest muscle fibers the first free bronchial ring is a partly membra
known (Elemans et al. 2004), which suggests a role nous, lateral lamella (lamella lateralis) that proj
in vocalization. In hummingbirds the evagination ects into the air passage of the drum (Fig. 3C)
of the ICM surrounding the syrinx may act as a lig and extends from the base of the pessulus to the
ament (functionally replacing the sternotrachealis upper limit of the first, free bronchial ring. Mül
muscle) that limits rostral movement of the syrinx ler (1878:37) described it as an "excessively small"
initiated by m. tracheolateralis. In Apus an inter first bronchial ring. The lamella is strengthened
bronchial ligament (ligamentum interbronchiale) by an internal cartilage in some species or is ossi
from each bronchus attaches separately on the ad fied in others (e.g., P. superciliosus USNM 511312).
jacent, dorsally situated esophagus. This ligament The osseous portion, somewhat irregular in shape,
is lacking in hummingbirds. may be limited to the midsection of the lamella.
Here, I offer a description of the syrinx, based In hummingbirds the first free bronchial ring
mainly on G. hirsutus, Threnetes leucurus, Eulampis is larger than the others. It is incomplete in its
holosericeus, and Coeligena coeligena, that expands medial portion, as in other bronchial rings
on those by Müller (1878) and Cannell (1986). In associated with the medial tympaniform mem
Aegotheles and Apodiformes the free tracheal and brane. Its C-shaped cartilage is roughly circular
bronchial rings are cartilaginous, and the syrinx in transverse section except at the dorsal end,
(rings or drum) is ossified. The free tracheal rings where it is expanded and flattened. The dor
and all bronchial rings except the rostral three or sal portion or head (caput) is ossified, as is the

F ig. 3. The syrinx of a swift and hummingbird. (A) Swift (A p u s a ffin is), drawn from spirit specimen; dorsal
view. (B) Hummingbird (T h ren etes leu cu ru s) drawn from a cleared and stained specimen in which only cartilage,
bone, and ligaments remain; dorsal view. (C) Semidiagrammatic composite of section through a hummingbird
bronchus with view into the interior of the drum. (B, C) Lumen of drum shown in solid black. Adjacent bron
chi, intrinsic muscles, modified head of first bronchial ring, tympanic ossicle, and lateral lamella are unique to
hummingbirds within Apodiformes. Hummingbirds lack the sternotrachealis muscle and interbronchial liga
ment. Abbreviations: bro. = bronchus, bro. lum. = lumen of bronchus, bro. r. = bronchial ring, bro. r. 1 = first
bronchial ring, eso. = esophagus, int. lig. = interbronchial ligament, int. mus. = intrinsic syringeal muscles, lat.
lam. = lateral lamella, med. tym. mem. = medial tympanic membrane, m. ste. = sternotrachealis muscle, m. tra. =
tracheolateralis muscle, pes. = pessulus, ten. = tendon of intrinsic syringeal muscles, tra. = trachea, tym. oss. =
tympanic ossicle, vent. por. = ventral portion.

ventral portion to a varying degree (Fig. 3C). Campylopterus, Phaethornis, Lampornis, Orthorhyn-
The ring's cranial margin is separated from the chus, and "Ornismyia" and in Hylocharis cyanus.
caudal edge of the drum by the lateral margin of My superficial dissection of muscles in G. hirsutus
the lateral lamella, and the ventral end is attached confirmed two major pairs, but observations on
by connective tissue to the apex of the pessulus. Pterophanes cyanoptera revealed additional differ
The head of this ring projects rostrad over the entiation of muscle slips originating midventrally
caudolateral portion of the drum, producing a from the ossified drum, the rostral bronchial rings,
translation articulation. and the caudal tracheal rings. The insertions of three
Attached to the medial surface of each slips were on the ossified head of the first bronchial
tympanic membrane is a partially ossified, ring, whereas other portions inserted more broadly
cartilaginous, tympanic ossicle (ossicula tym- along the first bronchial ring. Naming of humming
panica). The ossicle (Fig. 3C) varies in size and bird muscles must await further study.
shape among species, but in all cases it projects Differences between the syrinx of a swift and
into the extra-syringeal space bounded by the the species of hummingbirds studied (Fig. 3) are
medial tympaniform membrane and the ICM. In summarized in Table 1. I tentatively assume that
single specimens of E. holosericeus and G. hirsu- the character states listed for hummingbirds are
tus sectioned histologically, the ossicle was solid constant for Trochilidae, and that the states listed
cartilage with a thin, ossified layer on all surfaces for a swift are characteristic of Apodidae. If so,
except at the basal contact with the medial tym- the states of hummingbirds are probably synapo-
paniform membrane. The ossicle rests on a liga morphic within Apodiformes.
ment that passes along the membrane from the In a sample of seven species, bilateral syringeal
ossified head of the first bronchial ring to its os nerve branches (ramus syringealis) were inter
sified ventral portion. Medial fibers of the main connected rostral to the syrinx along the cranial
intrinsic muscle insert by a short tendon on the edge of the ventral, intrinsic muscle mass (Eu-
base of the tympanic ossicle. The presence of an toxeres aquila, Anthracothorax nigricollis, Coeligena
ossicle on the external surface of each medial bonapartei, Heliodoxa xanthogonys, Campylopterus
tympaniform membrane of hummingbirds is ap falcatus, C. duidae, and Chalybura buffonii); in three
parently unique among birds (Müller 1878). The others the nerves entered the muscle mass with
ossicle is not homologous with internal cartilages out external interconnection (Amazilia fimbriata,
of certain passerines such as Tyrannidae (Ames A. viridigaster, and Leucippus fallax).
1971) or Pipridae (Prum 1990) because it is not a Functional considerations.—Little is known about
flat, cartilaginous extension of a bronchial or tra functional anatomy in the hummingbird's syrinx,
cheal ring. or about its specific adaptations. In the first free
Müller (1878) and Cannell (1986) described two bronchial ring the cartilaginous portion prob
pairs of intrinsic muscles in unspecified species of ably allows for some change in its shape. Muscle
Table 1. Morphological comparisons of the syrinx in swifts and hummingbirds.
Swift Hummingbird
(A p u s affin is, (G la u cis h irs u tu s ,
Character C h a etu r a p ela g ica ) C o elig en a co elig en a )
Location of syrinx Thorax Neck

Sternotrachealis muscle Present Absent
Intrinsic syringeal muscles Absent Present
Interbronchial ligament Present Absent
Bronchi Diverge caudal Parallel and adjacent
to drum caudal to drum
First bronchial ring Unmodified Enlarged, ossified head
First bronchial ring Separate from drum Head articulates with drum
Lateral lamella Absent Present
Tympanic ossicle Absent Present
Tendon from intrinsic muscles Absent Present
to tympanic ossicle

fibers that originate on the drum and insert on oriented in different directions. Motion of the first
the enlarged, ossified head of the first bronchial bronchial ring probably also causes positional
ring serve to move its head rostrally, laterally, or changes of the lateral lamella.
caudally on its translational articulation with the
drum. A tendon from the medial fibers to the tym The F eeding M echanism
panic ossicle may represent a unique instance in
birds of direct muscle action on the medial tym The feeding mechanism embodies many aspects
panic membrane. All intrinsic muscles apparently of the skull (Fig. 4). Emphasis here is on the up
effect changes in tension of the medial tympanic per jaw (maxilla) and lower jaw (mandibula), the
membrane by moving the first bronchial ring tongue, and the hyobranchial apparatus (appara
or the tympanic ossicle (Fig. 3D). The tympanic tus hyobranchialis). Functions of these structures,
ossicle may serve as a focal point for attachment including cranial kinesis of the upper jaw, strep-
of ligaments of the medial tympanic membrane tognathism of the lower jaw, and motions of the
F ig. 4. Topography and nomenclature of the skull of E u la m p is ju g u la ris . (A) Skull with lower jaw separated;
lateral view. (B) Skull with mandible and part of prepalatal upper jaw missing; dorsal view. 1 = ventral bar,
2 = dorsal bar, 3 = nasal roof, 4 = mesethmoidale, 5 = ectethmoidale, 6 = olfactory sulcus, 7 = supraorbital mar
gin, 8 = interorbital septum, 9 = orbitocranial fonticulus, 10 = optic foramen, 11 = orbital process of quadratum,
12 = postorbital process, 13 = cerebellar prominence, 14 = temporal fossa, 15 = otic pillar, 16 = otic process of
quadrate, 17 = zygomatic process, 18 = lateral condyle of quadrate, 19 = pterygoideum, 20 = jugal arch, 21 =
palatinum, 22 = nasolacrimal sulcus, 23 = rostral mandibular fenestra, 24 = rostral concha, 25 = rostral bar of
palatinum, 26 = maxillary process of nasale, 27 = craniofacial hinge, 28 = ectethmoidale, 29 = insertion area of
stylohyoideus muscle, 30 = sulcus for cucullaris capitis muscle.

tongue driven by muscles of the hyobranchial ap and the palatum articulates with the cranium
paratus, are applicable not only to the mechanism at the parasphenoidal rostrum (rostrum paras-
of nectar eating and arthropod eating but also to phenoidale) and/or the basipterygoid processes
some social displays. (processus basipterygoideus). Features unique to
Trochilidae are emphasized in this section.
P repalatal U pper Jaw The prepalatal upper jaw is basically one of open
construction—that is, the bony nasal opening (aper
Technically, the upper jaw of birds includes a tura nasi ossea) occupies most of its length (Cracraft
rostral portion, the prepalatal upper jaw (maxilla 1988). Although open construction is exempli
prepalata), and a caudal portion, the palatal fied also in long-billed Chardrii and Gruiformes,
upper jaw (palatum), whereas the lower jaw the open construction in hummingbirds becomes
consists of the mandibula. Both jaws articulate obscured during development as explained below.
with the quadratum, which, in turn, suspends All outgroups differ from hummingbirds in
them from the cranium. The prepalatal upper having bills that are short, broad at the base,
jaw of outgroups and passeriform nectarivores and roughly uniform in shape. However, the
is composed of two parts—symphysial (pars symphysial part is short in relation to the nasal
symphysialis) and nasal (pars nasalis). By con part throughout Apodiformes (Cracraft 1988). In
trast, the prepalatal upper jaw of hummingbirds hummingbirds a ventrally concave conforma
includes three parts, regardless of bill length or tion characterizes both the intermediate part (see
shape—symphysial, intermediate (pars inter- below) and the symphysial part, but it becomes
medialis), and nasal (Fig. 5). In most birds the progressively less deep anteriorly and is essen
prepalatal upper jaw forms a craniofacial hinge tially absent at the bill tip. Passerine nectarivores
(zona flexoria craniofacialis) with the cranium, (Nectariniidae) differ from hummingbirds in that
UPPER JA W (MAXILLA)
PREPALATAL UPPER JAW PALATUM
SYMPHYSIAL INTERMEDIATE NASAL

PART PART =ART
par. rosl
cran -fac hm
quad
ros man fen
SYMPHYSAL NTERMED ATE CAUDAL

PART PART PART
FREE RAMUS
LOWER JAW (MANDIBULA)
F ig. 5. Topography and nomenclature of the jaws in hummingbirds. Lower jaw removed from quadrate.
Semidiagrammatic, with cranium shaded. Presence of an intermediate part of the prepalatal upper jaw in adult
hummingbirds is unique within Apodiformes. Abbreviations: b. nas. op. = bony nasal opening, cran.-fac. hin. =
craniofacial hinge, dor. bar = dorsal bar, nas. roof = nasal roof, par. rost. = parasphedoidal rostrum, quad. =
quadratum, ros. man. fen. = rostral mandibular fenestra, ven. bar = ventral bar.

F ig. 6. Prepalatal upper jaw of a hummingbird, showing developmental change in C h lo r o s tilb o n s w a in s o n ii. (A)
Nestling. (B) Adult. Shaded drawings are of cleared and stained specimens in lateral (upper) and dorsal (lower)
views, drawn to same scale. Solid black figures are diagrammatic transverse sections of the intermediate part of
the prepalatal upper jaw. Note the change in orientation of the ventral bars and their association with the dorsal
bar from nestling to adult. Arrows show approximate rostral limit of the nasal part. Vertical hatching represents a
thin portion of the ventral bar that is often missing in skeletal specimens. Abbreviations: b. nas. op. = bony nasal
opening, dor. bar = dorsal bar, lat. wing = lateral wing, nas. = nasale, nas. roof = nasal roof, sym. pt. = symphysial
part, ven. bar = ventral bar.
the symphysial portion is relatively long, the maxillary process (processus maxillaris) of the
intermediate part is essentially absent, and the in premaxillare, are dorsoventrally compressed
ternal concavity is extensively developed within and somewhat concave ventrally. The planes
the symphysial part. of the flattened ventral bars are approximately
Intermedlate part.—In the juvenile humming parallel to the frontal plane, although each tilts
bird (exemplified here in Fig. 6A by Chlorostilbon upward medially (Fig. 6A).
swainsonii) the entire prepalatal upper jaw more Compared with the juvenile, the adult C. swain-
closely resembles the adult bills of outgroup sonii (Fig. 6B) exhibits a more dorsoventrally
taxa and is both proportionally and actually flattened dorsal bar. During ontogenetic, posthatch
shorter than that of the adult. The nasal part is ing metamorphosis the intermediate part elongates
relatively long and the intermediate part rela disproportionately toward adult length. At this
tively short. In the juvenile the dorsal bar (pila time the ventral bars rotate in opposite directions
supranasalis) is moderately long, the symphys- and the medial edge of each moves dorsolaterally
ial part short, and the bony nares extensive. The to occupy a position ventral to the lateral margin
dorsal bar consists of the paired frontal process of the dorsal bar. Thus, each ventral bar becomes
(processus frontalis) of the premaxillare and is an approximately vertical and medially concave
oval in transverse section. The ventral bars (pila lamina (Fig. 6B). Together, the single dorsal and
subnasalis), formed by the premaxillary process paired ventral bars produce an inverted U-shaped
(processus premaxillaris) of the maxillare and trough that houses the tongue and most of the

closed mandíbula. The medial (now dorsal) por medially and lies ventral and parallel to the lat
tion of the ventral bar is well ossified, as is the lat eral wing of the dorsal bar, where the bars are
eral (now ventral) portion. However, between these separated by a venous sinus (sinus venosus) and
well-ossified portions, the ventral bar may be thinly fibrous connective tissue. It is not known whether
or incompletely ossified (Fig. 6B). The result in an rostrocaudal translational movement of the ven
adult skeleton is often that the middle portion of tral bar in relation to the dorsal bar is possible.
the lateral wall of the prepalatal upper jaw may be Nasal part.— The maxillary process of the nasale
artifactually missing after preparation and may (processus maxillaris nasale) in adult humming
therefore comprise two bars rather than one. This birds is flattened and appears to have undergone
may account for an apparent extra bar in the prepala torsion along its length (Fig. 8), a conformation
tal upper jaw of hummingbirds described by Bühler apparently unique to hummingbirds (Moller
(1981) as the "palatine bar (rostral part)." Probably 1930, Livezey and Zusi 2006). This configura
all juvenile hummingbirds undergo a posthatching tion probably results from restructuring of bone
metamorphosis to produce the unique adult struc during development to accommodate passage of
ture. The effect of axial rotation of the ventral bar an adjacent artery (probably arteria ethmoida-
is that the original nasal opening is closed rostrally lis, ramus lateralis). The nasal part of the upper
and is relatively short caudally in adult humming jaw includes the nasal cavity (cavitas nasale) and
birds, regardless of bill length (Fig. 6B). its associated rostral conchae (concha rostralis),
A histological transverse section through the the latter unossified in outgroups but ossified
prepalatal upper jaw of G. hirsutus (Fig. 7) shows in many hummingbirds. (Variation in the cav
that the dorsal bar has a central rod of cancellous ity and conchae is described for hummingbirds
bone flanked on either side by a thin, lateral wing in Section II.) Caudally, the nasal part is defined
(ala lateralis). The dorsal margin of the vertical largely by the morphology of the nasale and its
portion of the ventral bar is sharply inclined relation to the bony nasal opening and the cra
niofacial hinge (Fig. 8A). Partial ossification of the
roof of the nasal part (tectum nasi) occurs rostral
to the nasale in Trochilines, but in Hermits the
ossified nasal roof abuts the nasale, and both os
sifications influence the posterior contour of the
bony nasal opening. The latter configuration oc
curs also in some swifts (e.g., Streptoprocne semi-
collaris). Eutoxeres differs from other Hermits in
that the notch medial to the maxillary process of
the nasale extends caudally almost to the cranio
facial hinge. Although Hermits and Trochilines
differ from each other in the structure of the na
sal part, both differ from the simple structure of
Hemiprocnidae and most Apodidae (Fig. 8B), in
which a nasal roof is absent or very small.
C raniofacial H inge
F ig. 7. A histological section through the tongue and
intermediate part of the prepalatal upper jaw of an adult The base of the prepalatal upper jaw and the cranio
hummingbird (G lau cis h irsu tu s). Semidiagrammatic. facial hinge (or bending zone) of birds have been
Bone is solid black. The arrow shows the dorsal por characterized as either holorhinal or schizorhinal
tion of the ventral bar, narrowly separated from the lat (Garrod 1873b). "Holorhinal" indicates a caudal
eral wing of the dorsal bar by connective tissue and a
border of the bony nasal opening that terminates
venous sinus. Rostrocaudal motion of the ventral bar
rostral to the craniofacial hinge and usually is more
in relation to the dorsal bar (not yet demonstrated in
or less rounded. "Schizorhinal" typically indicates
hummingbirds) is required for independent raising and
lowering of the tip of the upper jaw (demonstrated in a bony nasal opening that extends caudally beyond
some hummingbirds). Abbreviations: con. tis. = connec the craniofacial hinge (Garrod 1873b, Bock 1964,
tive tissue, dor. bar = dorsal bar, lat. wing = lateral wing, Zusi 1984) in a narrow or slit-like (less commonly
ven. bar = ventral bar, ven. sin. = venous sinus. rounded) contour. In Trochilines, the bony nasal

F ig. 8. Variation in the craniofacial hinge and bony nasal openings of hummingbirds compared to other
Apodiformes. Dorsal views, with most of the prepalatal upper jaw missing in the hummingbirds. (A) Partial hum
mingbird skull for orientation of detailed drawings in B and C. (B) Triangles point to the transverse axis or axes of
the craniofacial hinge, showing the continuous, single axis in the Hermit (G lau cis) and the transected, double axes
in the Trochilines (A n d rod on a n d A n th ra co th o ra x ). Black triangles show the medial portion of the double hinge. A
nasal roof, prominent in most Trochilines, is absent or small in Hemiprocnidae and Apodidae. (C) Comparison of a
Hermit (left) and a Trochiline (right). Stipple represents the nasal roof. The hatched membrane in adult Trochilines
(ossified in nestlings) is visible in spirit specimens but lost in skeletons. Its widespread occurrence is inferred
from the angled medial margin of the maxillary process of the nasale in skeletons of adult Trochilines. See text.
Abbreviations: b. nas. op. = bony nasal opening, cr.-fac. hin. = craniofacial hinge, dor. bar = dorsal bar, max. pr.
nas. = maxillary process of nasale, memb. = membrane, nas. = nasale, nas. roof = nasal roof, ven. bar = ventral bar.
opening extends caudally almost to, or usually be other through the medial portion of the nasale
yond, the craniofacial hinge, and therefore they are and the frontal process of the premaxillare (Fig.
essentially schizorhinal. Aegothelidae, Hemiproc- 8 A). If the two axes are sufficiently separated, cra
nidae, Apodidae, and Hermits are holorhinal. nial kinesis produces forces that require bending
In many schizorhinal birds the craniofacial not only at the craniofacial hinge but also within
hinge has two axes of bending (diaxial), one the prepalatal upper jaw (rhynchokinesis) (Zusi
through the lateral portion of the nasale and the 1962, 1984). Close apposition of the two bending

axes in Trochilines probably reduces the conflict as a flattened blade between the rostral bar and
ing forces, and rhynchokinesis may be minimal. rostromedial process (processus rostromedialis)
Hermits have only a single axis (monaxial). of the palatinum (Fig. 9B, C). The rostral bar is
Conformation of the nasale and bony nares is dorsoventrally compressed rostrally, forming a
complicated in Hermits by partial ossification of palatine hinge (zona flexoria palatini). In hum
the nasal roof, and in Trochilines by bone resorp mingbirds the palatal process of the maxillare is
tion during development. An understanding of broad at its base and narrow medially, and it is
the nasale in adult Trochilines is best gained by fused with the dorsal margin of the rostral bar
revisiting the juvenile and adult specimens of (Fig. 9D). The resulting T-bar structure resists lat-
C. swainsonii discussed above. The nestling is eromedial and dorsoventral bending and forms
holorhinal, with bony nasal openings ending in a a firm pterygopalatine arch (arcus pterygopalati-
rounded contour rostral to the craniofacial hinge nus) between the palatum and prepalatal upper
(Fig. 6A). During development the calcified ros- jaw. In some apodids the medial portion of the
trodorsal portion of the nasale evidently becomes palatal processus has limted synostosis with the
decalcified and the unossified portion of the nasal medial edge of the rostral bar, but both processes
opening is correspondingly expanded caudally are dorsoventrally flattened, and dorsoventral
beyond the craniofacial hinge; however, the origi flexibility exists as a palatine hinge.
nally calcified portion of the nasale is still discern Vomer.— The avian vomer is derived from
able as a thickened portion of the membranous bilaterally paired elements and consists of a body
roof of the nasal cavity, and the angular projec (corpus vomeri) and paired pterygoid processes
tion on the medial rim of the maxillary process (processus pterygoideus). The vomer of Aegothe-
of the nasale in most adult Trochilines indicates les is markedly pneumatic and inflated (Fig. 9A).
the rostral location of the thickened membrane Its body is rod-like and truncate rostrally, and
(see Fig. 8C). Thus, C. swainsonii changes from it abuts the palatal process of the maxillare just
monaxial and holorhinal in the nestling to diaxial medial to the palatinum. At that juncture the
and schizorhinal in the adult, a transformation palatal process terminates or extends slightly
that may be typical of Trochiline hummingbirds. caudad, but it lacks the prominent caudal exten
sion seen in Hemiprocnidae and Apodidae. The
Palatum pterygoid processes are variously fused rostrally.
In Hemiprocnidae and Apodidae the vomer is
The palatal upper jaw or palatum, as defined less pneumatic and the pterygoid processes less
here, consists of the membrane bones forming fused; the body is blunt rostrally but flared rostro-
the roof of the pharynx. Specifically, it includes laterally to form processes that closely approach
the jugal arch (arcus jugalis), quadratum, ptery- or abut the medial base of the palatal process as a
goideum, palatinum, vomer, and portions of the syndesmosis (Fig. 9B, C).
maxillare (Fig. 9). Whether or not hummingbirds The vomer in hummingbirds (Fig. 9D) makes
and swifts have an aegithognathous palate has no direct contact with any part of the maxillare,
been debated (Huxley 1867, Parker 1878, Lowe and the anterolateral margin of the vomeral body
1939), but this question is less important than is only distantly connected by membrane to the
comparison of the individual constituents of the palatal process of the maxillare and the caudal
palatum (Zusi and Livezey 2006). tip of the rostral concha (concha rostralis). Lowe
Maxillare.— In all outgroups the palatal process (1939) stated that the pterygoid process of the vo
of the maxillare (processus palatus maxillaris, of mer abuts the anterior tip of the pterygoideum,
ten referred to as "maxillopalatine") passes dor but my interpretation of a cleared and stained
sal to the rostral portion of the palatine, or rostral specimen of a juvenile C. swainsonii is that the
bar (pila palatini; synonym of "processus rostralis caudal portion of the palatinum separates these
palatini" of Zusi and Livezey 2006), with limited bones. In any case, Lowe's contention that hum
or no direct contact between them. In Aegotheli- mingbirds display a "palaeognathous condition"
dae the palatal process passes medial to the ros is unjustified (Zusi and Livezey 2006).
tral bar of the palatinum and becomes truncate or Unlike all outgroups, almost all hummingbirds
angled slightly caudad (Fig. 9A). By contrast, in exhibit a bony, vomeral spine (spina vomeris) di
Hemiprocnidae and Apodidae a marked caudal rected rostrally from the vomeral body (Fig. 9D).
extension of the tip of the palatal process occurs The spine lies ventrally within the nasal septum

F ig. 9. Palatum of Aegothelidae and Apodiformes. Ventral view. The parasphenoidal rostrum is vertically
hatched, the lateral part of the palatinum is obliquely hatched, and the vomer is solid black. Abrupt, caudal
broadening of the parasphenoidal rostrum, extreme reduction of the lateral part of the palatinum, lateral dis
placement of the pterygoid process of the palatinum, and presence of a vomeral spine characterize Trochilidae.
(A) Aegothelidae (A eg o th eles). (B) Hemiprocnidae (H em ip ro cn e). (C) Apodidae (H iru n d a p u s). (D) Trochilidae
(T h ren etes). Abbreviations: ect. = ectethmoidale, jug. arch = jugal arch, lat. pt. = lateral part of palatinum, max. =
maxillare, pal. hin. = palatine hinge, pal. pr. = palatal process of maxillare, pter. = pterygoideum, pt.-pal. art. =
pterygopalatine articulation, pt. pr. pal = pterygoid process of palatinum, ros. bar = rostral bar of palatinum, ros.
pr. = rostromedial process of palatinum, sw. = swelling of parasphenoidal rostrum, ven. cho. lam. = ventral choanal
lamella of palatinum, vom. = vomer, vom. sp. = vomeral spine.
(septum nasi), and it may be strong and linear or Palatinum.—In most birds, including humming
more slender and sometimes angled dorsally. As birds as described above, the pterygopalatine arch
an artifact, the entire spine may become displaced transmits compression and tension forces during
toward the dorsal bar of the upper jaw in cleaned cranial kinesis (Zusi and Livezey 2006). In out
skeletons. groups of this monograph, the rostral bar of the

palatinum is dorsoventrally flattened, forming a hummingbirds has been interpreted as fused

palatine hinge just caudal to its association with basipterygoid processes by some authors. For
the maxillare. The palatine hinge is associated example, Parker (1879) and Lowe (1939) each
with prokinesis. By contrast, in hummingbirds stated that the "basipterygoid process" in hum
the rostral bar has a T-bar form and lacks a pala mingbirds was shifted farther forward than in
tine hinge, thus providing a stronger arch that is any other bird. In swifts and crested swifts a few
compatible with rhynchokinesis. Therefore, I dis adult specimens retain nonfunctional vestiges
agree with the conclusion of Moller (1930) that the or spicules of basipterygoid processes caudal to
palatinum of hummingbirds is too thin anteriorly the pterygoidal articulation on the parasphenoi
to be useful for transmitting forces during kinesis. dal rostrum (Hemiprocne mystacea USNM 560827,
Caudal to the rostral bar, the palatinum of 560829; Streptoprocne niger USNM 290999, 555770;
hummingbirds consists largely of a choanal part, S. phelpsi USNM 622775, 622774; S. rutilus USNM
which delimits a portion of the respiratory pas 614122). Similar vestiges, and corresponding
sage. Although the dorsal choanal lamella (lamella spicules on the pterygoideum, also occur rarely
choanalis dorsalis) is poorly developed in hum in Podargidae (Batrachostomus javensis AMNH
mingbirds, the ventral lamella (lamella choanalis 9189), indicating their loss in most Apodidae,
ventralis) is prominent and broad caudally, with Hemiprocnidae, and Podargidae. I found no such
wide bilateral separation of the pterygoid pro vestiges in hummingbirds.
cesses of the palatinum (Fig. 9). The choanal region The pterygoideum of outgroups has a uniform,
in outgroups is less expanded, and the pterygoid rod-like shape and lacks a dorsal process (pro
processes (processus pterygoideus) of the pala cessus dorsalis). Anteriorly the pterygoideum
tines abut or closely converge toward the midline. articulates with the parasphenoidal rostrum and
The lateral part of the palatinum (pars lateralis with the palatinum. Caudally, the articulation in
palatini) is well developed in Aegotheles, and in Aegotheles, Hemiprocnidae, and Apodidae is a
Hemiprocnidae and Apodidae typically forms as ball-and-socket structure located ventral to the
a prominent, caudolaterally directed process (Fig. orbital process (processus orbitalis) on the body
9). By contrast, the lateral part of the palatinum in of the quadratum (corpus quadratum), with
hummingbirds is restricted to a small tubercle or additional linear contact dorsally on the quad
short hook (hamulus). As noted by Lowe (1939), rate body. The linear contact is reduced or lost in
development of the lateral part of the palatinum hummingbirds, leaving only the ball-and-socket
is correlated with width of the mouth—it is wide joint.
in outgroups and narrow in hummingbirds. The palatine part of the pterygoideum (pars pa
From the tip of the lateral part of the palatinum, latina pterygoidei)— "mesopterygoid" of Parker
m. pterygoideus passes caudally to the tip of the (1879)—in juvenile swifts becomes fused with the
medial process of the mandible (processus me- palatinum in adults. Thus, the articulation that
dialis mandibulae; Morioka 1974, Zusi and Bentz appears to be between pterygoideum and palati-
1984). This portion of m. pterygoideus is thus num in adult swifts is actually between the pala
oriented roughly parallel to the midsagittal plane tine part of the pterygoideum and the main body
of the skull throughout Apodiformes, maximiz of the pterygoideum (pars proprius pterygoidei)
ing its efficiency in lowering the prepalatal upper and represents an intrapterygoid articulation
jaw (kinesis) and in rotating the caudal part the (articulatio intrapterygoidea). The same is true
mandiblar ramus laterally (streptognathism). of hummingbirds, as seen in juvenile and adult
Pterygoideum and basipterygoid process.—A C. swainsonii (see also Parker 1879). However,
functional basipterygoid process is absent from the intrapterygoid articulation may be present
Aegotheles and Apodiformes. The pterygopara- or absent in adult hummingbirds, and localized
sphenoidal articulation (articulatio pterygopar- flexibility of the bone probably exists even in its
asphenoidalis) in swifts is denoted on the absence (see Zusi and Livezey 2006). A pterygo
parasphenoidal rostrum by a faint swelling. In palatine articulation (articulatio pterygopalatina)
hummingbirds this articulation occurs on the an is present in Aegotheles and Apodiformes.
terior, medially inclined surface of a marked swell Quadratum.—The orbital process of the quadra-
ing near the base of the parasphenoidal rostrum tum is extremely reduced in Aegothelidae, and is
(Fig. 9D). The swelling is more pronounced short, blunt, and narrow in Hemiprocnidae and
caudally and ends abruptly. This structure in Apodidae. In Trochilidae the process is better

developed and often manifested as an acute an the rostral mandibular fenestra and throughout
gle of the rostral margin of the quadratum in the intermediate part of the ramus. Their man
lateral view (Fig. 4A: 11). As noted by Shufeldt dibula differs from that of passerine nectarivores
(1885) for Archilochus alexandri, the long axis of in greater length of the free rami in relation to the
the otic process (processus oticus) of the quadra- symphysial part (Fig. 10A, D).
tum in lateral view is oriented more horizontally Unlike outgroups, all bones of the adult
in many hummingbirds than in outgroups. I did mandible of hummingbirds are fused.
not measure variation in this character through
out hummingbirds, but it may play a significant Jaw A rticulation
role in kinesis and nectar eating (see below under
CRANIAL KINESIS). The quadratum of hum The quadratum of Apodidae and Hemiprocni-
mingbirds and all outgroups is similar in having dae has a prominent, ridge-like medial condyle
pneumatic foramena (foramen pneumaticum) on (condylus medialis) of the quadratomandibular
the caudal surface of its otic process and in lack articulation oriented caudolaterally to rostrome-
ing a caudal condyle (condylus caudalis). dially. The articular fossa (fossa articularis) of the
The jugal arch articulates with the quadratum mandible in outgroups contains a moderately
at a deep cotyla in the anterolateral surface of the developed lateral cotyla (cotyla lateralis) and
lateral condyle (condylus lateralis) of the quadra- well-developed medial cotyla (cotyla medialis),
tum in hummingbirds (Fig. 4A: 18), but it rests on both trough-like, oriented rostromedially, and
top of the condyle as a weak syndesmosis in out bordered by prominent ridges. The pneumatic
groups. The lateral condyle of hummingbirds is foramen (foramen pneumaticum) of the articu
located more distally on the body of the quadrate lare opens just medial to the medial cotyla, and
than in outgroups. there is no pronounced medial process medial
to the foramen. By contrast, hummingbirds (Fig.
M andibula 10B) have a poorly defined lateral cotyla and a
shallower, more caudo-rostrally oriented medial
The avian mandibula may be divided into (1) a cotyla, neither of which is bordered by a promi
symphysial part with a more-or-less protrusive nent ridge. The pneumatic foramen lies between
tip where the rami (ramus) abut rostrally and the caudal end of the medial cotyla and a well-
become fused, and (2 ) the diverging free rami defined, medial process of the mandible.
(Fig. 5). The latter are subdivided into two parts; A medial portion of the postorbital ligament
the intermediate part (pars intermedia) and the (ligamentum postorbitale) attaches on the jugal
caudal part (pars caudalis), often separated by arch in some hummingbirds. The main, lateral
the rostral mandibular fenestra (fenestra rostra- portion of the ligament makes no separate connec
lis mandibulae). The caudal part of the ramus tion with the mandibula. Instead it merges with
receives insertions of jaw muscles and the facets the lateral jugomandibular ligament (ligamen
and condyles of the quadratomandibular articu tum jugumandibulare laterale), which extends
lation (articulatio quadratomandibularis). The rostroventrally from the caudal end of the jugal
mandibular symphysis approximately equals the arch or adjacent quadratum to the lateral surface
symphysis of the prepalatal upper jaw in length of the mandibula (Fig. 10C).
in Aegotheles and Apodiformes.
Lateromedial flexibility is present in the rami CRANIAL KINESIS
of Aegotheles and Apodiformes, particularly at
two intramandibular hinges of the ramus—an Despite the name, "cranial kinesis" in modern
anterior one (zona flexoria intramandibularis birds does not refer to mobility of parts of the cra
rostralis) caudal to the symphysial part and a nium, but rather to movement of the upper jaw
caudal one (zona flexoria intramandibularis on the cranium, or mobility within the prepalatal
caudalis) between the intermediate and caudal upper jaw.
parts. Only in Aegothelidae does a narrowing of Apodiformes.—The configuration of the jaw
the rami mark the anterior hinge, and the caudal in Aegotheles, Hemiprocnidae, Apodidae, and
hinge is poorly demarked or absent in Apodi- Hermits is holorhinal, and the jaw motion is
formes. Lateromedial flexibility of the free ramus prokinetic around a single craniofacial hinge
in hummingbirds is possible at or just caudal to axis, as confirmed by manipulation of hydrated

F ig. 10. Mandibula and associated ligaments typical of hummingbirds, and a mandibula typical of nectarivo-
rous passerines. (A) Mandibula of hummingbird in ventral view. Long arrow shows force vector of pterygoideus
muscle on the medial process of the mandibula, associated with lateral motion (short arrow) at the caudal bend
ing zone of the free mandibular ramus around the rotational axis (black dot) of the jaw articulation. (B) Detail
of articular fossa of a hummingbird mandibula in dorsal view of the left ramus. Most notable is the presence
of a process (med. pr.) that is lacking in other Apodiformes. (C) Jaw articulation of hummingbird; jaw muscles
shaded, and mandibular ligaments shown in black; left, lateral view. Unlike other Apodiformes, the postorbital
ligament has no separate attachment on the mandibula; instead it joins the lateral jugomandibular ligament in
a common attachment. (D) Mandibula typical of nectarivorous passerines, showing much enlarged symphysial
part; there is little or no lateral motion of the free ramus. Abbreviations: add. m. = adductor mandibulae externus
muscle, caud. pt. = caudal part of mandibular ramus, fr. ram. = free mandibular ramus, lat. cot. = lateral cotyla,
lat. jug. lig. = lateral jugomandibular ligament, mand. = mandibula, med. cot. = medial cotyla, med. pr. = medial
process of mandibula, pn. for. = pneumatic foramen, po. lig. = postorbital ligament, post. pr. = postorbital pro
cess, quad. = quadrate, sym. pt. = symphysial part of mandibula.
skeletons. Some Trochiline hummingbirds and the portion of the craniofacial hinge formed by the
non-apodiforms, notably many charadriiforms nasale, and two hinge axes are usually present.
and gruiforms, pigeons, and ibises, have an upper This configuration of the jaw is schizorhinal and
jaw that is flexible at one or more hinges rostral the jaw motion, which usually entails dorsoven-
to the craniofacial bending zone. The bony nares tral bending of the bill tip, is rhynchokinetic (Zusi
extend backward, sometimes as a slit, to transect 1984). Several early studies indicated presence of

independent bill-tip movement in hummingbirds fluid. The tip appeared to be the only portion of
(Nitzsch 1816, 1817; Moller 1930; Simonetta 1967). the upper jaw in motion. Slight bending of the tip
Prokinesis maintains static relations between of the upper jaw is shown by Rico-Guevara and
the dorsal and ventral bars of the prepalatal upper Rubega (2011; compare frames A and C of fig. 4)
jaw during jaw movement because the two bars in high-speed video frames of a captive Amazilia
are firmly connected proximally by the nasale. cyanifrons. These data suggest that distal rhyn-
Rhynchokinesis includes rostrocaudal transla chokinesis facilitates nectar eating in at least two
tional motions of the ventral bar in relation to the Trochiline species, and probably many others.
dorsal bar, made possible by separation of the Kinetic motion at the tip of the upper jaw occurs
nasale into two independent parts. Thus, fusion while the rest of the bill maintains a nearly closed
of the nasal capsule or conchae with both bars tube for nectar transport.
of the upper jaw are possible only in prokinetic My manipulation of fresh specimens of hum
birds. Despite extensive ossification in the nasal mingbirds, causing wide opening of the jaws,
region of many hummingbirds, the lack of synos produced marked bending at the craniofacial
tosis with the ventral bar in any hummingbird is hinge in G. hirsutus and P. guy, and moder
compatible with rhynchokinesis. ate bending in Anthracothorax nigricollis and
These morphologies are reflected by devel Amazilia tobaci. If these examples reflect differ
opmental changes in C. swainsonii. During post ences in both form and magnitude of cranial
hatching development, that species (and all kinesis between Hermits and Trochilines, they
other Trochilines?) transforms a holorhinal and supplant the tentative conclusions about hum
potentially prokinetic, prepalatal upper jaw into mingbird kinesis by Zusi (1984). There are no
a schizorhinal and presumably rhynchokinetic data on kinesis for Hermits during nectar eating,
one, while also, curiously, reducing the probabil but with the bill opened widely they appear to
ity of independent motion of the ventral and dor exhibit prokinesis.
sal bars required for rhynchokinesis. Such motion Bending within the upper jaw of highly rhyn-
would depend on the elasticity of the connective chokinetic Scolopacidae occurs usually at flat
tissue connecting the ventral and dorsal bars (Fig. tened regions (hinges) of the dorsal and ventral
7). It is also possible that the midsection of the bars, and the axes of bending are circumscribed
ventral bar is less mineralized and more flexible (Zusi 1984). Free rostrocaudal movement of the
than its dorsal and ventral portions (Meyers and ventral bars in relation to the dorsal bar causes
Meyers 2005), allowing the bar's ventral por the bill tip to rotate about the distal hinge on the
tion to move forward and backward, parallel to dorsal bar. Even the longest-billed shorebirds
its more stabilized dorsal portion—a movement (e.g., Long-billed Curlew) maintain the integ
analogous to that in rhynchokinetic shorebirds. rity of their bill shape under the forces of prob
Unfortunately, precise measurements of cranial ing by a strongly configured dorsal bar (caudal
kinesis of live hummingbirds and knowledge of to its anterior hinge), and by immobility of the
the physical properties of the structural compo medial portion of the craniofacial hinge by fusion
nents of the prepalatal upper jaw are lacking. The with the underlying mesethmoid. Some long
following observations are related to kinesis, first billed hummingbirds (e.g., Ensifera and Coeligena)
in nearly closed mandibles and second in widely have similarly lost mobility of the medial portion
opened ones. of the craniofacial hinge, leaving distal (bill tip)
In 1986, I observed captive birds (Archilochus rhynchokinesis as their only option.
colubris) drinking sugar water from an inverted Cranial kinesis always is driven by muscles
tube feeder (see below under STREPTOGNA- that rotate the quadratum about its squamoso-otic
THISM). At rest, the tomia of the bill tips met pre articulation(articulatioquadrato-squamoso-otica).
cisely when closed. While feeding, the tips of the The anteroposterior component of this motion is
upper and lower mandibles separated enough transmitted through the palatum to the ventral
to permit the tongue to flick in and out. In lat bars of the prepalatal upper jaw. In prokinetic
eral view the bill tips vibrated dorsoventrally birds this produces rotation of the entire prepala
without actually closing, as the tongue flicked in tal upper jaw around the craniofacial hinge axis. In
and out. During feeding, the tongue protruded rhynchokinetic species, palatal motion is passed
a third or less the length of the bill whether the directly to the ventral base of the symphysial part
bill tips were submerged in or just beyond the through the ventral bar, causing upward tilt of

the tip of the jaw around the anterior hinge of the accommodated by a deep, internal concavity of
dorsal bar. Even a slight anteroposterior motion the symphysial part and of the adjacent portion
of the ventral bar in a slender upper jaw would of the nasal part. In the most highly specialized
cause significant rotation of the symphysial part species the ventral bar and adjacent wall of the
(Zusi 1984). A more horizontal orientation of the symphysial part are oriented dorsomedially, and
body of the quadratum in hummingbirds men superficially resemble that of hummingbirds. The
tioned earlier would limit the forward compo lateral walls of the passerine upper jaw, how
nent of the quadrate's rotation and maximize the ever, are less vertical than in hummingbirds, and
mechanical advantage of m. protractor quadrati they are largely associated with the symphysial
et pterygoidei muscle on the quadrate— actions part (Fig. 10). Except at the tomia, the lower jaw
that would raise the symphysial part of the up does not fit within the upper jaw as it does in
per jaw forcefully through a limited angle. The hummingbirds.
symphysial part is lowered when m. pseudo-
temporalis profundus rotates the quadratum STREPTOGNATHISM
ventrolaterally. Antagonistic actions of these two
muscles could be significant for safely maintain Many birds have (at least limited) lateromedial
ing rapid but limited motions of the bill tip dur flexibility of the mandibular rami associated with
ing nectar eating. lateromedial rotation at the quadratomandibular
By contrast, arthropod eating often employs articulation (Zusi 1967, Zusi and Warheit 1992).
wide opening and rapid closing of the jaws. Streptognathism is the capability of pronounced
Maximum opening is effected by m. protractor lateral bowing within the rami of the mandibula
quadrati et pterygoidei (raising the prepalatal in the living bird (Buhler 1981). This capability is
upper jaw) and m. depressor mandibulae (depress indicated by the presence of two ramal bending
ing the lower jaw). Maximum power for closing the zones (hinges), a rostral one near the symphysial
jaws is found in m. pterygoideus (prepalatal upper part and a caudal one between the rostral and
jaw) and m. adductor mandibulae externus and caudal parts of the rami. The caudal intraramal
m. pseudotemporalis superficialis (mandibula). hinge is not vertically oriented on the horizontal
Lack of extensibility in the postorbital ligament of ramus; rather, its axis slopes caudoventrally from
many birds may play a role in coordinating open the dorsal margin in lateral view. As a result,
ing of both jaws (Bock 1964, Zusi 1967). This role when lateral bowing occurs at the hinge, the por
may pertain in Chaetura and Hemiprocne because tion of the bill anterior to the hinge also bends
the postorbital ligament makes direct contact with downward in relation to the rest of the man
the mandibula. In hummingbirds the postorbital dibula (Zusi and Warheit 1992). Streptognathism
ligament merges at an obtuse angle with the lat allows some aerial insect-eaters (Caprimulgidae)
eral jugomandibular ligament (Fig. 10C). Tension to broaden the opened mouth as a funnel (Buhler
in the postorbital ligament would not occur until 1970); the mechanism for similar broadening of
the rostral section of the lateral jugomandibular the mouth in Apodidae has not been studied (but
ligament became collinear with the main portion see photograph of Apus in Tidman 2007:489).
of the postorbital ligament in the widely opened Pelicans and some hummingbirds are unusual
mandible, as confirmed by my manipulation of the in their capability of strong streptognathism,
jaws in cleared and stained specimens. The postor despite the absence of an anatomically defined
bital ligament therefore has no coupling effect on caudal intraramal hinge. The degree of flexibility
the nearly closed jaws during nectar eating. in bone of the pelican's mandibula is inversely
Passeriformes.—Long-billed nectarivores occur in related to its mineral content (Meyers and Meyers
only two avian orders within Aves—Apodiformes 2005), a relation that may also pertain to flexibil
(Trochilidea) and Passeriformes (Meliphagidae, ity in hummingbirds.
Zosteropidae, Nectariniidae, Drepanidini, Thrau- Activation of m. pterygoideus at its attachment
pini, and Mohoidae; see Fleischer et al. 2008). All on the medial process of the mandible causes lat
of these birds also eat arthropods. The upper jaw eral rotation of the caudal portion of the ramus
of passerine nectarivores is holorhinal and has a around the quadratomandibular articulation
monolithic structure that bends only at a single (Fig. 10A) and maximum widening between the
craniofacial bending zone (prokinesis). Housing bilateral, caudal intraramal hinges. Stored energy
of the tongue and transportation of nectar are within the bent mandible probably reverses

bowing upon relaxation of the muscle, perhaps Orthorhynchus cristatus, and Cyanophaia bicolor), ob
aided by contraction of m. intermandibularis. In served in the field, the mandibles did not always
hummingbirds the lateral contour of a relaxed form a tight seal during drinking, and some liq
ramus of the closed mandible is somewhat con uid escaped along the tomia. Whether this limited
cave in dorsal or ventral view, such that the entire streptognathism occurred through muscle contrac
rostral portion of the mandible is markedly nar tion (m. pterygoideus) or passively by pressure of
rower than the caudal portion. nectar within the mandibles is unknown. In either
I have observed a limited form of streptogna- case it apparently expanded the tubular structure of
thism of the fully closed jaw in captive humming the bill during nectar transport. In passerine nectar-
birds (Archilochus colubris) while they drank nectar. eaters, the mandibular symphysis is long, constant
Observations with a dissecting microscope were in shape, and suitable for transporting nectar in the
made on an adult male, two females, and an im closed bill (Fig. 11C). Whether the tube is main
mature male. From ventral view of birds that were tained during nectar uptake is not known.
not feeding, I saw a gap between the lateral walls A well-developed streptognathism of the
of the lower and upper mandibles from the sym- opened mandible also occurs in some humming
physial part to the rictus, and the intermandibular, birds. A few species of Phaethornis are known
gular region (regio gularis) was concave. When to spread the rami of the opened jaw during
feeding began, the mandibular rami spread lat display, revealing a brightly colored mouth lin
erally and made contact with the ventral bars of ing. Reference to spreading is stated explicitly
the upper mandible and the gular region became by Snow (1973b) for P ruber, Snow (1974) for P.
stretched and flattened (Fig. 11A, B). These relations guy, Stiles and Wolf (1979) for P guy, and Schuch
were maintained throughout feeding, and no nec mann (1987) for P griseogularis. Snow (1973b:171)
tar leaked from the jaws except for several drops observed that "In displaying the gape the rami
at the rictus. In other species (Eulampis jugularis, of the lower mandible were spread wide apart
F ig. 11. Structure of the mandibles in relation to nectar eating in hummingbirds and passerines. Semidia
grammatic representation of mandibles in ventral view (right), and transverse section, with upper mandible
shown in black (left). (A) Mandibles of a hummingbird while relaxed, showing a lateral gap between the mandi
bles in solid black (above), and while drinking, with manibular rami spread, the gular region stretched, and the
gap between mandibles closed (below). In lower left, note the increased space for nectar transmission in the bill
while drinking. (B) In passerines, nectar transmission is largely through the symphysial parts of the mandibles,
and there is no capacity for spreading of the mandibular rami. Abbreviations: gul. = gular region, l. mand. =
lower mandible, sym. pt. = symphysial part, u. mand. = upper mandible.

so they were about four times further apart which can be flexed or extended on the basi
than when the beak is closed." Similarly, Snow hyale in both frontal and midsagittal planes. The
(1974:285) noted that epibranchiale abuts the caudal end of the cera
tobranchiale at a syndesmotic articulation, and
The gape-flash is very spectacular and looks like together they constitute the hyoid horns. Caudal
the sudden flashing of a red light in the dark to the ceratobranchiale articulations, an ossified
forest. This effect is produced by the light shin urohyale is fused with the basihyale in swifts and
ing through the red skin of the gape stretched
hummingbirds. The urohyale of swifts supports
between the rami of the lower mandibles. The
the larynx, but that of hummingbirds is shorter
two rami are flexible and when the bird opens
its beak to make the to c k they bow apart to a dis
and there is no support for the larynx by the
tance of approximately 15mm. hyobranchial skeleton. Through its extrinsic and
intrinsic muscles, the hyobranchial apparatus
supports and moves the tongue and floor of the
INTEGRITY OF THE BILL pharynx. When the bill is closed and the tongue
retracted, the tongue and paraglossales occupy
How does the long, slender bill of the Sword the mouth cavity and the ceratobranchiales lie
billed Hummingbird (Ensifera) maintain its shape largely below the floor of the mouth; the basi-
against external forces and while performing hyale represents a link between the tongue and
precise motions of the bill tip when drinking nec hyoid horns (Fig. 12). With respect to humming
tar? Motions of the tip of the upper mandible in birds, Weymouth et al. (1964:254-255) wrote that
Ensifera and in other Trochilines originate in the
quadratum and are transmitted to the ventral bars Lying immediately deep to M. mylohyoideus is a
within the sheath of the ramphotheca. The pre tough sheet of tissue which forms part of the floor
palatal upper jaw of hummingbirds is inherently of the oral cavity. Within the oral cavity the basihyal
and its musculature are surrounded by a dense tube
flexible throughout much of its length because
of fibrous tissue formed by a series of ringlike bands
the dorsal and ventral bars are usually long and
separated by less dense connective tissue. This
flattened. In adult birds the upper mandible dense tube is composed of an outer, covering layer
forms a partial tube. This skeletal morphology of statified squamous epithelium underlain first by
and the leathery rhamphotheca resist bending a thin layer of loose connective tissue and then by
in any plane unless stressed by cranial kinesis or a dense ligament containing large amounts of col
external forces other than gravity. Additionally, lagenous and elastic fibers. The tube apparently
in the closed bill, the lower mandible is largely holds the basihyal in position and permits it to move
embraced by the upper mandible, completing freely as the tongue is protruded or retracted.
a tubular conformation that strengthens even
extremely long, slender, and lightweight bills. I refer to this tube as "elastic tube" (tuba elastica)—
General flexibility, possibly related to reduced a structure noted over a century ago, but not named,
mineral content of the bone, would permit bend by Lucas (1897). The tongue of outgroups is short,
ing and protect the bill from fracture if stressed broad, and roughly triangular, whereas that of hum
externally. Such forces may be considerable mingbirds is long and slender. Neither the elas
when hummingbirds peck at rivals during terr tic tube nor capability for strong protrusion of the
itorial fights. tongue is present in the outgroups.
The paraglossales of hummingbirds are short
H yobranchial A pparatus despite their support of a long, partly carti
laginous tongue that occupies most of the bill.
In outgroups and hummingbirds this complex In spirit specimens the tongue of Ensifera en
consists of the fleshy tongue and its supporting sifera (USNM 505429) was 104 mm long and the
hyobranchial apparatus (Fig. 12) and muscles. lower jaw (from the rictus (angula oris) 108 mm,
The tongue is supported basally by a paired para- whereas the tongue of Ramphomicron microrhyn-
glossum that articulates with the basihyale. The chum (USNM 615936) was 12.6 mm long, and
articulation allows flexion and extension of the the mandible from rictus 12 mm. The basihyale
paraglossum on the basihyale in the midsagittal of hummingbirds is laterally compressed and al
plane. Caudally, the basihyale supports a paired, most completely occupied laterally by m. hypo-
laterally diverging rod, the ceratobranchiale, glossus obliquus, which rotates the paraglossum

F ig. 12. The hyobranchial apparatus of hummingbirds. (A) Hyobranchial elements in black; skull in gray.
Mandibula removed from quadrate and separated at the rostral mandibular fenestra. Semidiagrammatic. (B, C)
Diagrammatic representation of hyobranchial elements in relation to the elastic tube and hyobranchial muscles.
Paraglossum and epibranchiale in solid black; basihyal and ceratobranchiale in gray; open circles are articulations.
Black triangles indicate stable position of base of elastic tube. Arrows show direction of force on hyobranchial
apparatus from muscle contraction. (B) Schematic representation with tongue retracted, showing collapsed elastic
tube in floor of mouth. Intrinsic muscles are represented by continuous lines, and extrinsic muscles by dashed
and dotted lines. With bony elements largely free of the elastic tube, intrinsic muscles could effect flicking of the
tongue. (C) With the tongue fully protracted, the basihyale and ceratobranchiale are enclosed in the expanded
elastic tube, and only the extrinsic muscles could control tongue flicking. Abbreviations: bas. = basihyale, cer. =
ceratobranchiale, elas. tub. = elastic tube, epi. = epibranchiale, m. branchio. = branchiomandibularis muscle, m.
cerat. = ceratoglossus muscle, m. hypogl. obl. = hypoglossus oblique muscle, m. intercer. = interceratohyoideus
muscle, m. stylo. = stylohyoideus muscle, par. = paraglossum, uro. = urohyale.
and tongue upward around the basihyal. When exceptionally it extends forward beyond the cra
the tongue is retracted, its base lies just rostral niofacial hinge, sometimes into the bony nasal
to the larynx and is attached to the compressed, opening. By contrast, the epibranchiale of swifts
elastic tube from the floor of the mouth. The is shorter than the ceratobranchiale. The cerato-
two ceratobranchiales diverge from their articu branchiales are slender and cylindrical, but the
lation with the basihyale and extend caudally epibranchiales are dorsoventrally compressed.
roughly to the jaw articulation. I found that the Although a woodpecker can actively change
ceratobranchiales of a swift and hummingbird of the direction of the tip of its tongue, this capabil
equal body size (indexed by coracoideum length) ity is not present in hummingbirds. In many re
were approximately equal in length. Most vari spects woodpeckers are fundamentally different
able in hummingbird genera is the epibranchiale, from hummingbirds in the structure of the tongue
which always exceeds the ceratobranchiale in and hyobranchiales (Lucas 1891, Scharnke 1931a,
length; commonly it passes around the occiput Bock 1999). The tongue and paraglossales form
and terminates mid-dorsally on the cranium, and a relatively short, stiff unit that can be extruded

far beyond the bill tip, where it can be guided in muscle of even the longest-billed passerine necta-
different directions by the hyobranchial muscles. rivores (e.g., Arachnothera longirostris) originates
Except for protrusion and retraction, the less caudal to the orbits; in most hummingbirds the
protrusable, flexible tip of the hummingbird's origin is farther forward, almost to or sometimes
tongue is not directly guided by motion of the beyond the craniofacial hinge. Although these
paraglossales. two muscles, extrinsic to the hyobranchial appa
ratus, could power the rapid licking motions of
MOBILITY OF THE TONGUE the tongue during nectar eating, another mecha
nism is postulated below.
The hyobranchial apparatus of birds serves as Spirit specimens preserved with variously
a vehicle for movement and stabilization of the protruded tongues have the basihyale and both
tongue, larynx, and floor of the mouth. In most ceratobranchiales variously enclosed within the
birds the larynx is limited to a position within the elastic tube. When fully enclosed and the tongue
pharynx opposite the somewhat elongate open fully protracted, the extended elastic tube occu
ing of the internal nares (choana) as a conduit for pies almost the full length of the bill (illustrated
breathing, and the tongue has limited rostrocaudal by Scharnke 1931a: fig. 2). In this state, the en
movement. Extension of the tongue far beyond the closed ceratobranchiales and the associated
limit of the bill is a capability of long-billed necta- interceratobranchial muscles are pressed together
rivores, and coupling of the larynx and hyobran- and collinear with the basihyale within the tube.
chial apparatus is reduced correspondingly. By During extreme protraction of the hummingbird
manipulation of a cleared and stained specimen tongue, the interceratobranchial muscles prob
(Threnetes leucurus USNM 512702), I confirmed ably draw the ceratobranchiales together as they
that the larynx remained near the base of the enter the elastic tube. I was surprised to note that
elastic tube while the hyobranchial skeleton was in some species, even the rostral portion of the
greatly protracted and the elastic tube greatly ex epibranchiale was enclosed by the elastic tube
tended. Moller (1930) stated that a tracheal muscle during extreme protraction, and that in those
(m. tracheohyoideus) arises from the basihyale in cases the insertion of m. branchiomandibularis
Eulampis holosericeus, but neither Weymouth et al. began farther caudally on the base of the epi-
(1964) nor Zusi and Bentz (1984) found any muscle branchiale. (Examples are spirit specimens of
connecting the trachea or larynx to the hyobran- Heliodoxa leadbeateri [USNM 55623] and Ensifera
chial elements in hummingbirds. ensifera [USNM 505429], in which the rostral por
Specimens, photographs, and personal obser tion of the epibranchiale free of muscle insertion
vations indicate that many hummingbirds can measured 4.9 mm and 22.4 mm, respectively.) All
extend the tongue almost fully beyond the bill intrinsic muscles of the hyobranchiale apparatus
tip (e.g., Grant and Temeles 1992; Schuchmann and part of m. stylohyoideus are enclosed in the
1999:478, 507; Temeles et al. 2002). Such extension elastic tube during full extension of the tongue.
from nearly closed mandibles may serve to clean To reach nectar far beyond the tip of the bill,
the tongue, and the exposed tongue is sometimes hummingbirds might fully protract the tongue
used for display (Davis 1958). Extreme extension as described above, and the lapping rate prob
is accomplished by the paired m. branchioman- ably would decrease. Ewald and Williams (1982)
dibularis, strap-like muscles that originate on the found the licking rate to be inversely proportional
lower jaw and extend back to engulf the epibran- to distance between the bill tip and the sugar
chiales along most or all of their length. Contrac solution. However, frequent, full exposure of the
tion draws the base of the epibranchiale forward, tongue when the bird is not feeding indicates that
and the reduction in muscle length at full con extreme protraction also serves purposes other
traction must roughly equal the length of the bill. than nectar uptake.
Retraction of the tongue is accomplished by m. Here, I propose another mechanism for flick
stylohyoideus, which originates dorsally on the ing of the tongue while feeding on nectar. It is
braincase. This muscle curves around the skull possible that the ceratobranchiales and part of
to insert on the basihyale. Motions of the long, the basihyale usually remain caudal to and free
slender hyobranchial horns are guided along the from the elastic tube, allowing the two bones to be
braincase by their enclosure in a narrow sheath of flexed or extended in both the frontal and sagittal
connective tissue. By contrast, the stylohyoideus planes, and the basihyale to be flexed or extended

against the paraglossum (see Fig. 12). In this con and after young birds leave the nest (Scharnke
figuration, seen in some spirit specimens, the 1931a). Nestlings are fed by regurgitation into
ceratoglossus muscles could cause these flexions their throats by adults, and parental feeding con
simultaneously. Also, extension of the paraglos tinues after fledging for ~3 weeks (Schuchmann
sum on the basihyale by m. hypoglossus obliquus 1999:513). Schuchmann also noted that young
and extension of the basihyale on the ceratobran- learn to feed on flower nectar by watching adults
chials by m. interceratobranchialis could occur. and through trial and error.
I suggest that alternate contraction of these antago The tongue apparently is not involved in the
nistic flexor and extensor muscles (see Zusi and capture of arthropods. However, it was used for
Bentz 1984: fig. 4g), when free from the elastic tube, licking ashes from the soil by a bird standing
would produce rapid flicking of the tongue tip in on the ground, for licking the wall of a house
and out of the bill as long as the tongue and hyo- painted with calcium hydroxide while hovering,
branchiales were not strongly protracted. During and for licking a road surface. In these cases the
tongue flicking, the amount of tongue protrusion birds were probably ingesting calcium-rich com
would be roughly proportional to the length of pounds (Graves 2007, Estades et al. 2008), but
the basihyale and, thus, not highly correlated with whether saliva was used to lubricate the tongue
bill length. This mechanism could be the norm for tip in these instances is unknown.
nectar drinking. Rapid tongue flicking cannot be
observed during normal feeding at flowers, but it ARTHROPOD CAPTURE
is visible at transparent feeders. As proposed by
Ewald and Williams (1982), the amount of tongue Arthropods (insects and spiders) are an essential
extension may be similar (adjusted for body size) in part of the diet of hummingbirds and are found
both short- and long-billed species, the advantage in virtually all examined stomachs (Remsen et
of long bills mainly being access to nectar in long al. 1986, R. L. Zusi unpubl. data). They are ob
corollas. Licking rate and its mechanism would tained by a variety of foraging techniques (Young
remain roughly the same despite differences in 1971, Montgomerie and Redsell 1980, Chavez-
bill length. Ramirez and Dowd 1992, Stiles 1995). Most
prevalent are hover-gleaning from spider webs,
NECTARIVORY leaves, branches, epiphytes, tree buttresses, and
other substrates; probing mosses and lichens on
Detailed discussion of tongue structure and cor branches, while hovering; rapid gleaning between
rections of earlier misrepresentations are found sallying from and returning to a perch; hawking
in Weymouth et al. (1964) and are not repeated (taking prey from midair) by short dashes and
here. The tongue is capable of taking up nectar hovering; and hawking after sallying from a
in its twin, epidermal tips and of transferring it perch (Stiles 1995). Androdon aequatorialis some
to the bill and mouth by lapping; nectar is then times probes into curled leaves or cavities for ar
stripped from the protruding tongue (Paton and thropods (Schuchmann 1999:506). Although the
Collins 1989) by the nearly closed bill tips (Ewald sicklebills (Eutoxeres) may employ hawking, Her
and Williams 1982). However, the traditional as mits specialize in gleaning. The details of captur
sumption of capillarity of the tongue as a method ing and swallowing prey are difficult to observe
of initial nectar uptake has been replaced. Rico- in the field and are recorded only rarely. Lateral
Guevara and Rubega (2011) showed that nectar widening of the rami of the mandible apparently
capture involves unfurling and furling of lamellae is not involved during prey capture when hawk
of the tongue tip that are supported by stiffer rods. ing. Instead, while chasing airborne prey (Mobbs
Furling of the nectar-filled lamella occurs through 1979) or a spider baling out of its web on a strand
Laplace pressure and surface tension forces as the of silk (Stiles 1995), the bill is opened wide and
tip leaves the nectar. As noted above, nectar is then the prey is captured in the gape at the back of the
stripped from the protruding tongue by the nearly mouth. "When a hummer captures an insect in
closed bill tip. These authors also point out that the flight, its forward movement forces the prey so
method of nectar transport within the bill leading far to the rear of the gape that it is readily swal
to swallowing is still unknown. lowed. Should for some reason the insect not be
The lamellae at the tip of the tongue develop taken far enough into the gaping beak, it will be
gradually in the nestling (Lucas 1891, 1897) discarded" (Mobbs 1979, captive birds). The role

of the neck in insect capture, especially regard each represented by a short caudal spike attached
ing rapid head motions to receive prey into the to the caudal margin of the maxillary process
throat, is unknown. of the nasale, in a few specimens (Hemiprocne
When gleaning from spider webs or vegetation, comata USNM 488940; H. mystacea USNM 560827,
hummingbirds take their prey in the tip of the 560828), suggesting absence rather than fusion in
beak, toss it into the air, and fly at it with the bill Apodiformes. No vestige of a lacrimale was evi
agape as when hawking. Alternatively, some cap dent in a nestling of Chlorostilbon swainsonii. The
tive birds may "toss it into the air and then with the ectethmoidale of Aegotheles is poorly developed,
beak agape, fly backwards tilting the head so as to lying entirely medial to the rostral bar of the
enable the prey to fall into the rear of the gape" palatinum. In Hemiprocnidae it is more inflated
(Mobbs 1979:28). Similarly, species of high eleva and extends slightly lateral to the palatinum; that
tions that forage while walking or running on the of Apodidae is similar but larger, reaching later
ground, sometimes hover-assisted, snap at insects ally almost to the jugal arch, and in Trochilidae it
and toss them into the air for capture in the gape extends laterally beyond the jugal arch and sup
with the head tilted backwards (Mobbs 1979). Fly ports it; Figs. 4A, B and 9).
ing insects may be captured also while a bird is Interorbital septum.—In Aegotheles and Hemipro
perched by lunging with the bill widely open. cnidae the interorbital septum (septum interorbitale)
Downward bending of the opened mandible is complete, but in Apodidae it is thin and usually
in several captive individuals of three species of perforated with one or two interorbital fonticuli (fon-
Trochiline hummingbirds was filmed by Yanega ticulus interorbitalis). Shufeldt (1885) regarded the
and Rubega (2004). When the bill opened during interorbital septum of hummingbirds as partially
the act of catching an insect in aerial pursuit, the displaced by the orbitocranial fonticulus (fonticulus
intermediate parts of the two rami were closely orbitocranialis), but I found the latter to be restricted
appressed and apparently bent downward. When to the braincase, and the interorbital septum
the insect passed between the opened mandibles (Fig. 4A) to be complete in all hummingbirds.
and into the wide, posterior mouth opening, the Muscle impressions.—Hummingbirds have long
bill snapped shut. In the absence of an anatomi hyoid horns (cornu branchiale), consisting mainly
cally defined, posterior, intramandibular bending of the epibranchales, that lie in a depression lat
zone, no mechanical explanation for ventral bow eral to the cerebellar prominence (prominentia
ing of the mandibular rami was proposed. cerebellaris) and rostrally along the mid-dorsum
Rhamphothecal serrations along the tomia of the of the cranium (see below). Deep to the epi-
upper mandible or both mandibles occur in many branchiale is m. stylohyoideus, which usually
species of hummingbird (Ornelas 1994). With re originates in a shallow depression caudal to the
spect to Androdon, Schuchmann (1992) thought the craniofacial hinge (Fig. 4B). Long epibranchiales
serrations were important in the capture of spiders and the depression for m. stylohyoideus are lack
and nonflying insects. Detailed descriptions of uses ing in all outgroups.
of the bill and of the kinds and extent of serrations In both Apodidae and Trochilidae, a prominent
on the mandibles, their ontogeny, and intraspecific sulcus on the dorsolateral cranium is occupied by
variation throughout hummingbirds are incom m. cucullaris capitis (Fig. 8 B). The sulcus in hum
plete or lacking. The anatomy of serrations is best mingbirds begins caudolaterally and passes ros-
studied in live, freshly dead, or alcohol specimens tromedially along the margin of the orbit (orbita).
because curling of the rhamphothecae in dried Although it channels the muscle, insertion occurs
museum skins may prevent observation. only in its rostral portion.
Vascular tube.—In hummingbirds the rostral
C ranium semicircular canal (canalis semicircularis ante
rior) is accompanied along a portion of its dorsal
Ectethmoidale and Lacrimale.—The ectethmoidale and caudal surface by a previously undescribed
extends laterally from the median mesethmo- ossified vascular tube (tuba vascularis) that is ab
idale. Shufeldt (1885) thought that a lacrimale sent from all outgroups. Part of the tube is visible
was fused with the ectethmoidale in humming through the thin bone of the occiput in skeletons
birds, but Parker (1879) and Cracraft (1968) con and in cleared and stained specimens of hum
sidered it absent. I found vestiges of the lacrimale, mingbirds. The content of the tube is unknown.

The F light M echanism and the secondary remiges are both of reduced
aerodynamic importance. Hummingbirds have
Apodiformes were not included in Sy's (1936) developed some of these specializations further
excellent description and analysis of the avian than other Apodiformes and evolved new struc
flight mechanism covering osteology, arthrology, tures related to hovering, as discussed below.
and myology. Hummingbirds and swifts share
many qualitative and proportional attributes of Sternum
the flight apparatus correlated with stiff-winged
flight and a powered upstroke of the wing The sternum of hummingbirds (Fig. 13) shares
(Stolpe and Zimmer 1939, Savile 1950, Cohn several properties with that of swifts: the sternal
1968, Warrick et al. 2005). These include rela body (corpus sterni) is long in relation to overall
tively long hand (manus) and distal primaries, body size, and the carina is deep in relation to
and relatively short humerus and forearm that sternal length (Fig. 13A); the caudal border of the
are steadily flexed at the elbow and extended at sternal corpus is entire and markedly broader
the wrist. The correspondingly small patagium between the lateral angles (angulus lateralis)
F ig . 13. The sternum of hummingbirds. (A) Left lateral view. (B) Dorsal view. (C) Rostral view. All drawings
are to same scale. Rostral narrowing of the sternal body and great depth of the carina in relation to length of
the sternal body reflect extreme enlargement of the major breast muscles. Abbreviations: car. ap. = carinal apex,
car. lim. = dorsal limit of carina, car. pil. = carinal pillar, cran. pr. = craniolateral process, cor. fac. = coracoidal
facet of sternum, int.-m. lin. = intermuscular line, lat. ang . = lateral angle, med. rid. = medial ridge, st. art. pr. =
sternocostal articular process, st. body = sternal body.

F ig. 14. Muscles of the sternum in modern hummingbirds and E u ro tro c h ilu s; coracoid of a swift and hum
mingbird; and shoulder girdle of a hummingbird. (A) Lateral view of hummingbird sternum with left pectoralis
muscle removed (above) and left pectoralis plus supracoracoideus muscles removed (below). (B) Carina of the
Oligocene fossil, E u r o tro c h ilu s, in lateral view. (A, B) Oblique hatching indicates origin of m. supracoracoideus on
the carina. Compared with modern hummingbirds, E u ro tro c h ilu s exhibits reduced depth of the carina in relation
to sternal body length, and difference in the ventral intermuscular line, both indicating reduced area of origin of
m. supracoracoideus (oblique hatching). This configuration is similar to Apodidae. (C) Coracoids of a swift (left)
and hummingbird (right); dorsal views, drawn to same length. The hummingbird has a reduced lateral process,
larger foramen of the supracoracoidal nerve, and a coracoidal bar. (D) Articulated right clavicle, coracoideum,
and scapula of a hummingbird; dorsal view. Both the clavicle and scapula are supported by the coracoidal bar.
Abbreviations: acr. pr. = acrocoracoidal process, acro. pr. = acromion process of clavicle, car. lim. = dorsal limit of
carina, car. pil. = carinal pillar, cla. = clavicle, cor. = coracoideum, cor. bar = coracoidal bar, cor. can. = coracoidal
canal, fur. = furcula, glen. pr. = glenoid process of scapula, int. m. lin. = intermuscular line, lat. pr. = lateral prcess
of coracoideum, m. cor. caud. = coracobrachialis caudalis muscle, m. pect. = pectoralis muscle, m. supracor. =
supracoracoideus muscle, pn. cav. = pneumatic cavity, pro. pr. = procoracoid process, sca. acro. = scapular acro
mion, sca. sha. = scapular shaft, SCC memb. = sternocoracoclavicular membrane, st. body = sternal body, st. lig. =
sternoclavicular ligament, sup. n. for. = supracoracoidal nerve foramen.
than at the rostral border (Fig. 13B); the cora in swifts are irregularly perforated. The carina is
coidal facets (prominentia articularis) are oval strengthened anteriorly by a thickening or pillar
and convex, and nearly meet at the midline (Fig. (pila carina) (Figs. 13A, C and 14A). Although
13C); and the external spine (spina externa ros the external spine is absent in apodiforms, short,
tri) is lacking. Surfaces of the body and carina paired processes are present in Aegotheles cris-
are irregular (resembling hammered metal) and tatus, and the spine is replaced in apodiforms

by a raised, medial ridge (eminentia media- portion of the sternal body. Buri (1900), Marshall
lis) between the coracoidal facets that receives (1906), and Cohn (1968) also showed that m. su-
the sternoprocoracoidal ligament (ligamentum pracoracoideus of hummingbirds arises from a
sternoprocoracoideum). larger portion of the sternal body than it does in
On the sternum, the largest pectoral muscles swifts. Thus, osteological features of the sternum
are m. pectoralis and m. supracoracoideus (Buri that shed light on the size of the supracoracoideus
1900, Marshall 1906, Hartman 1961, Cohn 1968, muscles may be preserved in fossils. In all apodi-
Karhu 2001). In hummingbirds, the pectoralis forms, m. supracoracoideus also originates from
muscle originates from the peripheral portions of the shaft of the furcula (scapus claviculae) and the
the sternal body and keel, and also from the keel SCC membrane (Fig. 14).
ventral to the intermuscular line, from the furcula, The sternocoracoideus muscle of most birds in
and from the sternocoracoclavicular membrane terconnects the medial surface of the craniolateral
(membrana sternocoracoclavicularis, or SCC process of the sternum and the lateral process
membrane). Aponeuroses from the intermuscular of the coracoid (processus lateralis coracoidei).
lines and ventral margin of the sternal carina are In hummingbirds the craniolateral process is
part of the origin. In hummingbirds, the aponeu smaller than in outgroups and m. sternocoracoi-
rosis is best developed from the caudal part of deus is lacking. Nevertheless, m. coracobrachialis
the ventral carinal margin and the caudal margin caudalis, originating from the lateral surface of
of the sternal body, where the bony sternum is the craniolateral process and adjacent portion of
largely occupied by the supracoracoidal muscle. the sternal body, is well developed in humming
Although the pectoralis muscle overlaps the ven birds and represents the third important flight
tral portion of the rib cage laterally, the muscle is muscle originating from the sternum.
completely independent from the ribs. Sternocos
tal articular processes (processus sternocostalis C oracoideum , C lavicula , and S capula
articularis) for sternal ribs occur along the lateral
margin (margo costalis) of the sternal body and The coracoideum of hummingbirds differs from
sometimes on the caudal edge of the craniolateral that of other Apodiformes in possession of an ossi
process (processus craniolateralis). fied coracoidal bar (pila coracoidei) that seamlessly
Size of the supracoracoideus muscle is indicated interconnects the procoracoidal process (processus
in part by a carinal intermuscular line, which in procoracoideus) and base of the acrocoracoidal pro
swifts extends the full length of the carina (Sclater cess (processus acrocoracoideus) (Fig. 14B). It en
1865), and a corresponding intermuscular line of closes the coracoidal canal (canalis coracoidei) and
ten is present in Hemiprocnidae. By contrast, the replaces the acrocoraco-procoracoidal ligament
homologous intermuscular line of hummingbirds (ligamentum acrocoraco-procoracoideum) of other
intersects the carinal margin midventrally (Fig. Apodiformes (in one specimen of A. cristatus
14). Swifts and crested swifts also exhibit inter [USNM 620228] the latter ligament was ossified).
muscular lines that are oriented rostrolaterally on In addition, hummingbirds have a large pneu
the ventral surfaces of the sternal body. The lines matic cavity (cavitas pneumaticum) on the dor
are well developed in hummingbirds along the sal surface of the coracoid, just proximal to the
lateral margins of the sternal body (Figs. 13A and coracoidal canal (Fig. 14B). The pneumatic cavity,
14A). These differences reflect a more complete which approximately equals the coracoidal canal in
occupation of the carina and almost complete length, receives the supracoracoidal nerve (nervus
occupancy of the sternal body by m. supracora- supracoracoideus) and probably a portion of the
coideus in hummingbirds. I confirmed that the interclavicular air sac. Other apomorphic features
intermuscular lines circumscribe the limits of the of the coracoid in hummingbirds represent terminal
muscle in hummingbirds by dissection of G. hirsu- stages of morphoclines within Apodiformes: (1) the
tus, in which m. supracoracoideus occupies most lateral process is well developed in Hemiprocnidae,
of the carinal surface except the rosroventral por reduced in Apodidae, and vestigial in Trochilidae;
tion, and the entire ventral surface of the sternal (2 ) the sternal articular facet (facies articularis ster-
body except its caudolateral extremity; by contrast, nalis) is ovoid medially, tapering to a narrow trough
in Collocalia esculenta the muscle narrows caudally on the lateral process in Hemiprocnidae, broadly
and is absent from the ventral and caudal por ovoid with a small extension onto the lateral pro
tions of the carina and from a large, caudolateral cess in Apodidae, and broadly ovoid with no

extension or involvement with the lateral process in the clavicle has a tight juncture with the coracoid
Trochiidae; and (3) the supracoracoidal nerve fora in hummingbirds and provides firm support for
men is small on the ventral surface of the coracoi- the sternocoracoclavicular membrane. The scapu
deum in Hemiprocnidae, larger in Apodidae, and lar acromion (acromion) also articulates with the
markedly larger in Trochilidae. (Dissection of single base of the coracoidal bar, where, in addition to its
specimens of G. hirsutus and C. esculenta, species usual articulation across the caudal surface of the
of similar body weight, revealed that Glaucis has a coracoideum, it abuts the acromion process of the
thick, branching nerve, whereas that of Collocalia is clavicle (Fig. 14C).
a single, thin strand.) The sterno-acrocoracoidal lig
ament (ligamentum sterno-acrocoracoideum) con Shoulder J oint
nects the medial ridge of the sternum (1 ) with the
acrocoracoidal process and medial and dorsal sur The shoulder joint (articulatio omalis) is a synovial
faces of the coracoideum in Hemiprocnidae; (2) with articulation between the head of the humerus and
the acrocoracoidal process, procoracoidal process, the glenoid cavity (cavitas glenoidalis), the latter
and part of the dorsal surface of the coracoideum in consisting principally of the ligaments supported by
Apodidae; and (3) exclusively with the dorsal sur the coracoideum and scapula (Baumel and Raikow
face of the coracoideum medial to the pneumatic 1993). The glenoid cavity is somewhat malleable,
cavity in Trochilidae. As one might infer from these conforming to, but partially restricting, movements
morphological differences, manipulation of cleared of the humeral head (caput humeri) during flight
and stained specimens of a swift (Chaetura pelagica) (Sy 1936). The glenoid cavity and its relation to the
and several species of hummingbird revealed that humerus in hummingbirds are illustrated by Stolpe
the sterno-acrocoracoidal ligament restricted ven and Zimmer (1939) and Karhu (2001).
tral, lateral, and dorsal displacement of the cranial
portion of the coracoideum in relation to the ster H umerus
nal articulation in the swift, and ventral and lateral
displacement in the hummingbird. From the nearly In most avian orders the humerus is an elongate
adjacent sternal articulations, the coracoids of hum bone with well-defined features of its proximal
mingbirds diverge anterolaterally such that the portion that are associated with the shoulder
shoulder joints are positioned laterally to the same joint and with insertions of muscles powering
degree as the caudolateral angles of the sternum. motions of the upper arm (brachium; Fig. 15A).
The claviculae are fused medially to form a slen The morphology of its distal end is associated
der furcula that is U-shaped in rostral view and C- with the elbow articulations (juncturae cubiti)
shaped in left lateral view, and the space between and with muscles effecting motions of the fore
the clavicla and coracoideum is occupied by the arm (antibrachium) and hand, but the elongate
SCC membrane. The clavicular symphysis (apoph shaft is nearly featureless. Aegotheles has a typi
ysis furculae) of hummingbirds and swifts has no cal avian shaft, but that of Hemiprocne is relatively
close contact with the sternum, but the furcula is shortened. By contrast, hummingbirds and swifts
stabilized to the apex of the sternal carina by a ster are extreme among birds in the extent to which
noclavicular ligament (Fig. 14A). In apodiforms the shaft has been shortened. As a result, in both
with a shallower carina, the clavicular symphysis taxa, several of the muscles and osteological
is near the carinal apex. The furcula in Aegothe- landmarks usually associated with the distal por
les has a blunt, plate-like acromial region (regio tion of the humerus intermingle with those of the
acromialis), whereas that of apodiforms is slender proximal portion (Fig. 15B). Most notably, swifts
and extends beyond the acrocoracoidal tubercle and hummingbirds exhibit a well-developed,
(tuberculum acrocoracoidale). In Hemiprocnidae proximately situated process of m. extensor
and Apodidae the clavicular acromion process metacarpi radialis (processus extensor metacarpi
(processus acromialis) is straight, articulating only radialis; hereafter "EMR process"); this process
with the acrocoracoid process (processus acrocora- is synonymous with the "processus supracondy-
coidalis) of the coracoid. By contrast, the clavicu laris dorsalis" of Lowe (1939), Cohn (1968), and
lar acromion of hummingbirds is down-curved, Zusi and Bentz (1982). Only in hummingbirds
articulating not only with the acrocoracoid but does a crest (crista) interconnect the EMR process
also with the coracoidal bar (Fig. 14C). As a result, with the angle of the tensor propatagialis muscle

FOREARM
HAND (ANTE BRACHIUM)
(MANUS) UPPER ARM
(BRACHIUM)
p a ta g iu r r v /^
WRIST '
(CARPUS)
ELBOW >»" humerus

(CUBITUS)
hum. head
hum.head
hum. shaft
EMR pr.
HEMIPROCNIDAE APODIDAE TROCHILIDAE
F ig. 15. Configuration of the wing skeleton of a hummingbird as in stiff-winged flight, and comparison of
the humerus in Apodiformes. (A) Approximate positions of skeletal elements of a hummingbird's left wing in
dorsal view, as in directional or hovering flight (semidiagrammatic). The brachium is caudally adducted toward
the body, the antibrachium flexed on the brachium, and the manus extended on the antibrachium. The manus
supports the primary remiges and is of greatest aerodynamic importance. The triangle formed by the brachium,
antebrachium, and patagium encloses the bulk of the wing muscles that power the manus. (B) Caudal views
of the left humeri in Apodiformes, drawn to similar widths of the distal extremities. Length of the humeral
shaft (between the EMR process and deltopectoral crest) is reduced almost to zero in Apodidae and Trochilidae.
Abbreviations: cap. tub. = capital tuberculum, delt. cr. = deltopectoral crest, EMR pr. = process of extensor meta
carpi radius muscle, hum. head = humeral head, hum. shaft = humeral shaft, pro. tub. = pronator tubercle, TPB
ang. = angle of tensor propatagialis brevis muscle, ven. pr. = ventral process of humerus.
(TPB angle). In Hemiprocnidae, Apodidae, and sulcus, and a weaker portion is confined to its
Trochilidae the EMR process has shifted proxi more dorsal portion. In hummingbirds the sulcus
mally on the humerus in relation to the width of is reduced to two scars (Livezey and Zusi 2006:
the distal portion of the humerus (Fig. 15B). fig. 21F), the ventral one associated with the main
The humeral head of Apodiformes, as in many portion of the ligament, and the shallower dor
other birds, displays a transverse sulcus (sulcus sal scar with the weaker part. In all apodiforms,
transversus) that receives the acrocoracohumeral the weaker part of the ligament attaches near the
ligament (ligamentum acrocoracohumerale). The long axis of rotation of the humeral shaft (scapus
two-parted ligament spans the acrocoracoidal humeri), and probably serves to maintain the
process of the coracoid and the cranial surface humerus within the glenoid socket. The stronger
of the humeral head (Sy 1936). Except for hum part of the ligament attaches ventral to the axis
mingbirds, the sulcus of Apodiformes is long and of rotation and limits axial pronation of the hu
well defined, extending ventrally from the dorsal merus on the downstroke of the wing (Sy 1936).
portion of the head onto the ventral process. The In both swifts and hummingbirds the tendon of
main part of the ligament occupies most of the m. supracoracoideus inserts on the ventral surface

of the deltopectoral crest (crista deltopectoralis) di Zimmer 1939, R. L. Zusi unpubl. data). I found a
rectly opposite the dorsal insertion of m. pectoralis less developed capital tuberculum in one speci
(Stolpe and Zimmer 1939, Karhu 1992). I have no men of Hemiprocne comata (YPM 7039). As noted by
ticed that symmetrical juxtaposition of insertions of Karhu (2001), a small capital tuberculum is found
these two major, antagonistic flight muscles is rare also in some galliforms and tinamous, probably
in birds, occurring elsewhere in penguins (Sphenis- associated with humeral supination during take
cidae) and the Great Auk (Pinguinus impennis). That off. A shallow sulcus between the capital tubercu
configuration (Fig. 16) appears to equalize the me lum and the humeral head channels the tendon of
chanical advantage of the two muscles in relation m. supracoracoideus toward its insertion on the
to a strong, powered upstroke of the wings and to humerus in hummingbirds.
the axial rotation of the humerus. The ventral tubercle (tuberculum ventrale) of
A well-developed capital tuberculum (tubercu the humerus found in most birds has expanded
lum capitis) on the caudal surface of the humerus to become a curved process in Apodiformes
extends the articular surface of the humeral head (Figs. 15 and 16), and for Apodiformes I name it
uniquely distad in hummingbirds (Fig. 16). In "ventral process" (processus ventralis humeri).
modern hummingbirds the dorsal portion of It is longer in Apodidae than in Hemiprocne and
this tuberculum is semiglobose, providing an Aegotheles and longest in hummingbirds (Karhu
articulation with the glenoid process of the scapula 1992: fig. 6 ). Insertions of muscles from the scap
(processus glenoidalis scapulae) during adduc ula and coracoid are concentrated distally on the
tion and supination of the humerus (Stolpe and ventral process in hummingbirds. For example,
m. scapulohumeralis caudalis inserts on the bi
cipital crest (crista bicipitalis) in Hemiprocnidae
and Apodidae, but on the caudoventral extremity
of the ventral process in Trochilidae (Cohn 1968,
Zusi and Bentz 1984, Karhu 1992).
I noted but did not measure a progressive
increase in the depth and breadth of the olecra
non fossa (fossa olecrani; Fig. 15) that houses the
insertion tendon of m. triceps brachii within apo-
diform families (Hemiprocnidae, Apodidae, and
Trochilidae). This extensor muscle of the forearm
acts with forearm flexors to maintain flexion of
the elbow during stiff-winged flight and, espe
cially, during hovering. The angled tendon at the
flexed elbow is strengthened by an enlarged sesa
moid, as described by Stolpe and Zimmer (1939).
The distal portion of the humeral shaft in swifts
F ig. 16. Insertions of major flight muscles on the
and hummingbirds is exceptionally wide (dor-
humerus of hummingbirds. Left humerus; dorsal
soventrally), and the ventral condyle (condylus
view (left); caudal view (right). The dotted line shows
the general area of insertion of the pectoralis muscle ventralis) and dorsal condyle (condylus dorsais)
on the cranial side of the deltopectoral crest; hatch are enlarged (Karhu 1992). The dorsal, or radial,
ing represents insertion of supracoracoideus muscle. condyle slopes distomedially and the ventral, or
The two insertions are roughly opposite on the del ulnar, condyle curves caudomedially to a greater
topectoral crest in hummingbirds and swifts, equaliz degree in hummingbirds than in swifts—both fea
ing the mechanical advantage for axial rotation of the tures enhancing the ability to rotate the ulna about
humerus during upward (m. supracoracoideus) and its long axis and supporting the radius during su
downward (m. pectoralis) phases of the wing stroke.
pination of the hand (Stolpe and Zimmer 1939).
Abbreviations: bic. cr. = bicipital crest, cap. tub. =
capital tuberculum, cr. = crest, delt. cr. = deltopectoral
R adius and U lna
crest, dor. cond. = dorsal condyle, EMR pr. = process
of extensor metacarpi radialis muscle, hum. head =
humeral head, pro. tub. = pronator tuberculum, TPB Hummingbirds differ from outgroups in having
angle = angle of tensor propatagialis brevis muscle, a stout radius that bows away from the ulna (Fig.
ven. cond. = ventral condyle, ven. pr. = ventral process. 17), providing space and increased leverage for

F ig. 17. Wing elements of swifts and hummingbirds. (A) Articulated elements of hummingbird wing (left
wing, dorsal view), for orientation of B-D. (B) Proximal end of right ulna in cranial view; C h a etu r a (left), E u la m p is
(right). The notched ventral cotyla is thought to permit axial rotation of the ulna in hummingbirds. (C) Left
carpometacarpus in dorsal view; C y p s elo id e s (left), P a ta g o n a (right); alular digit not shown. Dotted lines indicate
the courses of insertion tendons of the flexor digitorum profundus muscle; hummingbirds lack the alular branch
tendon. (D) Left wrist, showing carpals and ligaments in the extended wing of C o llo c a lia e s c u len ta (left) and
C o elig en a c o e lig e n a (right); ventral views (upper) and dorsal views (lower). In swifts, but not hummingbirds, the
long and short arms of the ulnare clasp the carpal trochlea of the carpometacarpus in the extended manus, limit
ing supination of the carpometacarpus. Abbreviations: alu. br. = alular branch tendon, alu. dig. = alular digit,
car.-met . = carpometacarpale, car. tro. = carpal trochlea, c.-t. pad = connective tissue pad, den. pr. = dentiform
process, ext. pr. = extensor process, hum. = humerus, int.-met. pr. = intermetacarpal process, int.-met. spa. =
intermetacarpal space, lon. arm = long arm of ulnare, mag. dig. = major digit, maj. met. = major metacarpale,
min. dig. = minor digit, min. met. = minor metacarale, ole. = olecranon, rad. = radius, ses. = sesamoid, sh. arm =
short arm of ulnare, uln. = ulna, ven. cot. = ventral cotyla.

hypertrophied pronator and supinator muscles From dorsal or ventral view, the carpometa-
(Karhu 1999) and for an enlarged extensor of the carpus of hummingbirds displays a proximally
major digit (M. extensor longus digiti majoris; truncate contour of the cranial part of the carpal
Cohn 1968, Zusi and Bentz 1984). trochlea (trochlea carpalis) (Fig. 17C). This cam
Mayr (2005) indicated that an elongate, nar like form may help stabilize the carpometacarpus
row, ulnar olecranon in hummingbirds (Fig. 17A) while in the extended position.
distinguishs them from swifts; however, I found As in other birds, the apodiforms have two
this character to be variable in both humming free carpales. The radiale is essentially a distal
birds and swifts. He also described a deep fossa extension of the radius that articulates distally
on the caudal surface of the ulna (Mayr 2007:109) with the carpometacarpus, whereas the ulnare
as characteristic of "Argornis and crown-group is associated with the carpal trochlea of the car-
Trochilidae." Karhu (1999) noted that the ven- pometacarpus. Vazquez (1992) described the
troproximal edge of the ventral cotyla of the structure and interactions of bones of the wrist
ulna (cotyla ventralis ulnae) of hummingbirds is and contended that flighted birds possessed me
somewhat eroded (Fig. 17B) whereas that of other chanical restrictions on pronation and supina
apodiforms is complete. He thought that the ven tion of the wrist in the extended wing, related in
tral condyle of the humerus in hummingbirds part to channeling of carpometacarpal rotation
could slide caudoventrally in relation to the ulna by the ulnare. He noted that only hummingbirds
during supination of the forearm, and he claimed possessed a significant deviation in this aspect
that the more prominent ventroproximal edge of of the wrist, but he did not describe the differ
the ventral cotyla in Apodidae resisted supina ence or discuss the functional consequences for
tion of the elbow joint in the spread wing. hummingbirds.
The long (crus longum) and short (crus breve)
C arpales and C arpometacarpus arms of the ulnare in swifts (and most birds)
embrace the caudal rim of the caudal part of the
The carpometacarpus of hummingbirds differs carpal trochlea in the extended wing (Fig. 17D)
from that of outgroups in its possession of an in and limit pronation and supination of the car-
termetacarpal process (processus intermetacarpa pometacarpus as described by Vazquez (1992).
lis), the insertion point of m. extensor metacarpi The metacarpal incisure of the ulnare of hum
ulnaris (Fig. 17B). In outgroups, the tendon of in mingbirds is obtusely angled and poorly defined
sertion of m. extensor digitorum communis (EDC) because its dorsal arm is extremely short. In ad
includes a branch to the alular digit proximal to dition, the caudal part of the carpal trochlea is
the intermetacarpal space (spatium intermetacar somewhat reduced (Fig. 17D). As a result, the
pale). The main tendon of EDC abruptly changes ulnare does not restrict supination of the carpo-
direction distal to the branch and lies within a metacarpus of hummingbirds in the extended
groove on the dorsal surface of the major metacar wing during the upstroke, and pronation on the
pale (metacarpale majus). Hummingbirds lack the downstroke is less strongly restricted than that
branch tendon to the reduced, largely immobile described for most birds by Vazquez (1992).
alular digit, and the tendon of EDC changes direc Cohn (1968) found that the wrist in swifts
tion more gradually distal to the intermetacarpal displayed strong ventral ligaments that limit su
space to follow a groove in the major metacarpal pination of the extended hand on the upstroke.
(Fig. 17B). Ossified connective tissue sometimes These ligaments are superficial on the ventral
encloses part of the groove as a tunnel (see also side of the wrist, fanning out from an attachment
Cohn 1968). Unlike in outgroups, the distal end on the caudodistal portion of the radius to multi
of the minor metacarpale (metacarpale minus) of ple attachments on the ventroproximal portion of
hummingbirds extends beyond that of the major the carpometacarpus (Fig. 18). I found that these
metacarpal. Among apodiforms, only humming ligaments would support the wrist against dorsal
birds have a dentiform process (protuberantia forces on the hand during wing strokes, and that
metacarpalis) on the cranial margin of the major the cranial portion of the ligamental fan would
metacarpal. It enlarges the area of origin of m. specifically restrict supination of the hand in the
abductor digiti majoris—an extensor of the major extended wing. These ligaments are not present
digit (digitus majoris). in hummingbirds.

The basal phalanx of the major digit is broader

in swifts and hummingbirds than in crested
swifts and Aegotheles, providing greater support
for the distal primaries (Sy 1936). In humming
birds the alular digit is small and bound to the
cranial surface of the carpometacarpus.
S esamoids of the Tail
The rectricial bulb (bulbus rectricium) is a bilat

eral complex of muscle and connective tissue that
supports the rectrices and permits coordinated or
partially autonomous motions of the rectrices and
coverts on either side of the pygostyle (Zusi and
Bentz 1984, Zusi and Gill 2009). Here, I highlight a
bilaterally paired oval bone unique to humming
birds within Apodiformes, noted also by Cohn
(1968) and Richardson (1972). The bone is a flat,
oval-shaped sesamoid embedded in the caudola-
teral portion of the expanded, cruciate aponeurosis
of insertion of m. depressor caudae. The sesamoid
supports individual tendons of that muscle that
angle abruptly upward to the follicles of the four
outer pairs of rectrices. In addition, the tendon of
m. caudofemoralis is anchored on the oval bone's
caudolateral margin before angling toward the
F ig. 18. Comparison of the wrist and superficial follicle of the lateral rectrix (Zusi and Bentz 1984,
ligaments in a hummingbird and swift. Ventral views
Zusi and Gill 2009). Like many sesamoids, it stabi
of left wrist of a hummingbird (above) and a swift
lizes a point of abrupt directional change in a ten
(below). Swifts exhibit superficial ligaments of the
wrist between the radius and carpometacarpus that don (in this case, five paired tendons). All of these
limit axial supination of the carpometacarpus and, tendons transmit forces that depress the rectrices
thus, of the entire hand. Hummingbirds lack these and rectricial bulbs. Repeated, rapid depression of
ligaments, allowing supination of the hand during the tail is common in hummingbirds when chang
upstroke of the wing. Abbreviations: alu. dig. = alular ing position while hovering at flowers.
digit, car.-met. = carpometacarpus, EMR ten. = tendon
of extensor metacarpi radialis muscle, ext. pr. = exten s t if f -w in g e d f l ig h t
sor process, hum.-uln. b. = humeroulnar band, rad. =
radius, sup. lig. = superficial ligaments.
From morphological evidence, Lorenz (1933) pro
posed that hummingbirds and swifts used a stiff
D igits winged mode of flight that included a strongly
powered upstroke (Stolpe and Zimmer 1939, Sav-
The major digit of hummingbirds (Fig. 17A), ile 1950, Cohn 1968). Observational data on wing
which supports the three outer primary feathers, kinematics of swifts and hummingbirds in free,
is the longest in proportion to wing length among rapid, forward flight are rare, but larger species
Apodiformes. According to Stolpe and Zimmer have lower wingbeat rates in both families, and
(1939) and Cohn (1968), axial rotation of the ma those of large swifts are amenable to direct ob
jor digit is facilitated by a transversely flattened servation of details. Cohn (1968:70-71) watched
articular surfaces of both the carpometacarpus the White-naped Swift (Streptoprocne semicollaris;
and major digit. The enlarged m. extensor longus ~175 g), at close range:
digiti majoris in hummingbirds probably effects
supination of the major digit, whereas the smaller In rapid forward flight C . sem ico lla ris moves
muscle in other apodiforms may serve more as a the wing from fully extended (up) to fully
damper on pronation from air pressure. flexed (down) with no perceptible folding of

the wrist.... In cruising [slower] flight the hand in which large diameter of the stout shaft pro
of the large swifts goes through the same row vides greater leverage for muscles that effect
ing movements so common in other large birds. axial rotation; (5) proximal shift of humeral pro
The hand is extended for the downstroke and cesses associated with uniquely enlarged exten
partially folded for the u p stro k e.. That large
sor muscles of the hand (Cohn 1968, Karhu 1999);
swifts fly in this manner makes it probable that
(6 ) elongate ventral process of the humerus, again
smaller swifts also move the hand in the same
way during relatively slow forward flight. Only providing greater leverage for muscles of axial
in ra p id flig h t or during sharp turns would the rotation and retraction of the humerus; (7) inser
wing move as a unit. tion of m. supracoracoideus opposite that of m.
pectoralis, equalizing the leverage for supination
The wing is "stiff" only in relation to mainte and pronation of the humerus by the two largest
nance of flexure of the antebrachium against the flight muscles; (8 ) widening of the articular sur
brachium, and extension of manus against ante- faces of the humerus and forearm in swifts and
brachium by muscle action during the full wing hummingbirds, accommodating an increased
stroke. In addition, dorsoventral flexion of the load in the elbow joint (Karhu 1992); (9) enlarged
manus on the antebrachium is restricted. How sternum that supports uniquely enlarged pecto-
ever, the wing is "mobile" through axial rotation ralis and supracoracoideus muscles (Buri 1900,
(supination and pronation) of the humerus, ulna, Greenewalt 1962); (10) stout coracoid with oval
and manus—especially in hummingbirds. High articular facets on the sternum that support the
speed photography of rapid flight in a wind tunnel shoulder against multidirectional forces; and
confirmed these propositions in a hummingbird ( 11 ) humeral head of swifts and hummingbirds
(Tobalske et al. 2007) and a swift (Henningsson angled caudally, apparently increasing support
et al. 2008). Although both the hummingbird (Se- for the humerus in the glenoid socket when the
lasphorus rufus) and the swift (Apus apus) flexed humerus is adducted—the normal position in
the wrist slightly during the upstroke, the wing stiff-winged flight—and during strong supina
remained essentially rigid. Nevertheless, the tion (Stolpe and Zimmer 1939, Karhu 1992). Axial
"stiff" wings of S. rufus exhibited slight pertur rotation of the humerus in the stiff-winged posi
bations of various parameters during flight in a tion contributes to the aerodynamic motion of the
wind tunnel (Tobalske et al. 2007). Throughout hand and primaries during the wing stroke.
stiff-winged flight, the flexed antebrachium con How does free, forward flight of humming
solidates the mass of enlarged forearm muscles birds differ from that of swifts? Aerial feeding by
near the shoulder joint; it also decreases the in swifts entails abrupt changes in direction, speed,
ertial moment of the moving wing and probably and wingbeat rate. Despite the ability to attain
favors intensive flapping flight (Karhu 1992). high speeds, the long, narrow wings of swifts also
Most of the aerodynamic role is transferred to favor gliding (Bruderer and Weitnauer 1992). Al
the much-enlarged manus and primary feathers. though bounding flight occurs in hummingbirds,
However, flexion of the elbow is not a permanent gliding and soaring are more pronounced in the
condition in hummingbirds; during one form of larger species. Wingbeat rates of hummingbirds
wing stretching, the elbow is extended and the exceed those of similar-sized swifts (Geenewalt
patagium elongated well beyond the position 1962), and they are roughly constant for each spe
maintained during flight (WNET-Nature 2010). cies whether in normal forward flight or hover
Cohn (1968) presented preliminary experi ing. Wingbeat rate of hummingbirds is inversely
mental evidence for stiff-winged flight and a correlated with wing length (Stresemann and
powered upstroke in swifts. Features common to Zimmer 1932; Greenewalt 1962, 1975). High wing-
swifts and hummingbirds, and probably associ beat rates of hummingbirds enhance stability by
ated with stiff-winged flight accompanied by a passive rotational damping (Hedrick et al. 2009).
strongly powered upstroke, include (1 ) extreme
reduction in humeral length (Böker 1927); (2) HOVERING
short radius and ulna (Böker 1927) with fewer,
shorter secondaries (9-10 in swifts, 6 or 7 in hum Asymmetrical hovering.— This weak form of hov
mingbirds); (3) long hand, in proportion to wing ering involves an extended wing on the down-
length, supporting long primaries; (4) humerus stroke and folding of the wing on the upstroke

(Norberg 1990). It is used occasionally during enough, and although hummingbirds do not
short periods of hovering by many species of exhibit the elegant aerodynamic symmetry of in
various orders that lack obvious, anatomical spe sects, natural selection rewards "good enough"
as richly as it does our aesthetic ideals. (Warrick
cializations for hovering. Even in swifts, hover
et al. 2005:1096)
ing is neither strong nor sustained. Manchi and
Sankaran (2010) described a foraging maneuver
(flutter) in swiftlets (Aerodramus fuciphagus and While the manus is continuously extended, the
Collocalia esculenta) as "a hover performed with wing tips move constantly in a figure-8 pattern
a rapid wing beat and a pause in flight" (p. 260). with rotational circulation involving pronation at
George (1971:178) saw swifts gleaning insects the upper end of the upstroke and supination at
from outermost branches of deciduous forest. the lower end of the downstroke (Stolpe and Zim
Sometimes a bird would "bank sharply up and mer 1939, Warrick et al. 2009). Lift during hover
flutter briefly" at foliage, or it plummeted more- ing (S. rufus and probably all hummingbirds) is
or-less tail first into canopy openings, braking nearly continuous because a leading-edge vortex
as when descending into a chimney, and flutter is maintained throughout the wing stroke during
ing briefly while gleaning among leaves. Sutton continuous motion of the sharp leading edge of
(1927) described entrance to a chimney (in Chae- the primaries. Swifts also benefit from a leading-
tura pelagica) as fluttering over the chimney and edge vortex when gliding with swept-back wings
settling down, backwards, into it. Cohn (1968:71) (Videler et al. 2004).
saw Chimney Swifts flying straight upward in a Anatomical correlates of hovering in hum
chimney with laborious "helicopter" wingbeats. mingbirds include extreme development of most
It is not clear whether these swifts were employ features of stiff-winged flight listed above. For
ing asymmetrical hovering. House Finches (Car- example, hummingbirds have the shortest hu
podacus mexicanus) have been observed hovering merus and ulna and the longest carpometacarpus
(asymmetrically) for <5 s below the down-angled and major digit in proportion to body size among
spout of a hummingbird feeder and inserting the birds (based on Thalurania compared with Apus
tip of the bill into the spout (Taylor 1972). and many other avian taxa in Boker 1927). The
Sustained hovering in hummingbirds requires inferred positions of the bony wing elements are
among the highest mass-specific rates of oxygen shown in dorsal views of a captive, hovering hum
consumption in vertebrates (Suarez 1992). Given mingbird (Florisuga fusca) by Stolpe and Zimmer
that hovering is energy-expensive and that it con (1939). Most notable are the general adduction of
stitutes the signature method of feeding on nectar the humerus and depression of the elbow at the
and non-airborne arthropods, it is reasonable to height of the upstroke. During hovering flight,
assume that flight morphologies unique to hum the elbow reaches its maximum forward position
mingbirds among apodiform birds are involved at the beginning of the backstroke as supination
with extended symmetrical hovering and rapid of the humerus begins (Cohn 1968:74). Neverthe
forward flight. less, details of skeletal kinematics, in particular the
Symmetrical hovering.—Only hummingbirds nature of abduction, adduction, elevation, and de
perform sustained and precisely controlled hov pression of the distal end of the humerus in rela
ering. However, "symmetrical" overstates the tion to the body axis, the amount of axial rotation
case for hummingbirds. (pronation and supination) of the humerus, and
the changing areas of humero-glenoid contact dur
Given that many birds possess the mass-specific ing free flight and hovering are lacking. Of special
power (using anaerobic metabolism) to hover interest is the precise role of tuberculum capitis,
for short periods, the selective pressure on hum which was considered the primary articulating
mingbird ancestors was probably for increased surface in hummingbirds by Stolpe and Zimmer
efficiency (resulting in stiff wings with greatly (1939). The role of the ventral process of the hu
simplified kinematics), and an upstroke muscle merus and its muscles in fast flight of swifts and
(the supracoracoideus) that makes the recov
hummingbirds and hovering in hummingbirds is
ery stroke rapid, while contributing enough to
also critical but little known (see Cohn 1968).
the hovering power requirements to allow the
downstroke muscle (the pectoralis) to operate Axial supination of the humerus within the
within its aerobic limits. In other words, this glenoid fossa is probably minimal when hovering
pseudosymmetrical wingbeat cycle is good with the body roughly vertical and the wingbeat

approximately horizontal (while hovering below In hummingbirds, exceptionally powerful exte

a flower to feed at a vertically suspended corolla). nsor muscles (extensor metacarpi radialis, exten
Supination would increase when hovering with sor digitorum profundus, extensor longus digiti
the body about 45° to horizontal and the wing- majoris, and flexor digitorum profundus) extend
beat horizontal at a horizontal corolla, and ex the hand. The radius and ulna are separated by
treme supination of the humerus would occur a substantial gap that is occupied in part by en
when both the body and plane of the wingbeat larged extensor muscles. The distal aponeurosis
are approximately horizontal. Among the unique or tendon of m. tensor propatagialis brevis (TPB
features of hummingbirds are those that facilitate tendon), unique to hummingbirds, also may con
supination of the wing at all of its joints, as sum tribute to extension of the manus in the extended
marized and discussed by Karhu (1992). wing. If so, it shows varying levels of specializa
I found that tensing the aponeurosis of m. tion for that function within hummingbirds (Zusi
supracoracoideus in cleared and stained speci and Bentz 1982; Appendix 3).
mens caused rotation (supination) of the humerus The pectoralis muscle of Sturnus vulgaris de
in the partly raised wing. Axial rotation of the velops force during the final third of the upstroke
humerus is effected not only by m. pectoralis and and sustains it during downstroke, and the su-
supracoracoideus but also by muscles inserting pracoracoideus is activated by late-downstroke,
on the ventral process of the humerus—m. scapu- which suggests that reduction of wing inertia
lohumeralis caudalis to pronate the humerus and (damping) is an important function of the major
coracobrachialis caudalis to supinate it (Cohn flight muscles (Dial et al. 1991, Biewener et al.
1968). Increase in size of pronator muscles that 1992). Limited study of Selasphorus rufus showed
counter supination of the forearm from air pres that damping effects of the pectoralis and supra-
sure during the downstroke is associated with the coracideus muscles during a wingbeat applied
stout and bowed radius of hummingbirds (Dial also to hummingbirds, but that the timing of
1992). Supination of the hand during the upstroke stimulation was different (Tobalske et al. 2010).
is facilitated by changes in the carpal structure of M. extensor digitorum communis effects supina
hummingbirds and by loss of supination-limit tion of the major digit during the upstroke (tra
ing wrist ligaments present in swifts. According ditional function), but probably also damps or
to Cohn (1968), the maximum cumulative axial limits strong pronation forces from air pressure
rotation of the shoulder, elbow, wrist, and digits on the distal primaries during the downstroke
at outer primaries equals 180°. Thus, at the end (unstated function). It is likely that damping or
of the upstroke the distal primaries are reversed limiting effects represent a significant function
with the ventral side uppermost, and the second of many muscles.
aries roughly vertical with their ventral surfaces Hovering limits.— Experiments on hovering
facing forward. The alular digit is reduced in size limits in gas mixtures at reduced air pressure or
and its aerodynamic function in hummingbirds reduced oxygen pressure show that humming
is not known. birds demonstrate considerable power reserves
The major pectoral muscles (M. pectoralis for hovering under normal conditions (Chai and
major and M. supracoracoideus) that power Dudley 1996). They compensate for reduced air
the upstrokes and downstrokes, respectively, in pressure by increasing wingbeat amplitude but
hummingbirds are the largest in relation to body reach an anatomical limit at amplitudes slightly
weight of any apodiform bird (Greenewalt 1962). over 180° (Chai and Dudley 1995). In field experi
Given the extreme reduction of the deltoideus ments performed at different altitudes, amplitude
muscles in trochilids, the upstroke is powered increased but limits were not reached (Altshuler
mainly by the supracoracoideus muscle, which in and Dudley 2002, 2003; Altshuler et al. 2004).
hummingbirds is also larger in relation to that of Altshuler et al. (2010) also performed experi
m. pectoralis (supracoracoideus/pectoralis ratio 1 ments in muscle physiology under conditions of
to 1.7) than in any other family. The downstroke in maximum load lifting and found that Calypte
S. rufus produces 75% of weight support and the anna could increase stroke amplitude even at the
upstroke 25% (Warrick et al. 2005). The tendon of highest wingbeat rates.
insertion of the supracoracoideus muscle is firmly Despite rapid advance in the study of vari
directed toward the humerus through an enclosed ous aspects of hummingbird flight, precise de
passageway, the coracoidal canal, of the coracoid. scription of the skeletal elements during wing

kinematics, as well as detailed functional anat

omy of the wing joints and functions of most
wing muscles, are still rudimentary.
Ve r t e b r a l C o lu m n
Boas (1929) described taxonomic and functional

diversity of the vertebral column (columna ver-
tebralis) in many families of birds, but humming
birds were excluded. Swifts and hummingbirds
have exceptionally large intervertebral openings
(foramen intervertebrale) that accommodate the
enlarged nerve complexes associated with stiff
winged flight, and the pygostyle is strongly de
veloped in hummingbirds. Variation in the atlas
and axis associated with variation in the splenius
capitis muscle was documented by Fritsch and
Schuchmann (1988). Information on length and
mobility of the neck in Apodiformes and within
Trochilidea is lacking.
P elvis (P elv ic A r c h and Sy n s a c r u m )
F ig. 19. The pelvis of hummingbirds. Dorsal view

The pelvis of apodiforms differs from that of
of E u la m p is ju g u la ris . The left pelvic arch is horizon
Aegotheles in several respects: (1) the preacetabu
tally hatched. A gap between the pelvic arch and syn-
lar ilium (ala preacetabularis ilii) is a nearly hori sacrum is shown in solid black. Transverse processes
zontal lamina rather than one raised >45° to the of the synsacrum support the pelvic arch only oppo
frontal plane, (2 ) the dorsal iliac crest (crista iliaca site the hind limb articulation (acetabulum) and at the
dorsalis) is absent, (3) the medial border of the rostral end of the preacetabular ilum. Abbreviations:
preacetabular ilium is tightly sutured to trans ace = acetabulum, ace. il. = acetabular ilium, dor. il.
verse processes of the synsacrum rather than ele cr. = dorsal iliac crest, dor.-lat. il. cr. = dorsolateral iliac
vated above them, (4) the preacetabular ilium lies crest, post.-ace. il. = postacetabular ilium, pre.-ace. il. =
parallel to or converges rostromedially toward preacetabular ilium, pub. = pubis, syn. = synsacrum,
tra. pr. = transverse process.
the long axis of the synsacrum rather than diverg
ing laterally from it, and (5) the acetabular ilium
(ala acetabularis ilii) receives no support from a hummingbirds. Apodidae have one or no such
rib process as it does in Aegotheles. In addition, vertebrae, and Aegotheles has none.
the obturator foramen (foramen obturatum) is
separated from the ischiopubic fenestra (fenestra Ta r so m eta ta r su s
ischiopubica) rather than partially or wholly sub
sumed within it; and the caudal spine of the dor In Hemiprocnidae and Apodidae, metatarsal
solateral iliac crest (crista iliaca dorsolateralis) is trochlea II and IV (trochlea metatarsus) lie below
absent. Within apodiformes, hummingbirds (Fig. the plane of I and diverge from the direction of
19) are unique in having the preacetabular ilium the middle trochlea (III), allowing adduction and
supported rostrally by both the transverse pro abduction of the digits. The trochlea of metatar
cess and rib process of only one or two vertebrae, sus I is modified to allow a variety of motions of
and in receiving little or no support of the pelvic the hallux. Steinbacher (1935b) showed that these
arch from the synsacrum elsewhere except at the characteristics are more developed in Apodidae
acetabular and postacetabular ilium (ala postac- than in Hemiprocnidae and that Cypsiurus graci
etabularis ilii). In hummingbirds and Hemiproc- lis could spread digits I and II medially, and III
nidae the synsacrum projects rostrad from the and IV laterally to effect transverse grasping of
ilium by one or two vertebrae, a morphology a vertical, stem-like structure. Collins (1983) de
mistaken by Rydzewski (1935) for a notarium in scribed this form of grasping in live Apus, and

at 90° to the plantar plane of the tarsometatarsus

and in osseous enclosure of the canal for m. flexor
digitorum longus. Cypseloides niger lacks the os
seous enclosure, and Chaetura and Apus exhibit a
medial shift of the hypotarsal crest and a deep,
caudal concavity (sulcus hypotarsi; Lucas 1895).
D iscussion
F ig. 20. The metatarsal trochleae of Apodiformes.
Proximal view of the articular surfaces for digits 2, 3, Synapomorphies of Trochilidae,—Hummingbirds
and 4 at the distal end of the tarsometatarsus. A sec
exhibit >28 osteological characters of the axial
tion through the plane of the caudal surface of the
and appendicular skeleton that are synapomor-
metatarsals (II, III, and IV) is represented by a line
diagram below each tarsometatarsus. Uniformity phic in relation to Aegotheles, Hemiprocnidae, and
of orientation of the plane in hummingbirds reflects Apodidae. Most (~90%) are clearly or potentially
reduced versatility of lateromedial movement of the associated with either nectarivory or hovering
digits. Abbreviation: met. tro. = metatarsal trochlea. flight. Not included are characters of the sternum
and humerus of hummingbirds that are similar to
saw it also in live individuals of six other genera those of Apodidae in relation to their shared be
of Apodinae, but he rarely observed a pampro- havior of stiff-winged flight with a powerful up
dactyl arrangement of toes, where all four toes stroke of the wing. Probably unique within Aves
are directed rostrally, in live birds. Nevertheless, are the developmental metamorphosis of the ven
pamprodactyly is frequently cited as an adapta tral bars of the prepalatal upper jaw, extreme re
tion for vertical clinging in swifts. duction of the lateral part of the palatinum, and
In hummingbirds, the foot is anisodactyl, with the globose nature of the capitular tubercle of the
digits II, III, and IV directed rostrally and digit I humerus. A clasp formed by the carpometacarpal
(hallux) directed caudally. The plantar surfaces of trochlea and ulnare restricts supination of the ex
trochleae of metatarsi II, III, and IV lie on a single tended wing in most birds. The clasp is apparently
plane (Fig. 2 0 ) and the trochleae are of approxi lacking only in hummingbirds (Fig. 17). Although
mately equal length. Unlike in swifts, the forward streptognathism of the opened mandible occurs in
toes lack the capability of adduction or abduction, other birds (especially fish-eaters and aerial insect-
and the foot is best suited for simple grasping. eaters), streptognathism of the closed mandible,
During their evolution, swifts and humming associated with nectarivory in hummingbirds, has
birds have lost more thigh muscles than any other not been reported in other birds. A double sulcus
birds (Garrod 1873a, Hudson 1937, Zusi and Bentz on the head of the humerus at the attachment of
1984), reflecting the limited use of bipedal locomo the acrocoracohumeral ligament occurs also in
tion. They also lack several abductor muscles of Passeriformes, but its functional significance is
the toes found in Hemiprocnidae and Apodidae unclear.
(Steinbacher 1935b, Hudson 1937, Zusi and Bentz The following lists summarize characters that
1984). The leg muscles of hummingbirds usually are unique to Trochilidae within Apodiformes.
represent <1.5% of body weight (Hartman 1961) Characters of the syrinx of unknown function:
whereas pectoral muscles represent >20% (Hart • The syrinx lies within a rostral diverticulum
man 1954). The legs of hummingbirds provide of the interclavicular membrane.
less boost at take-off than those of other birds. In • A tympanic ossicle is present on the medial
stead, hummingbirds essentially fly off the perch tympanic membrane.
(Blake 1939, Tobalske et al. 2004). Nevertheless, • The first free bronchial ring has ossified ex
simple clasping by hummingbirds when perch tremities.
ing, clinging vertically, or hanging upside down • Muscle scars and a bronchial articulation are
is supported by strong development of intrinsic, present on the tympanic drum.
tarsometatarsal flexor and extensor muscles of the Other characters of unknown function:
digits (Zusi and Bentz 1984). • The ventral choanal portion of the palatinum
The hypotarsus of hummingbirds (Fig. 20) is bilaterally broad.
resembles that of Hemiprocnidae in having a • The coracoideum has a large, dorsal pneu
strong hypotarsal crest (crista medialis hypotarsi) matic foramen.

• The humerus has a double sulcus for the acro- • The articular surface of the capital tubercu
coracohumeral ligament. lum of the humerus is semi-globose.
Skeletal characters potentially associated with • The process of m. pronator superficialis is
nectar eating: well developed.
• The intermediate portion of the upper jaw is • The radius is stout and bowed.
internally, deeply concave. • The ventral cotyla of the ulna has a weakly
• The upper jaw undergoes a unique develop defined ventroproximal margin.
mental metamorphosis. • The ulnare does not clasp the carpal trochlea
• The intermediate portion of the closed man in the extended wing.
dibula lies within the prepalatal upper jaw. • The carpometacarpus has a dentiform process.
• All bones of the mandibula are fused. • The distal articular surface of the carpometa-
• The mandibular medial process is well de carpus is flattened.
veloped. • The proximal articular surface of the major
• The palatal process of the maxillare is fused digit is flattened.
with the palatinum. Fossils.—The diversity of skeletal characters
• The lateral part of the palatinum is extremely related to feeding and locomotion that defines
reduced. modern hummingbirds raises the possibility of
• The parasphenoidal rostrum is abruptly inferring functions and biological roles of se
widened at its pterygoid articulation. lected skeletal characters found in fossils. Various
• All bones of the jugal arch are fused. exclusively fossil taxa attributed to Cypseli have
• The epibranchiale is long in relation to the been described from the Eocene and Oligocene.
ceratobranchiale (Table 2). The most commonly found elements are those of
• A sulcus for the origin of m. stylohyoideus is the wing, shoulder girdle, and sternum. When
present on the cranium. the cranium was preserved, it revealed a swift
Skeletal characters associated with hovering like bill and braincase. In the fossils, the shape
rather than stiff-winged flight: and proportions of the humeri show a morpho-
• The coracoideum has a coracoidal bar between cline similar to that of modern taxa (Aegotheli-
the acromial and procoracoidal processes. dae-Hemiprocnidae-Cypseloidinae-Apodinae;
• The supracoracoidal nerve foramen is pro Zusi and Bentz 1982, Mayr and Peters 1999).
portionally large. However, occurrences of highly derived, swift
• The lateral process of the coracoid is ex like, fossil humeri by Middle Eocene and one
tremely reduced. species (Scaniacypselus szarskii) with swift-like
• Size-adjusted sternal body length and keel feathering (Mayr and Peters 1999) imply an early
depth are uniquely great. diversity of aerial insect-eaters with stiff-winged
• An intermuscular line intersects the ventral flight. Among those species with swift-like jaws
margin of the sternal keel. (beak wide and short with pointed tip and large,
• An intermuscular line follows the lateral bony nasal opening) is one (Paragornis messelen-
margin of the sternal body. sis) with short, rounded wings and long, broad
Table 2. Length of bill and hyobranchiale elements of hummingbirds divided by cube root of
body mass.
Cube root Cerato-

Species body mass Bill Basihyale branchiale Epibranchiale
D ory fera lu d o v ica e 1.82 19.3 1.8 2.6 11.6

C o elig en a coelig en a 1.89 17.8 2.2 3.0 16.9
G lau cis h irsu tu s 1.82 17.0 2.3 3.0 14.1
H elio d o x a b ran ickii 1.74 15.3 2.0 2.5 16.0
H . lea d beateri 1.94 14.3 2.3 3.0 22.9
H . x an th og on y s 1.91 14.0 1.9 2.9 16.6
H . ja c u la 2.04 13.2 2.2 2.9 19.8
C h ry sola m p is m o squ itu s 1.57 10.2 2.0 2.6 12.8
F lo risu g a m elliv ora 1.95 10.8 2.2 2.3 14.1

rectrices, suggesting an adaptive radiation in but it develops rapidly with increase in length of
Cypseli by the Middle Eocene (Mayr 2003a). One the jaws during the first few weeks after fledging.
taxon (Jungornis; Lower Oligocene) displayed Eurotrochilus evidently grew a long bill without
a rudimentary tuberculum capitis, a character acquiring adaptations characteristic of modern
now best developed in modern Trochilidae. As hummingbirds.
developed in modern hummingbirds, this struc The same fossil revealed a pair of ceratobran-
ture was claimed to facilitate hovering (Stolpe chials associated with the skull, prompting the
and Zimmer 1939). More recently, fossils from statement that "As in modern hummingbirds,
the early Oligocene of Europe have been inter the new fossil has...very large hyoid bones"
preted as members of a hummingbird clade and (Louchart et al. 2007:173-174). These authors
were said to be hummingbirds of "essentially thought that the latter confirm nectarivory be
modern appearance," exhibiting morphological cause a large hyoid apparatus supports the long
specializations toward nectarivory and hover protractile tongue used by hummingbirds to lap
ing flight (Mayr 2004). Apparently representing up nectar. However, I found that the mean cera-
several species of the genus Eurotrochilus (Mayr tobranchial lengths of a swift and two humming
2004, 2007; Louchart et al. 2007; Bochenski and birds, divided by coracoid length, were as follows
Bochenski 2008), they reveal many skeletal ele (n = 4): Collocalia marginata, 0.757; Phaethornis guy,
ments, some in articulation, and skulls with long 0.689; and Eulampis jugularis, 0.649. In summary,
bills; one specimen shows feathering. In my opin there is no evidence from the ceratobranchiale or
ion, the phylogenetic relationships of Paragornis, bill structure to support nectarivory.
Argornis, Jungornis, and Eurotrochilus, shown as Tuberculum capitis of the humerus in Euro-
a "stem group" to Trochilidae by Mayr (2005), trochilus is less developed than in modern
are not convincingly resolved. Here, I comment hummingbirds and apparently lacked a dorsal,
only on characters claimed by Mayr (2004) to in globose articular condyle. The globose, ventral
dicate a capacity for hovering and nectivory in surface of the tuberculum capitis of modern hum
Eurotrochilus. mingbirds articulates with the scapular portion
The evidence for nectarivory in Eurotrochilus in- of the glenoid capsule when the humerus is
expectatus was "a greatly elongated beak" (Mayr adducted and supinated during hovering (Stolpe
2004:863). None of the Apodiformes, modern or and Zimmer 1939, Karhu 2001, R. L. Zusi unpubl.
fossil, has a long bill other than Eurotrochilus and data). A reduced version of the capital tuberculum
Trochilidae, but the bill of Jungornis is unknown. occurs also in the fossils Jungornis and Eurotrochi-
The prepalatal upper jaw of modern humming lus, rarely in Hemiprocne, and in some modern
birds usually is long and bilaterally narrowed dis galliforms (Karhu 2001, Mayr 2004), but in view of
tal to the nasal region, with lateral margins roughly the small tuberculum in Eurotrochilus, a significant
parallel in dorsal or ventral aspect. Although Mayr role in articulation is questionable.
(2004) described the beak of Eurotrochilus as "nar The carpometacarpus of Eurotrochilus has a
row," there is no marked narrowing or nearly poorly developed intermetacarpal process and
parallel profile visible in the published figures. lacks the dentiform process. Illustrations in Mayr
According to Louchart et al. (2007), the bill of Flo- (2004, 2007) and Louchart et al. (2007) show that
risuga mellivora most closely approximates that of the caudal border of the carpal trochlea of the car-
Eurotrochilus in width. The dorsoventral profile of pometacarpus was not truncate as it is in modern
the bill of Eurotrochilus does not preclude nectar- hummingbirds, which suggests that the ulnare
ivory, but it is not evidence for it. The long bill of would restrict supination of the carpometacarpus
another fossil referred to Eurotrochilus (Louchart in the extended wing of Eurotrochilus as it does in
et al. 2007) is exposed in lateral view and differs swifts, but not in modern hummingbirds.
from modern hummingbirds in its angled gonys, The sternum of E. inexpectatus clearly shows
stout dorsal and ventral bars, and long nasal open that linea intermuscularis on the carina has a
ing. There is no reduction of the nasal opening by configuration like that of modern swifts. This im
vertical orientation of the ventral bars in the inter plies that m. supracoracoideus is not as enlarged
mediate part of the upper jaw. As described pre as in modern hummingbirds. Smaller size of the
viously, the inverted U-shape of the intermediate coracoidal foramen (and probably the supracora-
part of the prepalatal upper jaw in transverse sec coideus nerve) is also consistent with a smaller
tion is not present in the nestling hummingbird, supracoracoideus muscle. Given the swift-like

proportions of the flight apparatus presented (1999:506) suggested that nectarivory, not in-
by Mayr (2004) and the reduced tuberculum sectivory, was the major stimulus for evolution of
capitis, the combined evidence suggests that the hummingbird feeding apparatus.
Eurotrochilus lacked the hovering skills of modern I think it likely that a bill longer than those seen
hummingbirds. in modern swifts and fossil Cypseli would have
Eurotrochilus inexpectatus shares a coracoid improved the efficiency of insect-gleaning from
length of 7.6 mm with Hylocharis grayi, Cyanophaia leaves or probing of vegetation. Perhaps in the first
bicolor, Heliangelus exortis, and Chalcostigma stan- stage, a subset of aerial insect hawkers or salliers
leyi. On the basis of published weights of the latter increased their use of hover gleaning for insects on
four species (Dunning 2008), Eurotrochilus prob vegetation, developing a longer bill and improved
ably had a weight in the range of 4.5-5.8 g. Using hovering capability. In a later stage, they may have
data on 208 species of hummingbirds from a va used the longer bill and more efficient hovering
riety of sources, Collins and Patton (1989) found to drink water from vegetation and obtain nectar
the mean (± SD) mass to be 5.1 ± 2.9 g. The fre from flowers. However, an intervening stage may
quency of mass classes was 54.3 for <5.0 g and 42.8 have occurred: a subset of hover-gleaning species
for 5.0-9.9 g. Of the 88 species of Apodidae listed with a long bill may have specialized on insects
by Dunning (2008), 46 (52%) fell within the size associated with nectar-producing flowers rather
range of hummingbirds (297 species), and of the than on those in nonfloral vegetation. This behav
297 species of hummingbird, 149 (50%) fell within ior might have initiated an introduction to nectar,
the range of swifts (4.9-108 g). Thus, "small size," first through consumption of nectar-eating insects
without qualification, is not a diagnostic feature of near or in flowers, or nectar-producing insects
the family Trochilidae (contra Mayr 2004), and Eu- (aphids or scale insects), and then through direct
rotrochilus was comparable in size to both modern contact with flowers and nectar. Addition of nectar
hummingbirds and swifts. to the diet could have led to increased selection for
Evolution of nectarivory and hovering.—The above improvements in hovering and growing reliance
considerations and the list of features in which Eu- on nectar for energy. Further adaptations of the
rotrochilus differs from "crown-group Trochilidae" bill, tongue, and hyobranchial apparatus for
presented by Mayr (2004) allow alternative inter nectar eating would make insect capture strangely
pretations of phylogeny and behavior of the fossil awkward, as seen in modern hummingbirds, and
taxa. Eurotrochilus (and possibly Jungornis) may be insect hunting would be focused on situations that
part of an adaptive radiation within Apodiformes provide the greatest success. In my opinion, the
independent of the hummingbird clade, in which available evidence from Eurotrochilus would place
feeding and locomotor methods differed from it in the first stage.
modern swifts. Alternatively, Eurotrochilus may
represent a branch of the clade that includes Tro- Section II. The D iversity of H ummingbirds
chilidae but embodies a stage in which hovering
was not yet highly developed, and nectarivory, if In this section, emphasis is on variation between
present, was supplemental to insectivory. species and among higher-level clades below
Assuming aerial, arthropod eating as ancestral the family level. Many variations throughout
in Cypselae, how does one envision the evolu the skeleton within Trochilidae are documented
tion of a nectar-adapted bill, tongue, and hyoid here for the first time. The taxonomic distribution
apparatus, and of sustained, controlled hovering of character states and examples of intraspecific
in hummingbirds? Cohn (1968:169) proposed that variation are broadly indicated below and further
hovering developed in birds that gleaned insects detailed in Appendix 2. Use of generic names as
from vegetation, and that maintaining position examples for character states indicates that the
in the air efficiently would be beneficial for that character state occurs in some, but not necessarily
behavior. Mayr (2003b:148) thought that hovering all, of the species. Regrettably, the functions and
might have "primarily evolved as an adaptation biological roles of most of the variation catalogued
for gleaning insects from the underside of leaves... here are currently unknown, but emphasis is on
or around flowers and as a preadaptation for the variation that I judged to have the most promise
highly derived nectarivory of extant Trochilidae for further study. For convenience and continu
(Mayr and Manegold 2002)." Schuchmann ity with the previous section, data are again

organized topographically, and I continue to use B ill

the informal terms "Hermit" and "Trochiline"
(see Fig. 1). In addition, I refer to subclades sup In general, hummingbirds have long bills in relation
ported by anatomical characters but not shown to cranial length, but they also exhibit a wide range
in Figure 1 as (1) the Anthracothorax group (Polyt- of bill lengths (Ramphomicron to Ensifera) and a
mus through Eulampis) within Mangoes and (2) lesser range of bill widths. Both variables may have
the Amazilia group (Chlorestes through Hylocha- ecological significance (Temeles et al. 2002). Hum
ris) within Emeralds (see Appendix 1 for a list of mingbirds are also noted for other differences in bill
included species). shape, from strong decurvature (Eutoxeres), mod
erate decurvature (most Phaethornis), or terminal
Size recurvature (Avocettula recurvirostris, Opisthoprora
euryptera) to no curvature (many genera). In this
General body size, represented by body weight, they differ from passerine nectarivores, almost all
is temporally and sometimes geographically vari of which have variously decurved bills.
able within each species. Nevertheless, the sample Differences in the form of the upper mandible,
of published weights presented by Dunning (2008) such as presence of a hook, terminal recurva
provided a useful approximation of size variation ture, tomial serrations (Ornelas 1994, R. L. Zusi
within the named clades of hummingbirds. Both unpubl. data), and lateral compression into a
the largest and smallest weight classes are appar blade (Heliothryx and Augastes), are primarily
ently derived within Trochilidae, but polarity of or completely restricted to the rhamphotheca.
size categories within clades is not firmly estab Similarly, extended basal feathering (e.g., Helio-
lished. Size ranges in grams are as follows: Her doxa and Ensifera) and fleshy dermal expansions
mits (2.3-10.9), Topazes and Mangoes (3-12.6), (Trochilus and Cynanthus) over the craniofacial
Brilliants (3-11.4), Coquettes (2.3-9.1), Patagona bending zones are not reflected in the skeleton.
(20), Mountain Gems and Bees (1.9-9.2), and Em Ventral expansion of the caudal rhamphotheca of
eralds (2.2-9.8). Note that each clade includes spe the upper mandible of Anopetia may or may not
cies within the size range of Bees (1.9-4.3). have an osteological counterpart (no skeletons
were available). Of special interest are the pro
Syrinx nounced, opposing hooks on the mandibles of
adult male Ramphodon and Androdon (Fig. 21) that
The following notes on syringeal variation are are little developed or absent in immature males
based on cursory examination of a small sample and in females. How do adult males perform
of hummingbird taxa (Eutoxeres aquila, Glaucis tongue lapping of nectar in the presence of such
hirsutus, Threnetes ruckeri, T. leucurus, Phaethornis opposing hooks? Sazima et al. (1995), Bleiweiss
malaris, P. superciliosus, Anthracothorax domini-
cus, Chrysolampis mosquitus, Florisuga mellivora,
Colibri coruscans, Doryfera lucovicae, D. johannae,
Coeligena coeligena, and Mellisuga minima). Among
these genera, ( 1 ) internal division of the bronchial
drum occurs only in M. minima, (2) the lateral
lamella is fully ossified only in Hermits, (3) the
drum is short or long (variable within genera),
(4) the drum may exhibit a dorsolateral ridge
(C. coruscans and D. johannae). The tympanic
ossicle varies in shape and occurrence: anvil
like in Hermits, slender and curved to knobby Fig. 21. Rhamphothecal serrations and hooks in a
hummingbird. Lateral view of A n d ro d o n aequ atorialis.
in Trochilines, and absent in F. mellivora. The
Serrations and hooks are not reflected in the underlying
mid-dorsal and midventral lengths of the drum
bone. Although serrations are found in many species,
are nearly equal and the pessulus rises almost prominent hooks on both mandibles are restricted to
vertically in Trochilines, whereas the midventral adult males of A . aequ a to ria lis and R a m p h o d o n n aeviu s.
portion of the drum is longer and the pessulus The apparent interruption of serrations on the upper
slopes rostrodorsally from its ventral attachment mandible is artifactual. Abbreviation: l. mand. = lower
in Apus and Hermits. mandible, ser. = serration, u. mand. = upper mandible.

et al. (2003), and Ornelas (1994) did not address

this problem.
P r epa la t a l U p p e r J aw
Intermediate part.—Among hummingbirds, the

prepalatal upper jaws of Heliothryx and Schistes
have a proportionally long, bony nasal open
ing in which the flattened plane of the ventral
bars is roughly horizontal, and a proportionally
short intermediate part in which the plane of the
ventral bars is more vertical.
Nasal part.—The transverse section of the
dorsal bar in the nasal part may be circular,
dorsoventrally compressed, or mediolaterally
compressed—configurations that may be modi
fied by the nasal roof. Species in which hyoid
horns penetrate the bony nasal opening on either
side display an excavation of the ventrolateral
portion of the dorsal bar on that side (e.g., Topaza
pella, Ensifera ensifera, Heliodoxa branickii, H. aure-
scens, H. rubinoides, and H. leadbeateri). The dorsal
bar at the rostral portion of the nasal region may
be uniformly narrow or gradually widened ros
trally in dorsal view, and variable in length.
Length of the nasal part, adjusted for body
size (indexed by coracoideum length), is modally
shorter in Hermits than in Trochilines (R. L. Zusi
unpubl. data). The nasal part (Fig. 22A, B) includes
the vestibular region (regio vestibularis) and Fig. 22. Structures of the nasal part of the prepalatal
respiratory region (regio respiratoria). Partial sep upper jaw in hummingbirds. (A) Partial humming
aration of the two regions is provided by the nasal bird skull in dorsal view for orientation of B-D. (B)
crest (crista nasalis), a ventral, transverse ridge of Diagrammatic composite of left side in dorsal view, with
the dorsal bar. The medial wall (paries) of both nasal roof and maxillary processes of nasale removed, and
regions is formed by a continuous, membranous nasal operculum added. Bone is stippled, rostral concha
nasal septum. A blind, caudodorsal pouch of the is gray, and medial concha is solid black. Both conchae
are suspended from the dorsal bar and nasal roof. The
respiratory region represents an olfactory region
vertical lamella rises from the ventral bar within the
(regio olfactoria), bounded caudally by the mes-
nasal opening of the nasal operculum. (C) Diagrammatic
ethmoidale and ectethmoidale. In hummingbirds, transverse sections through the rostral concha, which
the nasal part includes a broad, lateral, nasal oper may have an inverted T-bar form (above) or a J-bar
culum (operculum nasale) that defines the exter form (below). (D) Semidiagrammatic representations
nal, membranous nasal opening (naris). The latter of the left rostral concha in dorsolateral view; inverted
is a long, horizontal slit that widens posteriorly, T-bar form above, and J-bar form below. The base of the
bounded dorsally by the leathery operculum and medial concha in solid black. Variations shown have
ventrally by the ventral bar. The respiratory pas no known functional significance. Abbreviations: dor.
sage traverses the external naris, vestibular region, bar = dorsal bar of upper jaw, ext. spa. = external space,
int. spa. = internal space, lat. sec. = lateral sector, lat.
and respiratory region. Openings in the floor of
wing = lateral wing, med. sec. = medial sector, nar. =
the respiratory region are the internal nares me
external nasal opening, nas. pt. = nasal part of upper jaw,
dially and the antorbital sinus (sinus antorbitalis) nas. roof = roof of nasal region, nas. oper. = nasal oper
laterally. The nasal cavity is partially subdivided culum, nas. cr. = nasal crest, nas. sep. = nasal septum,
transversely into a medial sector (sector media- res. reg. = respiratory region, ven. bar = ventral bar, ven.
lis) between the nasal septum and the conchae wing=ventral wing, ver. lam. = vertical lamella, vert. wall =
and a lateral sector (sector lateralis) between the vertical wall, ves. reg. = vestibular region, vom. = vomer.

An olfactory concha (concha nasalis caudalis) is

lacking in hummingbirds and in Collocalia (Bang
1971), but its status in other apodiforms is un
known. There is no fusion of nasal structures
with the ventral bars (as noted also in Archilo
chus alexandri by Shufeldt (1885).
The conchae are a rich source of variation in
hummingbirds. In most Trochilines the medial
concha becomes broader and ribbon-like cau
dally and scrolls along its long axis from less than
one turn to one-and-a-quarter turns. Scrolling
Fig. 23. A sample of variation in the ossified nasal
is absent in most Hermits, Heliothryx, Androdon,
roof in Trochiline hummingbirds. Right side, dor Heliactin, Topaza, and some Colibri; instead, the
sal view; rostral direction to left. The vestibular and free margin of the shelf-like concha is thickened
respiratory portions are highly variable in size and and rod-shaped and contains venous sinuses. In
shape within Trochilidae, but some patterns reflect all hummingbirds the medial concha narrows
phylogeny at various levels. Patterns often found caudally and terminates on the ectethmoidale.
in A n th ra co th o ra x , E riocn em is (above, left and right), In transverse section, the rostral concha
H elio d o x a , and C h lorostilb on (below, left and right). See
(Fig. 22C) exhibits either an inverted T-shape
also Figures 4, 6, and 8. Abbreviations: dor. bar = dor
(most hummingbirds) or a J-shape with the
sal bar of the upper jaw, res. = respiratory roof, ves. =
ventral curve directed medially (Florisuga, An
vestibular roof.
thracothorax, Eulampis, Chrysolampis, some Helio
conchae and naris. The main air passage between doxa and Coeligena, and the Amazilia group). For
lateral and medial sectors lies just anterior to the brevity I shall refer to the inverted T-shape of
rostral concha, and a more restricted passage con the rostral concha simply as a "T-bar," and to the
tinues caudally as a narrow space between the J-shape as a "J-bar." Intermediate states occur. For
ventral border of the rostral concha and the ven example, the ventral wing (ala ventralis) of the
tral bar. In outgroups and Hermits the nasal roof T-bar may be reduced or missing in some portion
and conchae are largely cartilaginous. However, of the concha; or the ventral wing may taper ante
all hummingbirds have part of the roof of both riorly and disappear at, or near, the anteroventral
the vestibular and respiratory regions ossified in limit of the concha. Some form of intermediacy is
the vicinity of the nasal crest, and ossification found in Glaucis, Threnetes, Androdon, Heliothryx,
of the nasal roof and conchae in Trochilines is many Brilliants, Patagona, and some species in the
usually extensive (Fig. 23). Amazilia group. All states may be found within
The rostral concha is suspended from the roof the Heliodoxa group, and the genus Campylopterus
of the vestibular region by a vertical wall (paries is also highly variable.
verticalis) and continues, unsupported, into the Among the species with a T-bar, the ven
respiratory region. The rostral concha is cartilag tral wing of the rostral concha (Fig. 22D) may
inous in outgroups, Hermits (except Eutoxeres), protrude anteriorly beyond the vertical wall
and some Mangoes (Androdon, Colibri, Schistes, of the concha (Doryfera, various Brilliants and
and Augastes), and is ossified in Eutoxeres, Coquettes, Eugenes, Lamprolaima, and Bees).
Florisuga, some Mangoes, and all Neotrochilines. Uniquely to Lampornis and Lamprolaima, the an
The medial concha (concha nasalis medialis) is terior portion of the ventral wing is marked ven
suspended anteriorly from the roof and sides of trally by a groove that curves anteromedially and
the respiratory chamber by an ossified, rod-like produces a notch in the rostral tip of the concha.
base, and passes caudally, unsuspended and The vertical wall may curve laterally at its ante
cartilaginous, to its attachment on the posterior rior extremity (Ensifera, Phlogophilus, Sephanoides,
wall of the combined respiratory and olfactory Lophornis, Urosticte, most Coquettes, Eugenes,
chambers. I found that, in general, the vestibu Bees, Cynanthus, and Basilinna). Species with a
lar region is lined with stratified squamous T-bar usually have a well-developed vertical
epithelium, the respiratory region with ciliated lamella (lamella verticalis)—a vertically oriented,
cuboidal or ciliated columnar epithelium, and longitudinal baffle arising from the ventral bar in
the olfactory area with olfactory epithelium. the caudal part of the vestibular region just inside

the external naris and oriented parallel to the con The middle portion of the craniofacial hinge,
cha. This lamella partially subdivides the lateral comprising the frontal processes of the premaxil
sector into external and internal spaces (spatium lares and premaxillary processes of the nasales,
externum and spatium internum). Species with is underlain by the mesethmoidale. Flexibility
a baffle also may have one or more tubercles or of that portion of the hinge is lost in some gen
ridges that descend from the nasal operculum to era (Eutoxeres, Doryfera, Eugenes, Coeligena, and
cross or embrace the caudodorsal margin of the Ensifera) by fusion of mesethmoidale and pre
lamella. In species with a J-bar the vertical lamella maxillare, a specialization associated with "distal
is reduced typically to a low, roughly horizontal rhynchokinesis" in some Charadrii (Zusi 1984).
ridge that does not divide the lateral sector. The
J-bar apparently is a derived state within Trochili- Palatum
dae, primarily through loss of the ventral wing of
a T-bar and of the vertical lamella. Vomer.— The rostral profile of the vomer from
The roof of the nasal part of the upper jaw may dorsal or ventral view (Fig. 24A) varies from
be largely unossified (Androdon), but ossification rounded (most Hermits, Topazes, Mangoes, some
associated with both the vestibular and respira Brilliants and Coquettes, some Mountain Gems
tory regions occurs in most hummingbirds, in and Bees) to angular (some Mangoes, Brilliants,
various patterns (Figs. 7B, 8 , 22, and 23). Coquettes, Mountain Gems, Bees, and Emer
Flower mites.—Flower mites (Ascidae) are alds), and the angles may be enhanced by spic
known to travel from one flower to another (pho ules (some Heliodoxa; see Graves and Zusi 1990).
resis) in the nasal cavity of hummingbirds and The body may comprise little more than a junc
passerine nectarivores, gaining access to or depart ture of the pterygoid processes (most Hermits,
ing from flowers by running along the bill of the Topaza, Mangoes, Brilliants, Coquettes, Mountain
feeding bird. Mites may be found in any part of the Gems, and Bees) or it may be a variably exten
nasal chambers in spirit specimens of humming sive plate (Emeralds). Eutoxeres is distinguished
birds, possibly having wandered after death and among hummingbirds by a long, narrow vomeral
before fixation of the bird; their locations in the liv body that becomes spatulate rostrally. Huxley
ing bird are not well known. The biology of flower (1867:454) stated that "Trochilus has the true
mites has been investigated by various authors Passerine vomer, with its broad and truncated
(e.g., Colwell 1985, Colwell and Naeem 1993), but anterior, and deeply cleft posterior end." Since
little is known about the relation of mites to nasal then, other workers have overemphasized the
anatomy of the carrier. The lateral section of the systematic importance of an angular profile of
nasal cavity of hummingbirds (Fig. 22C), lined the vomeral body and the presumed aegithog-
with stratified squamous epithelium, may serve to nathous palate in hummingbirds. For example,
house mites in a location that permits their rapid Lowe (1939) accepted Huxley's conclusion after
departure and that isolates them from the respira dissecting species from eight genera, three of
tory region and its ciliated epithelium. which actually have a rounded or nearly rounded
Craniofacial hinge.—The amount and location vomer (Eulampis, Ensifera, and Patagona).
of decalcification in the nasale during posthatch The vomeral spine of hummingbirds is short in
ing development, discussed in Section I, probably Colibri, Brilliants, some Coquettes and Bees, Pan-
differs within Trochilines and probably explains terpe, Campylopterus, and some other Emeralds,
different forms of the caudal portion of the bony and long in Hermits (except Eutoxeres), Topazes,
naris—long and slit-like in Eutoxeres, narrow and the Anthracothorax group, Heliodoxa, Coeligena,
pointed in Androdon, or broad and delimited by Patagona, and some Emeralds. A bony spine is
the ectethmoidale. In some (e.g., Heliodoxa), the absent from Eutoxeres, but I found a cartilaginous
bony narial opening stops just short of the cra spine in a poorly cleaned skeleton of E. condamini.
niofacial hinge and is broadly rounded within Maxillare.—The palatal process of the maxillare
the nasal bone. The slit-like bony nasal opening may extend dorsally or dorsomedially beyond its
of Eutoxeres occasionally extends to, or transects, co-ossification with the rostral process of the palati-
the craniofacial hinge. Characterization of Her num, as either a slight ridge or a short hook (most
mits and Trochilines as strictly holorhinal and Hermits, Topazes, Mangoes, and Brilliants). In some
schizorhinal, respectively, is therefore somewhat species, the hook expands caudally and lies parallel
ambiguous and simplistic. and medial to the palatinum (some Brilliants and

F ig. 24. Examples of variation in shape of the vomer, palatal process, and palatinum in hummingbirds. (A)
Ventral view of hummingbird palate for orientation in B and C. Most of upper jaw (to left) not shown. Left
palatinum obliquely hatched, vomer in solid black, rostral is to left. (B) Vomers in dorsal or ventral view: (1)
P h a eth o rn is g u y , (2) E u to x eres a q u ila , (3) E u to x eres c o n d a m in i, (4) T opaza p ella , (5) F lo ris u g a m elliv o r a , (6) H elio d o x a
lea d b e a ter i, (7) C o lib r i d elp h in a e , (8) P a n te rp e in sig n is, (9) E u p e to m en a m a c r o u ra , (10) T rochilu s p o ly tm u s . Note lack
of vomeral spine in E u to x e re s . Except for the latter, a vomeral spine is found in all species of hummingbird.
Otherwise, no particular vomeral shape characterizes Trochilidae. (C) Variation in shape of palatal process of
maxillare and location of lateral process of palatinum (left, ventral view), scaled to similar length of palati
num; vomer absent and pterygoideum incomplete. The patterns are exemplified by (1) L a m p o r n is a m e th y s tin u s ,
(2) P h a eth o rn is h isp id u s , and (3) A n th ra c o th o r a x m a n g o . Note that the caudal extremity of the palatal process fuses
with the rostral bar of the palatinum and assumes various shapes. The lateral part of the palatinum may lie (1)
between the rostral bar and ventral choanal lamella of the palatinum (mostly in Neotrochilines), (2) on the rostral
bar (mostly in Hermits), or (3) on the ventral choanal lamella (mostly in Mangoes). Abbreviations: jug. arch =
jugal arch, lat. pt. = lateral part of palatinum, max. = maxillare, pal. pr. = palatal process of maxillare, pter. =
pterygoideum, pt. pr. = pterygoid process of vomer, ros. bar = rostral bar of the palatinum, ros. pr. = rostromedial
process of the palatinum, spi. = spicule, ven. cho. lam. = ventral choanal lamella of the palatinum, vom. ang. =
vomeral angle, vom. body = vomeral body, vom. sp. = vomeral spine.

Coquettes). The extended portion may be irregular In most species the ramus gradually widens
in outline, possibly indicating ossification of its sur caudally, becoming oval in transverse section,
rounding membrane (Patagona, all Mountain Gems, but the caudal part may exhibit a more abrupt
Bees, and Emeralds; Fig. 24C: 1). pneumatic inflation, the most extreme examples
Palatinum.— The lateral part of the palatinum manifesting also a large rostral mandibular fe
usually lies near the junction of the ventral cho nestra (some Mangoes, most Brilliants and Co
anal lamella and rostral bar, but it may lie farther quettes, Patagona, Mountain Gems, Bees, and
caudally on the lamella or more rostrally on the some Emeralds). In Hermits, the free rami are
rostral bar (Fig. 24C). It serves for insertion of narrowly oval in transverse section throughout,
m. pterygoideus (pars ventralis medialis), which vertically oriented caudally, and becoming more
originates on the medial process of the mandibula horizontal toward the symphysis. The rostral
in both swifts and hummingbirds (Morioka 1974, mandibular fenestra is absent or small in relation
Zusi and Bentz 1984: fig. 3a). The more rostral po to the depth of the ramus in Hermits, and largest
sition of the latter part probably reflects a longer in Heliothryx, Aglaeactis, Ensifera, Coeligena, Ptero-
pterygoideus muscle in Hermits and Androdon, phanes, Boissonneaua, Discosura, Loddigesia, Lesbia,
which also have conspicuously large adductor Ramphomicron, Oxypogon, Patagona, Mountain
mandibulae muscles. By contrast, a markedly Gems, and some Bees. Lateromedial bending of
caudal position of the lateral part is found in the rami occurs between the rostral mandibular
Topazes and Mangoes (except Androdon). fenestra and the inflated portion of the caudal ra
Pterygoideum.—A syndesmotic, intrapterygoid mus in many Trochilines, but the zone of bending
articulation occurs in all outgroups. In a minor is less restricted in Hermits. In them, the fenestra
ity of hummingbird species the articulation is is lacking or minimal.
present in adults, but in the majority the articu Although I did not measure the length of
lation is obliterated by fusion. The articulation, the mandibular symphysis in most species,
although variable in its occurrence in adults of Threnetes ruckeri is probably unique in having a
many species, is commonly found in Eutoxeres, symphysis that occupies almost half the length
Colibri, Schistes, some Brilliants and Coquettes, of the bill (that of T. leucurus is about one fifth)
Patagona, Lampornis, some Bees, Orthorhynchus, (Fig. 25). In T. ruckeri the ventral surface of the
and Klais. Individuals that lack the intrapterygoid symphysis is planar and forms an abrupt 90°
articulation have a pterygopalatine arch without angle with the lateral portion. The planar sym
articulations or well-defined hinges. physis fills the space between the ventral bars
Jugal arch.—In adults of Aegotheles, Hemiprocn- of the prepalatal upper jaw, and presumably
idae, and Apodidae and a juvenile hummingbird the bright yellow rhamphotheca of the enlarged
(Chlorostilbon swainsonii) the jugal arch consists of symphysis is conspicuous in display. The sym-
a long quadratojugale extensively sutured with a physial part of the prepalatal upper jaw is not
long jugal process (processus jugalis) of the max- correspondingly elongate.
illare. The jugale is absent. Adult hummingbirds
differ from other Apodiformes in that the two C ranium
bones forming the arch are fused. A minor and
variable lateral or medial widening of the rostral Cranial shape.— In dorsal view (Figs. 4, 26A, and
portion of jugal arch in the frontal plane occurs in 27A) the rostral contour of the ectethmoidale
a few species of hummingbird, most prominently usually slopes caudolaterally from the trans
in Ramphodon and many species of Phaethornis, vere axis of the craniofacial hinge, but in many
possibly in relation to the insertions of enlarged Coquettes it nearly parallels the hinge axis and
pterygoideus muscles. forms a right angle with the supraorbital margin
(margo supraorbitale). The profile of the frontal,
M andibula extending from the lateral limit of the ectethmoi-
dale to the caudal margin of the orbit, in dorsal
In its least differentiated form, the intermedi view, may resemble a medially concave V (most
ate part of the mandibular ramus is laterally Hermits, Topazes, Mangoes, most Brilliants,
compressed and the tomial and ventral mar some Coquettes, and Bees), a medially concave
gins somewhat swollen and rod-shaped (thus VJ (some Heliodoxa, many Coquettes, Mountain
roughly hourglass-shaped in transverse section). Gems, Bees, and Emeralds), or a medially concave

the cranium of all but the smaller species is

proportionally long, narrow, and caudally tapered,
with deep grooves that house the hyoid horns
(cornu branchiale). The orbitocranial fonticulus
(fonticulus orbitocranialis) may be narrower lat-
eromedially (Hermits and some Mangoes), wider
(most hummingbirds), or almost circular (many
Coquettes; Fig. 26B). A partial separation of the
optic foramen (foramen n. opticum) from the or-
bitocranial fonticulus is least prominent in Her
mits, some Mangoes, and some Coquettes, and
more prominent in other hummingbirds. Skulls
of the smaller Coquettes are proportionally short
and spherical. Although the profile of the cerebel
lar prominence of most hummingbirds is evenly
curved in lateral view, a few species show a
contour that is caudally blunt (Heliodoxa, Sterno-
clyta, Patagona, and Schistes; Fig. 26B). In rostral
view (Fig. 27A) the lateral margins of the ecteth-
moidales may be vertically parallel (Hermits,
Topazas, some Mangoes, Brilliants, Patagona, Bees,
and Emeralds) or may slope to varying degrees, al
ways converging dorsally (especially Coquettes).
Occiput and Basicranium.— Midventrally the
F ig. 25. Mandibular variation in T h ren etes. The sym- curve of the cerebellar prominence terminates
physial part of the mandíbula of T. ru c k e ri is propor
at the foramen magnum, either without modifi
tionally much longer than that of T. leu c u r u s , in which
cation (most hummingbirds) or with a swelling
the rami may be spread (while drinking nectar?) as
shown in the gray-shaded mandibula, or relaxed as (Fig. 26B) associated with pneumatization along
shown by the dashed line. In T. r u c k e ri the long and the dorsal rim of the foramen (e.g., Ramphodon,
broad symphysis maintains a mandibular profile simi Phaethornis, Doryfera, Chrysolampis, Coeligena,
lar to that of the spread state in T. leu c u r u s , and the flat Urochroa, Ensifera, Heliodoxa, and Ocreatus). In the
tened, bright yellow, ventral surface of the symphysis internal brain cavity (endocranium), a feature
may represent a display feature. Abbreviation: free sometimes visible through the foramen magnum
ram. = free ramus of mandibula, sym. pt. = symphysial (Fig. 27B) is the caudal wall (dorsum sellae) of the
part of mandibula. hypophysial recess (sella turcica). The caudal wall
is ligamentous, but its dorsal rim may be ossified
U (Eutoxeres, Ramphodon, some Phaethornis, some fully to form a bony bridge (Florisuga, Colibri,
Campylopterus, and Pterophanes). Chrysolampis, Eulampis, and many Coquettes). The
The cranium in adults of almost all humming ossified bridge is partial or absent in most other
bird species is fully ossified dorsally but unpneu hummingbirds, including Topaza. It is absent
matized medially. However, within the otherwise or present in swifts.
pneumatized, rostral portion of the frontal bones, Processes, crests, and fossae.—The size of m. ad
a frontal fenestra (fenestra frontalis) occurs in a ductor mandibulae externus (Fig. 10C) is related
few genera (Polytmus, Anthracothorax, Eulampis, to the size of the temporal fossa (fossa temporalis
Chrysolampis, and possibly Avocettula; Fig. 26A). musculorum), reflected in part by its defining crests,
Apparently, ossification (and pneumatization) and by the distance between the postorbital (pro
of this fenestra progresses slowly because most cessus postorbitalis) and zygomatic processes (pro
adult specimens of each species exhibit the fenes cessus zygomaticus; Figs. 4A and 26B). All of these
tra, but occasionally it is reduced or absent. I have features are most developed in Glaucis, Ramphodon,
found no similar fenestra in other avian families. and Androdon, but only Ramphodon has a midsag
The cranium in hummingbirds varies in ittal crest (crista nuchalis sagittalis). Androdon ex
the length in relation to the width of both the hibits a uniquely short and broad-based zygomatic
ethmoidal region and the brain case. In Phaethornis process (Fig. 26B, middle row left).

F ig. 26. Examples of variation in the cranium of hummingbirds. Jugal arch and most of the upper jaw not
shown. (A) Dorsal view. Above, left to right: G lau cis, A n th ra c o th o r a x , E u to x eres; below, left to right: A m a z ilia
and M e ta llu r a . Examples of the genera illustrated are intended to show variations in shape of the supraorbital
margin and adjacent margin of the ectethmoidale that sometimes typify genera or groups of genera. The fron
tal fenestra is found only in P o ly tm u s, A n th ra c o th o r a x , E u la m p is , C h r y so la m p is , and possibly A v o c e ttu la . (B) Left
lateral view. Left to right, top: P h a eth o rn is and H elio d o x a ; middle: A n d ro d o n and E n sifera ; bottom: C h a lc o stig m a
and M e llis u g a . Examples from the genera illustrated were selected to show variations discussed in the text; for
example, A n d ro d o n has a uniquely short and broad-based zygomatic process. Variations in the labeled features
are largely unexplained. Abbreviations: cer. prom. = cerebellar prominence, ect. = ectmethmoidale, fro. fen. =
frontal fenestra, int. sep. = interorbital septum, opt. for. = optic foramen, orb. fon. = orbitocranial fonticulus,
post. pr. = postorbital process, quad = quadratum, sul. m. cuc. = sulcus of cucullaris capitis muscle, sup. mar. =
supraorbital margin, zyg. pr. = zygomatic process.
Mid-dorsally on the cranium, a shallow depres- m. stylohyoideus remains at or slightly anterior to

sionindicatestheoriginofm.stylohyoideus(Fig.4B), the craniofacial hinge.
a muscle that lies between and below the two Interorbital septum and parasphenoidal rostrum.—
hyoid horns. In species with shorter horns, the Lateral expansion and pneumaticity of the inter
depression is about midway on the brain case; in orbital septum, rostral tympanic recess (recessus
those with long horns it is near or anterior to the tympanicus rostralis), and parasphenoidal
craniofacial hinge. Even when the horns extend far rostrum vary within the family (Fig. 27C). In
forward into the nasal or intermediate regions of general, character states of the three variables are
the upper mandible, the anterior limit of origin of highly correlated. Expansion and pneumaticity

F ig. 27. Variation in cranial characters of hummingbirds. The drawings illustrate extreme states of continuous
variation found in several characters, and they do not represent particular species. The significance of the varia
tions is largely unknown. (A) Rostral view of the cranium (right side only) to show a nearly vertical lateral margin
of the ectethmoidale (left) versus one that slopes toward the midline dorsally (right). (B) Semidiagrammatic.
Internal bony structures (oblique hatching) of the cranial cavity (vertical hatching), showing presence or absence
of a bony, caudal wall of the hypophysial recess, as seen through the foramen magnum; dashed line is a ligament.
(C) Ventral view of cranium. Dashed line shows the extent of pneumatic inflation of the parasphenoidal rostrum
found in some species. The occipital foramen is an opening of a previously undescribed vascular tube peculiar to
Trochilidae; the foramen may be absent. This drawing shows the abrupt swelling on the parasphenoidal rostrum
that supports the palatum in hummingbirds, and has been mistaken for basipterygoid processes. (D) Caudal view
of crania showing vascular foramena. In C and D the foramen magnum is solid black. Abbreviations: basicr. =
basicranium, caud. wall = caudal wall of hypophysial recess, cer. prom. = cerebellar prominence, dor. rim = dorsal
rim of foramen magnum, ect. = ectethmoidale, for. ext. occ. v. = foramen of external occipital vein, for. occ. ram. =
foramen of occipital ramus of ophthalmic artery, int. cran. cav. = internal cranial cavity, lat. sw. = lateral swelling
on parasphenoidal rostrum, occ. con. = occipital condyle, occ. for. = occipital foramen of vascular tube, orb. = orbit,
par. ros. = parasphenoidal rostrum, sul. nas. = sulcus of nasolacrimal ducts, zyg. pr. = zygomatic process.
are especially pronounced in Pterophanes, Helian- length might reveal a functional complex related
gelus, Aglaiocercus, Sappho, Lesbia, Ramphomicron, to feeding behavior.
Chalcostigma, and Boissonneaua, and least devel Other conformations of the rostrum may be
oped in Hermits, Florisuga, Androdon, Urochroa, independent of pneumatization. The paras
Heliodoxa, Sternoclyta, Patagona, Eugenes, and phenoidal rostrum typically is flat or slightly
Heliomaster. Regardless of lateromedial breadth, concave ventrally, occupying the entire space
the interorbital septum of hummingbirds is between the pterygoid processes of the vomer.
always complete. Relationships of these vari However, the midsection of the rostrum may
ables to size and orientation of the eyes and bill be narrowed (especially Eutoxeres, Ramphodon,

and some Phaethornis), creating a lateral space tongue and hyoids is accomplished by contrac
between it and the pterygoid processes (Ram- tion of m. branchiomandibularis, which inserts
phodon and Phaethornis). Doryfera, Schistes, and on most or all of the epibranchiale. Measure
Goldmania have a basally broad rostrum that nar ment of the curved epibranchiale can be made
rows rostrally to form a keel. In lateral view, the on cleared and stained specimens by straighten
midventral contour of the mesethmoidale may be ing the fragile bone without danger of damage.
smoothly continuous with that of the parasphe Measurements (in relation to cube root of body
noidal rostrum, or it may angle upward more or weight) of the bill and hyobranchial elements of
less abruptly from the tip of the rostrum toward single specimens of nine species in the USNM
the dorsal bar of the upper jaw. Abrupt angling is cleared-and-stained collection are summarized
extreme in Lafresnaya, Oreotrochilus, Lesbia, Ram- in Table 2 . In this sample the epibranchiales are
phomicron, Metallura, and Chalcostigma. roughly three or more times longer than the com
Foramena and Fenestrae.— The medial orbito bined basihyale and ceratobranchiale. Length of
nasal foramen (foramen orbitonasale mediale), the basihyale is roughly two-thirds that of the
located at the rostral end of the olfactory sulcus ceratobranchiale, and both elements show little
(sulcus n. olfactorius), is double in Hemiprocne, variation in this proportion (Table 2). In addition,
Cypseloides, Hermits, Topazes, Androdon, Colibri, regardless of relative bill length, relative lengths
and Schistes; typically, it is single in other of the basihyale and ceratobranchiale are approx
hummingbirds, but some intermediacy occurs. imately constant, and the relative length of the
Bilaterally on the occiput, the occipital ramus epibranchiale is highly variable among the spe
(ramus occipitalis) of the ophthalmic artery (a. cies of Heliodoxa. Heliodoxa jacula and, especially,
ophthalmica) is associated with one or two fora H. leadbeateri have relatively long epibranchiales,
mena (Fig. 27D) that may be closely, moderately, although relative bill length in the genus is mod
or widely spaced and connected by a roughly hor erate and approximately constant. Measurements
izontal sulcus. Single or closely spaced foramena from a large sample of species would probably
typify Hemiprocne, Cypseloides, Hermits, Polytmus, reveal interesting patterns and adaptations.
and Chrysolampis, whereas widely spaced fora The epibranchiales in most hummingbirds
mena typify Florisuga, Doryfera, many Brilliants extend dorsally along the occiput on either side
and Coquettes, and many Mountain Gems and of the cerebellar prominence and rostrally over
Bees. Moderate separation occurs in Topazes and the frontale, ending short of the craniofacial hinge
Patagona. (Fig. 28). In some, however, the two epibranchiales
Vascular tube.—Apart from its apomorphic sta continue forward along the dorsal surface of the
tus in hummingbirds among Apodiformes, the nasal region (Figs. 28 and 29A) on different sides
vascular tube exhibits topographic variations of of the dorsal bar (symmetry; most Phaethornis),
its foramina on the cranium. An occipital foramen or on the same side (asymmetry; some Phaetho-
(foramen occipitalis), located bilaterally on the rnis, Topaza, Eugenes, Ensifera, Sternoclyta, some
occiput dorsolateral to the foramen magnum Heliodoxa, and Coeligena). The epibranchials were
(Fig. 27C), is found in Hermits, Heliothryx, An- symmetrical in nine species of Phaethornis and one
drodon, Heliactin, Eulampis, Anthracothorax, Chrys of Threnetes. When they extend rostrally beyond
olampis, and Polytmus. When absent, an alternative the nasal region asymmetrically, the horns enter
foramen may occur in the external acoustic me the same bony naris and regain bilateral sym
atus (meatus acusticus externus). Documenta metry anteriorly, within a dorsomedial sheath of
tion, analysis of variation, and function of the the upper mandible (Topaza, Ensifera, Sternoclyta,
vascular tube are beyond the scope of the present and some Heliodoxa; Fig. 29B). Asymmetry of both
study. epibranchials to the right side was modal in nine
species of the Heliodoxa group, but extension of the
H yobranchial A pparatus epibranchials into the nasal region varies within
the Heliodoxa group.
The retracted tongue reaches almost to the tip of Bilateral asymmetry of the nasal skeleton is
the bill. Photographs and published statements an indication of long epibranchiales. Epibran-
(e.g., Davis 1958:33) indicate that many species chiales that enter the bill through the nasal open
are capable of protruding almost the entire tongue ing of one side are associated with depression
beyond the bill tip. Pronounced extension of the of the nasal roof on one side and erosion of the

F ig. 28. Variation in the epibranchiales of hummingbirds. Dorsal view of the cranium and base of upper
jaw, scaled to similar cranial width. The epibranchiales curve ventrally and then rostrally around the cranium
to articulate with the ceratobranchiales below the cranium. In hummingbirds the epibranchiales are the most
variable in length of all hyoid bones, and they are shown here as positioned with the tongue retracted. Upon
contraction of m. branchiomandibularis, the dorsal portions of the epibranchiales seen here move caudally, the
hyoid apparatus is pushed forward, and the tongue is protruded from the bill. Abbreviations: dor. bar = dorsal
bar of upper jaw, epi. = epibranchiale, nas. roof = roof of the nasal region.
Fig . 29. Asymmetry of the epibranchiales in H e lio d o x a lea d b ea teri. (A) Dorsal view of cranium; rostral portion
of upper jaw missing. Arrow shows rostral limit of epibranchiales when the tongue is retracted. The long, paired
epibranchiales pass on one side of the dorsal bar and enter a medial chamber in the connective tissue of the inter
mediate part of the upper mandible. (B) Semi-diagrammatic transverse section of the mandibles and tongue,
showing the intermediate part of the upper mandible containing the epibranchiales. Mandibles are solid black.
(C) Right lateral view of nasal part showing excavated dorsal bar and depressed rostral concha associated with
asymmetry of the epibranchiales (drawing reversed for comparison with A). Abbreviations: dor. bar = dorsal
bar of upper jaw, ect. = ectethmoidale, epi. = epibranchiale, l. mand. = lower mandible, nas. roof = roof of nasal
region, ros. con. = rostral concha, u. mand. = upper mandible, ven. bar = ventral bar of upper jaw.

ventrolateral portion of the dorsal bar on the same

side (Fig. 29C). This asymmetry is found not only in
H. leadbeateri, H. jacula, and H. xanthogonys, but
also in H. schreibersii, H. rubinoides, and H. aure-
scens. Lesser depression of the nasal roof and an
unaltered dorsal bar indicate shorter epibranchi-
als that barely penetrate the nasal opening or do
not reach it, as in H. gularis and H. branickii, re
spectively. Clytolaema has still shorter epibranchi-
als and shows no asymmetry (Heliodoxa imperatrix
and Hylonympha macrocerca were not available).
On the basis of comparison with Urochroa, elon
gation of the epibranchial of Heliodoxa jacula and
its extreme elongation in H. leadbeateri are both
derived conditions within the phylogeny of Helio-
doxa by McGuire et al. (2007). A detailed presen
tation of evolution within the Heliodoxa group is
not possible without inclusion of Clytolaema and
Hylonympha in the analysis.
Vertebrae
Fig . 30. Variation in length of rib processes of cervi

Cervical.—The cervical vertebrae (vertebrae cer-
cal vertebrae in hummingbirds. In Hermits the rib pro
vicalis) are defined as all vertebrae of the neck
cesses are typically shorter than those of Trochilines,
region rostral to the first vertebra attached to as exemplified here by Threnetes leucurus (above) and
the sternum by a complete rib (costae comple- Coeligena wilsoni (below). Abbreviations: caud. zyg. =
tae)—that is, one having both vertebral and ster caudal zygapophysis, rib pr. = rib process, tra. pr. =
nal segments. The cervical vertebrae number 14 transverse process, vert. arch = vertebral arch, vert.
in outgroups and 14 in hummingbirds. Relative body = vertebral body.
lengths of the necks in hummingbirds have not
been measured. In general, Hermits have shorter in Trochilines. Different degrees of fusion can be
cervical costal processes than Trochilinae (Fig. 30) found between vertebrae of the rostral portion of
in relation to the depth of the vertebral body. the synsacrum, and most variation within species
Thoracic.—Free thoracic vertebrae (vertebrae and between closely related species, in numbers
thoracicae liberae) begin with the first connected of free and synsacral vertebrae probably results
to the sternum by a complete rib and end with from presence or absence of fusion of a vertebra
the last that is not fused in any way to the pel into the synsacrum.
vis and synsacrum (Fig. 31). These vertebrae are
characterized by a large, rectangular spinous C ostae
process (processus spinosus) and a prominent
transverse process (processus transversus). They Numbers and polymorphism.— When present, ribs
number 4 in outgroups; 4 in Eutoxeres; 3 in other on the first 12 cervical vertebrae consist of rib
Hermits and in most Mountain Gems, Bees, and processes, whereas the last two cervical vertebrae
Emeralds; and 4 in most Coquettes, Brilliants, (13 and 14) bear articulated vertebral ribs. On
and Patagona. Mangoes are variable, with 3 in vertebra 13 the rib is very short, and it may be
Polytmus, Anthracothorax, Eulampis, Chrysolampis, disarticulated (and lost) as an artifact of skeletal
Colibri, Schistes, Heliothryx, and Androdon, 4 in preparation. The incomplete vertebral rib from
Doryfera, and 4 or 3 in Topazes. Thoracic vertebrae vertebra 14 is longer and spine-like.
of the synsacrum number 3 or 4 in Aegothelidae, True complete ribs (costae completae verae)
Hemiprocnidae and some Apodidae, and 2-5 in of the thorax are composed of two sections: a
other Apodidae. There are 3 (rarely 4) in Hermits vertebral rib (costa vertebralis) articulating with
and 3 or 4 in Trochilines. The number of thorac- the vertebra, and a sternal rib (costa sternalis)
ics (free and fused) is modally 6 in Hermits and 7 articulating syndesmotically with the tip of the

5; Apodini (14 spp.), 5, 4, or bilateral asymmetric

5/4 in Collocalia esculenta); and Cypseloides senex,
6 . Outgroup species typically are sexually mono-
morphic with respect to numbers of true, complete
ribs. In Trochilidae the number of true complete
ribs varies from 4 to 7 pairs. In the present study,
coverage of taxa that include at least one speci
men of each sex is as follows (number of genera
precedes number of species): Hermits, 4/17; Man
goes, 10/14; Brilliants, 12/24; Coquettes, 11/16;
Mountain Gems, 4/8; Bees, 7/11; and Emeralds,
21 /46. Sample sizes were 1 to 13, but most com
monly of 1 to 4 per sex. Modal numbers of true,
complete ribs and some variants within clades are
summarized below.
Hermits.— Both sexes 4; males of some species
either 4 or 5; Eutoxeres: both sexes 5.
Topazes.— Topaza pella: both sexes 5; Florisuga
mellivora: males 6, females 5.
Mangoes.— Both sexes 5 (some species 4 or 5
and others 5 or 6); Florisuga, males 6, females
5; Heliothryx: males 4, females 4.
Brilliants.— Males 6, females typically 5 or 6.
Coquettes.—Males 6, females 6 or 5.
Patagona.— Both sexes 6.
Mountain Gems.— Males 6, females 5 or 6; Pan-
terpe, both sexes 5 or 6.
Bees.— Males 6, females 5 or 6.
Emeralds.—Amazilia group: males 5 or 6, females
F ig. 31. Patterns in hummingbirds of free and syn- 5, a few 6; Other Emeralds: both sexes 5.
sacral thoracic vertebrae, and their association with Hermits, Mangoes, many Coquettes, and the
thoracic ribs. Diagrammatic. The synsacrum (white) Chlorostilbon group of Emeralds probably are mod
may incorporate one or two relatively unmodified ally sexually monomorphic. Presence of 5 both in
thoracic vertebrae (solid black rectangles). Dots on
outgroups and Eutoxeres—the latter, sister to the
the ribs represent articulations with the sternum
remaining Hermits (McGuire et al. 2007, R. L. Zusi
(not shown) and indicate true compound ribs. Ribs
that terminate on other ribs lack dots and represent
unpubl. data)—suggests that the apomorphic state
false compound ribs. The top pattern is common in in Hermits is 4, whereas the presence of 5 in out
Hermits, the middle pattern typifies most Trochilines, groups and Mangoes suggests that 6 or more rep
and the bottom pattern characterizes many Brilliants resents the apomorphic state in most Trochilines.
and Coquettes (Andean Trochilines). Abbreviations: Given sexual dimorphism within a species or
cer. ver. = cervical vertebrae, fr. tho. vert. = free tho clade, the larger number of true, complete ribs
racic vertebrae, syn. = synsacrum, tru. com. rib = true usually occurs in males. An example of this pattern
complete ribs. is Eutoxeres condamini, in which 10 males and 8
females had five pairs, one male had six, and four
vertebral rib and synovially with the sternum. females had four. Similarly, in male Thalurania
Caudally, those sternal ribs that do not reach the furcata, 12 males had six and 1 had five; among
sternum are false complete ribs (costae completae females, 10 had five and 1 had six. When poly
spuriae) in which the tip of the sternal rib abuts morphism occurs in both sexes, individuals with
the preceding sternal rib (Fig. 31). In humming a higher number are usually males, and those
birds false complete ribs number 3 or 2. with a lower number females.
Numbers of true complete ribs in outgroups Functional considerations.—Any attempt to pro
are as follows: Aegothelidae (2 spp.), 3 or 4; duce a functional explanation for the curious pat
Hemiprocnidae (4 spp.), 5; Cypseloidinae (4 spp.), tern of sexual dimorphism in the number of true,

complete ribs should include the main function of exhalation, and high-energy displays (e.g., Pizo
the ribs, which interconnect the vertebral column 2012) that increase the breathing rate. "There is...a
and sternum. Muscles of the rib cage (thorax) synchrony between abdominal muscle activity and
cause the ribs to push the sternum away from the changes in air sac driving pressure, air flow and
the vertebral column or, with help from abdomi sound v o lu m e .. The magnitude of these physical
nal muscles, to draw it toward the vertebrae, thus parameters varies greatly between different types
expanding and compressing posterior air sacs like of vocalization" (Brackenbury 1989:204-205). Thus,
a bellows during breathing (Brackenbury 1982, if singing produces an extra burden on the normal
Fedde 1987, Brown 1999). Although powerful process of exhalation in males, it is likely that inha
flight muscles originate on the sternum and pec lation would also be stressed. At present, there is
toral girdle, the muscles associated with thoracic no experimental support for these speculations on
and abdominal compression and expansion com sexual dimorphism.
prise an essentially independent functional system
(Duncker 1971, Brown 1999). Addition of one true, S t er n u m
complete rib and its associated muscles to the rib
cage probably would significantly increase the Carina.— The lateral profile of the carinal apex and
overall power of the ribs during respiration. the angle of the carinal pillar to the plane of the
Male behaviors that might benefit from such sternal plate are variable (Fig. 32A). The carinal
enhancement are singing, which occurs during apex is usually more extensive in larger species of
F ig. 32. Patterns of variation in sternal characters of hummingbirds. (A) Shape of the carinal apex and inclina
tion of the carinal pillar; left lateral view. Sternae are scaled to similar length, but caudal portions of some ster-
nae are not shown. Above, left to right: H e lio d o x a lea d b e a ter i, F lo ris u g a m elliv o r a , T opaza p ella ; below, left to right:
P a ta g o n a g ig a s , M y r tis fa n n y , M e ta llu r a w illia m i. The species are chosen to exemplify major differences in carinal
shape, but more than one shape may be found within a genus or even within a species. (B) Rostral portion of ster
num in dorsal view showing lateral separation of coracoidal articular facets; scaled to similar sternal width. Left:
C o lib r i s e rr iro s tris ; right: C a m p y lo p te ru s h y p e r y th r u s . Separated facets are common in the genus C a m p y lo p te ru s , a
fact of unknown significance. Abbreviations: car. ap. = carinal apex, car. lim. = dorsal limit of carina, car. pil. =
carinal pillar, cor. fac. = coracoidal articular facet, cran. pr. = craniolateral process, int.-m. lin. = intermuscular
line, med. rid. = medial ridge, st. body = sternal body.

hummingbird, possibly incorporating partial ossi Costal facets.— Bilateral asymmetry in number
fication of the sternoclavicular ligament. Although of sternal articular processes (processus articu-
intraspecific variation is common, a particular laris sternocostalis) involves the rostralmost of
profile of the carinal apex may characterize taxa the false complete ribs, in which the sternal rib
at generic or higher levels (Fig. 32A). A short and abuts the sternal rib of the adjacent true complete
bluntly pointed apex occurs in some Hermits and rib on one side, and abuts the sternal plate on the
Bees; a longer, broadly rounded protrusion typifies other. Additional sternal ribs are added caudally.
Heliothryx, Florisuga, Coeligena, and some Heliodoxa; New sternal facets are small and nearly adjacent
and a sharply pointed profile is found in many to the larger, penultimate facet.
Brilliants, Coquettes, and Mountain Gems and in
some bees and Emeralds. A profile intermediate H umerus
between sharply pointed and broadly rounded
occurs in some species of most major clades. In Proportions.—Apart from the humeral characters
them the apex has a rostral convexity that meets unique to hummingbirds, the humerus exhibits
the upturned ventral margin of the keel at an angle considerable variation in shape within the family
(Topaza, some Mangoes, and some Emeralds). The (Fig. 33A-H). Differences in relative stoutness of
long apex of Patagona and some species of Helio- the entire humeral shaft (Fig. 33C and E vs. D and
doxa is rounded rostrally, concave dorsally, and H) or in different parts of the shaft (Fig. 33G) are
pointed rostrodorsally (canoe-shaped). Species pronounced. Other variation is detailed below.
may be sexually dimorphic in keel shape, as ex Pneumaticity.—Pneumaticity of the bicipital crest
emplified by Trochilus polytmus— males: 10 convex caudoventrally on the humerus is present in Aego-
and angled, two pointed; females: 14 pointed, 2 theles and Apodiformes. Homologous pneumatic-
slightly convex and angled. ity in hummingbirds (Fig. 34A) is manifested by
Coracoidal facets.—The coracoidal facets of at least one pneumatic foramen within a caudal
most swifts and hummingbirds are separated recess along the ventral process. In addition, hum
from the midsagittal plane of the sternum only mingbirds may possess at least one prominent
by the medial ridge, which slopes dorsocaudally pneumatic foramen on the caudodorsal surface of
to form a caudal peak. However, the facets of the humerus between the humeral head and the
some hummingbirds are laterally displaced (Fig. deltopectoral crest. This deltopectoral foramen (Fig.
32B) from the ligamental ridge and connected by 34A) is usually absent from Hermits (except Eu-
a transverse, rostral shelf. Prominent separation toxeres) and present in Trochilines. A third area of
typifies at least Phaeochroa cuvierii, Campylopterus pneumaticity lies just distal to the ventral portion of
rufus, C. hyperythrus, C. largipennis, C. hemileucurus, the capital tuberculum, where the small to moder
Eupetomena macroura, Aglaeactis, and Phlogophi- ately large foramen may be partially hidden by the
lus. Moderate separation is unusual and occurs tuberculum (Fig. 34A). This foramen is commonly
only in a few Emeralds, Brilliants, and Coquettes. found in Hermits, Florisuga, and the Anthracothorax
Although the coracoidal facets on the sternum were group and may be polymorphically present or ab
markedly separated from the midline in Jungornis sent. Another pneumatic foramen may be present
(swift-like birds from the Lower Oligocene; see on the base of the ventral process. It occurs sporadi
Karhu 1988), separation is evidently apomorphic cally and is often polymorphic. Finally, a foramen
within modern Trochilidae. Greater separation just distal to the dorsal portion of the capital tuber
would enlarge the angle between the sternopro- culum may be present—usually small but occasion
coracoidal ligament and the coracoideum and ally prominent, and sometimes closely proximate
increase its mechanical advantage for resisting to the foramena near the deltopectoral crest. All of
lateroventral displacement of the coracoid. Cam- the above foramena may be found in some speci
pylopterus is known for its highly modified, wid mens of Phaethornis, Eutoxeres, and the Anthracotho-
ened rachis of the leading-edge primary feathers, rax group. Additional pneumatic foramina occur
of possible significance "for strengthening of the uniquely near the distal condyles of the humerus
wing during their fast, swift-like gliding among in all species of Boissonneaua, where the patterns are
semi-open vegetation, a common feature of these polymorphic and often bilaterally asymmetrical.
hummingbirds" (Schuchmann 1999:477), but no Processes.—The distal end of the ventral
functional explanation for separation of facets in process (Fig. 34B) may be truncate (or slightly
Campylopterus has been proposed. notched), or markedly notched symmetrically

cap. tub.
EMR tub
pro tub hum
TPB tub
TPB
HERMITS MANGOES
A— notch - ven
- EMR pr — OSS ten
— pro. tub. EMR
TPB ang." pro tub
TPB
E F G H
BRILLIANTS PATAGONA COQUETTES BEES
L NEOTROCHILINES------------------ _____ I
F ig. 33. Variation in shape of the humerus within hummingbirds. Caudal views; scaled to similar humeral
length. (A) P h a eth o rn is . (B) T opaza. (C) F io risu g a . (D) H elio th ry x . (E) P te ro p h a n e s. (F) P a ta g o n a . (G) M e ta llu r a . (H)
M ic r o stilb o n . These examples are chosen to emphasize differences within Trochilidae, but variation also occurs
within each major clade. Pneumatic foramena on the deltopectoral crest and a notch on the ventral process
are most prevalent in Neotrochilines. Nothing is known at present about the functional significance of intrafa
miliar variation. Abbreviations: cap. tub. = capital tubercule, delt. cr. = deltopectoral crest, EMR pr. = process
of extensor metacarpi radialis muscle, hum. sha. = humeral shaft, oss. ten. = ossified tendon (probably of the
subcoracoideus muscle), pn. for. = pneumatic foramen, pro. tub. = pronator tubercle, TPB ang. = angle of tensor
propatagialis brevis muscle, tub. FDP = tubercle of m. flexor digitorum profundus, ven. pr. = ventral process.
or asymmetrically. When asymmetric, the dorsal some Bees is variably elongate distally, probably
arm (crus dorsale fossae) of the ventral process by ossification of the tendon (tendo ossificans) of
is slightly longer than the ventral arm (crus m. subcoracoideus (Fig. 33H).
ventrale). Many species are polymorphic for Although the differences described above are
unnotched versus symmetrically notched; others small and variable, they may be significant because
are polymorphic for symmetrically versus asym the ventral process is strongly developed in
metrically notched. The ventral process is unnot swifts and hummingbirds. In swifts, m. scapu-
ched in outgroups, variable (from unnotched to lohumeralis caudalis inserts along the bicipital
moderately notched) in Hermits, Topazes, Man crest near the base of the ventral process, but
goes, Lophornis and Discosura, some Chlorostilbon in hummingbirds it inserts on the ventral arm
and Cynanthus, and Bees. It is symmetrically of the ventral process, and m. coracobrachia-
notched in Campylopterus, most of the Chlorostilbon lis caudalis inserts on the tip of the dorsal arm
group, and in many other Emeralds, whereas (Fig. 34C). The latter muscle effects supination of
asymmetrical notching is most prevalent in Bril the humerus, and the former effects pronation.
liants, Coquettes, and Patagona. The dorsal arm of Both muscles influence the rotation angle of the

F ig. 34. Processes, pneumatic foramena, and muscle insertions on the humerus of hummingbirds. (A)
Proximocaudal view of right humerus. Pattern of pneumatic foramena common in Hermits (above) and com
mon in Trochilines (below). Additional foramena may accompany these basic patterns. (B) Variation in shape of
the distal end of the ventral process; left humerus, caudal view. Upper left: A n th ra c o th o r a x m a n g o ; upper right:
H elio th ry x a u r ita ; these species show little or no notching on the ventral process and are typical of Hermits,
Mangoes, and Bees. Presence of a distal notch may reflect roughly symmetrical dorsal and ventral arms on the
ventral process, shown in lower left (C h lo r o stilb o n m ellisu g a ) and typical of most Neotrochilines, or asymmetrical
arms, shown in lower right (C o elig en a v io lifer ), typical of many Brilliants and Coquettes. (C) Muscle insertions on
the ventral process and deltopectoral process; caudal view. These muscles influence positions and axial rotation
of the humerus, but the functions of those on the ventral process are not fully understood. Abbreviations: cap.
tub. = capital tuberculum, delt. cr. = deltopectoral crest, dor. arm. = dorsal arm of ventral process, EMR pr. =
process of extensor metacarpal radialis muscle, m. cor. caud. = coracohumeralis caudalis muscle, m. supracor. =
supracoracoideus muscle, m. scap. caud. = scapulohumeralis caudalis muscle, m. subcor. = subcoracoideus
muscle, m. subs. = subscapularis muscle, pn. for. = pneumatic foramen, pro. tub. = pronator tubercle, TPB ang. =
m. tensor propatagialis brevis angle, ven. arm = ventral arm of ventral process, ven. pr. = ventral process.
wing throughout the wing stroke (Cohn 1968). the two walls in Hermits, Topazes, and Mangoes
As antagonists, isolation of the two muscles on (except Colibrì, Schistes, and Doryfera). The roof
different arms may improve efficiency of their re is smaller in Lophornis, Discosura, and Bees, and
spective actions. The roles of m. subcoracoideus absent in Colibri and most other Trochilines.
and m. subscapularis, also inserting distally on In most avian families, the origin of m. extensor
the ventral process, are not well documented. metacarpi radialis (EMR) is from an indis
The deep, pneumatic recess of the ventral pro tinct part of processus supracondylaris dorsa
cess is bounded by dorsal and ventral walls. At lis, located dorsally near the distal end of the
the tip of the process the recess is partly enclosed humeral shaft. By contrast, in Apodidae and Tro-
by a roof (tectum fossae; Fig. 34A) connecting chilidae it is from an enlarged, isolated process

complete humeri are shown in caudal view, scaled to similar humeral length. Numbers represent mean lengths
(mm) of the humeri. Corrugations on the humerus of the species shown are unique within Trochilidae and define
a subgroup (P y g m o rn is group) within P h a eth o rn is . Variation in the processes shown probably serve to identify
each species of the P y g m o rn is group. Abbreviations: cap. tub. = capital tuberculum, corr. = corrugation, delt. cr. =
deltopectoral crest, EMR pr. = process of extensor metacarpi radialis muscle, hum. head = humeral head, pn. for. =
pneumatic foramen, pro.tub. = pronator tubercle, TPB ang. = angle of tensor pronator superficialis muscle, tub.
FDP = tubercle of the flexor digitorum profundus muscle, ven. pr. = ventral process.
(EMR process) positioned more proximally on the or further distad (Urochroa, Pterophanes, Metallura,
shaft. Well developed in hummingbirds (Figs. 15, Aglaeactis, Lafresnaya, Boissonneaua, and Phlogophilus).
33, and 34B), it projects dorsally from the hu It is notably long and narrow in Oreotrochilus, Aglaio-
meral shaft, perpendicular to, or more often cercus, Lesbia, Sappho, and Polyonymus. Sometimes it
angled proximad to, the long axis of the shaft ends bluntly, often with terminal expansions proxi
(Fig. 15). The process is located variously along mally and distally. Rarely, the proximal expansion
the shaft (Fig. 33)—opposite the midpoint (most of the EMR process is extreme (and the distal one
Brilliants, Coquettes, Panterpe, Campylopterus, absent) such that the tip of the process approaches
Chalybura, and Trochilus), proximad (most Hermits, the deltopectoral crest rostrally (many Phaethornis)
Topazes, Mangoes, Patagona, Bees, and Emeralds), or abuts it (P. striigularis; Fig. 35).

The tensor propatagialis, pars brevis muscle of and P. ruber, exhibits a series of roughly parallel
hummingbirds arises from an angular projection ridges separated by grooves (corrugations). The
(henceforth TPB angle) on the dorsal surface of the corrugations extend from the ventral extremity of
humeral shaft (Fig. 33) and is variously positioned the ventral process toward the deltopectoral crest
between the distal end of the humerus and the and follow the course of the tendon of insertion
EMR process. A crest along the dorsal margin of of m. pectoralis major. The corrugations are
the humeral shaft joins the process and angle. The absent from about the mid-longitudinal axis of
TPB angle is located more distally on the shaft in the humerus to the deltopectoral crest (Fig. 35).
Hermits, Heliothryx, Topaza, and Phlogophilus than Numbering three to six, the corrugations are
in other hummingbirds. Usually it projects less dor deeper when more numerous. In the latter case,
sally from the shaft than the EMR process, but in I found that the adjacent surface of the isolated
Coeligena and Heliodoxa the reverse is true. Located tendon of m. pectoralis major was also ridged to
on the ventral surface of the humerus are the prona mesh with the grooves; in species with weak cor
tor tubercle (tubercle of m. pronator superficialis) rugations the isolated tendon was weakly ridged
and FDP tubercle (tubercle of m. flexor digitorum or unridged. Phaethornis longuemareus exhibits the
profundus). These tubercles may be strongly sepa plesiomorphic condition of a humerus and ten
rated (Hermits), moderately separated (Topazes don without corrugations; typically, P. griseogula-
and most Mangoes), or closely spaced (sometimes ris has three ridges, P. striigularis has four or three,
inseparable) in other hummingbirds. and P. atrimentalis, P. stuarti, and P. ruber have six.
Pygmornis group.—Among Hermits the largest The EMR process in P. longuemareus lies in the
genus (Phaethornis) includes a group of species proximal half of the humerus, where it is short,
that differ in their smaller size, several plumage stout, and expanded terminally. It is less stout and
features, and body proportions (Hinkelmann expanded in P. atrimentalis, longer and more slen
1990). They have been treated variously as a der in P. stuarti, slender and tapered in P. ruber, and
separate genus or subgenus (Pygmornis). Hin extremely long and curved proximocraniad in P.
kelmann and Schuchmann (1997) proposed a griseogularis and P. striigularis. In some specimens
subgenus Pygmornis comprising 10 species, but of the latter two species its distal tip reaches the
according to McGuire et al. (2007) these species crista deltopectoralis and forms an arch between
are not monophyletic or sister to all other Phaeth- the process and caput humeri.
ornis. Within subgenus Pygmornis, Hinkelmann Farther distad on the dorsal surface of the hu
and Schuchmann (1997) included a clade of five merus is the TBP angle, which varies from sharply
species, Phaethornis striigularis, P. atrimentalis, angular in P. longuemareus, P. stuarti, and P. atrimen-
P. griseogularis, P. stuarti, and P. ruber, and placed talis to more rounded in P. ruber, P. griseogularis,
P. longuemareus in another clade. Of the five, and P. striigularis. Also variable are the ventrally
P. striigularis, P. atrimentalis, and P. longuemareus situated tuberculum of m. pronator superficiallis
were lumped under P. longuemareus in the clas and a more distal tuberculum FDP. These tubercles
sifications of Peters (1945) and Morony et al. are in closest proximity to each other in P. longue-
(1975). For comparison, I include P. longuemareus mareus; they are in lesser proximity in P. stuarti, P.
in a " Pygmornis group" because of its taxonomic atrimentalis, P. griseogularis, and P. striigularis; and
history, along with the other five species. in least proximity in P. ruber. The tuberculum of
While examining skeletons of Phaethornis, I noted pronator superficialis is peg-like in all but P. ruber,
that features of the humerus of specimens labeled in which it is very short and inconspicuous.
P. longuemareus permitted recognition of three Another variable within the Pygmornis group
groups, each characterized by specimens collected is the pattern of proximal, pneumatic foramina;
from the allopatric distributions of Hinkelmann's P. most Phaethornis have one or more pneumatic
longuemareus, P. atrimentalis, or P. striigularis (Hinkel foramina within the ventral process, but in P. stri-
mann 1990). In addition, the humeral characters of P. igularis additional foramina are usually present
ruber, P. griseogularis, and P. stuarti in specimens from medial to the ventral process and near the delto-
allopatric portions of their respective distributions pectoral crest (Fig. 34). A foramen just distal to the
proved to be diagnostic for each species (Fig. 35). tuberculum capitis may be present or absent in
The proximocranial side of the humerus in five P. longuemareus, P. griseogularis, and P. striigularis.
members of the Pygmornis group, Phaethornis stri- Mean lengths of the humerus, based on samples
igularis, P. atrimentalis, P. griseogularis, P. stuarti, of 1 to 7, differ within the Pygmornis group, with

Phaethornis ruber shortest (3.5 mm), P. griseogularis wingbeat rates during extreme hovering. How
slightly longer (3.7 mm), and the others ranging ever, comparative data on boat posture behavior
between 4.2 and 4.5 mm. and hovering mechanics between species with
Although states of these five characters are and without ridges are not available.
not perfectly correlated among the species of the
Pygmornis group, each species studied here (two Tarsometatarsus
to five specimens per species) has a unique com
bination of states that apparently permit identi The size of the foot (pes) in relation to body size
fication by the humerus alone. The question of varies considerably within Trochilidae. Using
a sister relationship of Phaethornis longuemareus tarsal length divided by coracoidal length to rep
or P. atrimentalis to the recently named P. aetho- resent foot size in relation to body size, I found
pyga (Piacentini et al. 2009) might be answered that foot size in Hermits (except Eutoxeres) and
by presence or absence of corrugations on the Emeralds was small; in Bees small to medium;
humerus of P. aethopyga, and the other charac in Eutoxeres, Panterpe, and most Brilliants and
ters might clarify its relationships within the Coquettes medium; and in Lophornis, Discosura,
Pygmornis group. However, humeri are unavail Chalcostigma, Oreotrochilus, Lesbia, Adelomyia,
able for Phaethornis aethopyga, P. r. rupurumii, and Aglaeactis large (R. L. Zusi unpubl. data).
P. idaliae, P. griseogularis zonura, P. s. striigularis, Species with large feet often cling to a flower or
and P. ruber nigricinctus. Apart from their rel other substrate while feeding, and Oreotrochilus
evance to systematics and taxonomy, these estella is known to roost while clinging to vertical
variables are of interest as a rare case of species- rock surfaces (Carpenter 1976). Among Hermits,
specific diversity of the humerus within closely Eutoxeres is a habitual perch-feeder (Gill 1985).
related species of a genus. As mentioned above, However, many hummingbirds occasionally
determination of species limits in the Pygmornis cling to flowers while feeding (e.g., Pyke 1981,
group is important because, for several decades, Mobbs 1989, Zusi and Hamas 2001), regardless of
three species were lumped under Phaethornis foot size.
longuemareus in museum collections of skeletons,
spirit specimens, and tissue samples, as well as P halanges
in publications on phylogeny, behavior, ecology,
and other subjects. In most hummingbirds the number of phalan
Functional considerations.—In Glaucis and the ges (phalanx) in digits of the foot follows the
smaller Phaethornis, hovering sometimes oc formula 2,3,4,5 for digits I, II, III, and IV, respec
curs with the body axis horizontal and the tail tively. However, some taxa display only four
raised—the so-called "boat" posture (Skutch phalanges in digit IV. The smaller number re
1951, Stiles and Wolf 1979:65-66). This form of sults from fusion of phalanges 3 and 4 (counting
hovering, used in displays, was described for from the base), as shown by adult specimens that
G. hirsutus (Snow 1973a), P. longuemareus (Snow exhibit early stages of fusion between phalanges
1968), P. striigularis saturatus (Skutch 1951), and P. (Fig. 36). Phalanges of a cleaned skeleton may be
ruber (Mobbs 1971, Snow 1973b). It represents ex tightly conjoined but separable after hydration;
treme hovering because, as suggested above, the partially fused but retaining the flexor tubercle
wing is most strongly supinated with the body (tuberculum flexorium) of phalanx 4; fully fused
horizontal. The flattened tendon of insertion of but retaining reduced, tubercular swelling of
m. pectoralis passes over the cranial surface of phalanx 4; or fused with no trace of former troch-
the humerus before inserting on the deltopec- leae of phalanx 4. The length of the fused phalanx
toral crest, and the angle of this passage would roughly equals that of its two progenitors.
become more acute during the upstroke and with Reduction to four phalanges in digit IV appears
increasing supination of the humerus. Pressure of consistently in Hermits (Eutoxeres), Mangoes
the tendon on the humerus is probably greatest at (Schistes and Augastes), Brilliants (Boissonneaua),
the beginning of the downstroke, and especially Coquettes (Discosura and Lophornis), Patagona,
when the humerus is supinated in the boat pos and Mountain Gems (Panterpe), and sporadi
ture. Precise guidance of the tendon near its in cally in various species. By contrast, reduction is
sertion by corrugations as seen in members of the widespread in Emeralds of the Amazilia group
Pygmornis group may improve efficiency at high (Chlorestes through Hylocharis in Appendix 1).

detailed in Appendix 2 and discussed below is

largely individual variation independent of sex,
age, or geographic origin. The following are se
lected examples that exclude sexual dimorphism.
(1) In Hermits the rostral concha has a weakly
developed ventral wing (T-bar); the ventral wing
is either enlarged or lost within Trochilines, in
which both conditions are probably derived. One
stage in its loss retains only a reduced ventral
wing near the midpoint of the concha. Reduction
or complete loss of the wing occurs polymorphi-
cally within some species of Trochilines (e.g.,
Sternoclyta cyanopectus, Heliodoxa aurescens, Damo-
phila julie, and Amazilia tzacatl).
F ig. 36. Fusion in phalanges of the fourth toe of (2) The body of the vomer in dorsal view may
some hummingbirds. Phalanges are numbered, start be anteriorly rounded, angled, or with spicules.
ing at the base. The top figure shows the five pha Rounded and angled are polymorphic in some
langes found in most species. Lower figures show species (e.g., Archilochus colubris); presence or
successive stages in fusion of phalanges 3 and 4 found absence of spicules are polymorphic in others (He-
polymorphically in some species and suggest the evo liodoxa branickii, H. rubinoides, Urosticte benjamini,
lutionary path to a fourth toe of only four phalanges. Ocreatus underwoodii, Amazilia candida, A . amazilia,
The latter state is derived within hummingbirds and
A. tzacatl, Damophila julie, and Basilinna leucotis).
has evolved in parallel repeatedly within the family.
(3) Examples of intraspecific variation in position
Abbreviation: flex. tub. = flexor tuberculum.
of the epibranchiales in relation to the dorsal bar are
Several species in Apodidae also depart from as follows: symmetrical vs. both left (Phaethornis his-
the usual phalangeal formula (2,3,4,5). I found pidus, P. philippii, and P. syrmatophorus); symmetrical
five phalanges in digit IV of two specimens of vs. both right (P. superciliosus); symmetrical vs.
Streptoprocne zonaris (YPM 7572, 8197), and four both on right or left (P. guy); both right vs. both
in another (YPM 7573), that may have resulted left (Coeligena violifer, C . torquata, Ensifera ensifera,
from loss of a phalanx. Zehntner (1890) found Heliodoxa rubinoides, H. branickii, and H. gularis).
developmental reduction of phalanges in Apus (4) Examples of intraspecific polymorphism in
melba (phalangeal formula 2,3,4,5 in 10-day chick presence or absence of the intrapterygoid articu
to 2,3,3,3 in adult) to result from fusion of pha lation are Adelomyia melanogenys (17 of 19 with
langes differing from those of hummingbirds. articulation) and Metallura theresiae (39 of 42 with
Adults of Aeronautes saxitilis also have 2,3,3,3. articulation).
(5) In dorsal view, the supraorbital margin
In traspecific Variation on each side may be V-shaped (sometimes U-
shaped) or W-shaped. These two states are poly
Within a species, variation may be related to morphic in some species. In A. melanogenys, 20
geographic isolation, sexual dimorphism, or age specimens were W, 5 specimens V, and 8 speci
differences. Specimens used in the present study mens intermediate; Archilochus colubris had 16 V,
were of adult size, although some had more 15 W, and two intermediate.
pronounced sutures in the craniofacial region (6 ) Free thoracic vertebrae usually number 3 or
and more slender construction of the skeleton, 4. Polymorphic 3 or 4, and 4 or 5, occur in some
suggesting younger age. Using these criteria, species. I noted instances of 3/4 polymorphism
I compared variation in samples of specimens of of the free thoracic vertebrae in two to six species
apparently younger versus older individuals of each of Hermit, Mangoes, Coquettes, and Emer
a variety of species. The samples included both alds; 3/2 polymorphism occurred in P. guy, and
sexes and were collected within a restricted geo 4/5 in Doryfera ludovicae.
graphic range. In a variety of characters, I found (7) Polymorphism in the number of true, com
the same kinds of character variation in samples plete sternal ribs within each sex is widespread
of both younger and older individuals, and I con within hummingbirds. Examples in the major
clude that most variation (polymorphism) that is clades are as follows: Hermits— males 4/5, 5/6;

females 4/5. Mangoes—males 4/5, 5/6; females (10) The process of m. extensor metacarpus
5/6. Brilliants—males 5/6, 6/7; females 5/6. Co radialis may be sited distally on the humeral shaft
quettes—males 5/6, 6/7; females 5/6. Mountain (outgroups), about midway on the shaft, or proxi
Gems—males 6/7, females 5/6. Bees— males mally on the shaft (most Trochilines). Polymor
5/6, 6/7; females 5/6. Emeralds (Chlorostilbon phism of midway and proximally cited is most
group)— males 5/6; females 4/5, 5/6. Emeralds common in species of Brilliants and Coquettes.
(Amazilia group)— males 5/6; females 5/6. (11) Phalanges of digit IV may number 4 or 5,
(8 ) A foramen may be present or absent just and polymorphism occurs in G. hirsutus, Helio-
distal to the tuberculum capitis. Presence (most doxa aurescens, Heliangelus amethysticollis, Ocreatus
Hermits) and absence (most Trochilines) are underwoodi, Basilinna leucotis, Campylopterus
polymorphic in some species (e.g., Glaucis hirsu- largipennis, and T. polytmus. One specimen each
tus, P. philippii, P. ruber, P striigularis, P. yaruqui, of Colibri delphinae and T. polytmus was bilaterally
Florisuga mellivora, Colibri coruscans, Anthracocorax asymmetrical (4/5).
dominicus, Eulampis jugularis, E. holosericeus, States of characters that are synapomorphic
Chrysolampis mosquitus, Haplophaedia aureliae, for higher-level categories within Trochilidae
Eriocnemisluciani,Aglaeactiscupripennis,Pterophanes may occur as intraspecific variation, variation
cyanoptera, Heliangelus exortis, Ramphomicron among congeners, or differences between genera
microrhynchum, Oreotrochilus estella, M. theresiae, of a clade. As shown in Table 3, character states
and Eupetomena macroura). Separately, a foramen that distinguish Trochilines (+) from Hemiproc-
may be present or absent on the deltopectoral nidae, Apodidae, and most Hermits (-) are also
crest. Presence and absence are sometimes found as intraspecific variation (polymorphism)
polymorphic (e.g., Eutoxeres aquila, G. hirsutus, within one or more genera of Hermits (Table
Phaethornis ruber, and Ramphodon naevius). 3, characters 2 and 3). In character 3, different
(9) Ventrally on the humeral shaft are tubercles of species of Phaethornis show different states (-,
origin for m. pronator superficialis and flexor digi- +, or polymorphic +/-). A character state that
torum profundus. The tubercles may be adjacent, distinguishes Neotrochilines (+) from Hermits,
moderately separate, or distinctly separate. The Topazes, and Mangoes (-) is polymorphic in
states "moderately separate" and "adjacent" are Eutoxeres (character 4) and differs between gen
sometimes polymorphic (e.g., Doryfera ludovicae, F. era within both Topazes and Mangoes (charac
mellivora, Colibri coruscans, Anthrothorax dominicus, ters 4 and 5). Thus, there is strong support for
Eulampis jugularis, Heliothryx auritus, Chlorostilbon the concept that many phenotypic differences at
maugaeus, Cynanthus latirostris, Thalurania furcata, multiple phylogenetic levels had their origins in
Damophila julie, and Trochilus polytmus). species-level variation.
Ta ble 3. Distribution of skeletal characters in higher-order clades of A podiform es and o f Trochilidae, as show n in
Figure 1. N ote high levels of variation in Herm its, Topazes, and M angoes.
Trochilidae
Trochilines
H em iprocnidae
C haracter and A podidae H erm its Topazes M angoes N eotrochilines
1. Fusion of nasal roof w ith nasale ± N A or + + - - -

2. N asal opening transects craniofacial - —a + + +
hinge ±
3. Pneum atic foram en(a) on - , +, + + +
deltopectoral crest ± or ±
4. Rostral concha ossified ± - b + or - c + or - +
5. M edial concha scrolled ± + - + or - + or - +
a Eutoxeres polymorphic +/-.

b Eutoxeres +.
c Topaza -, Florisuga +.

D is c u s s io n additional fossils from the late Miocene might

prove to be informative about polarity.
Apomorphies o f major clades.—In contrast to the Within each of five major clades of Trochili
many skeletal characters that support monophyly dae, individual genera or groups of genera are
of Trochilidae within Apodiformes (Appendix 1), supported as clades by independently evolved
few or none support each major clade within synapomorphies (Table 4).
Trochilidae. The clade of Neotrochilines (Fig. 1) Diversity within major clades.—The following
is only weakly supported by skeletal characters summary reiterates the high level of interspecific
(Table 3), and even the traditional view of Her and intergeneric variation within major hum
mits and Trochilines as sister taxa (Phaethorni- mingbird clades. As noted earlier, each of these
thinae and Trochilinae, respectively) is supported clades contains species of a wide range of body
by only three characters for Trochilinae (Table sizes. Qualitative diversity of the skeleton within
3). The latter dichotomy is contradicted by Hermits is largely between Eutoxeres and all
molecular evidence for Topazes as sister taxon other genera. Eutoxeres differs in having the
to all other hummingbirds (McGuire et al. most strongly decurved bill, bony nasal open
2007). However, developmental change within a ing slit-like caudally, a proportionally short and
Trochiline (Chlorostilbon swainsonii) from holorhi- broad cranium, a spatulate form of the vomeral
nal nares of the nestling to schizorhinal nares of body and lack of a vomeral spine, modally five
the adult, largely achieved by bone resorption, pairs of true thoracic ribs, and four phalanges
is consistent with bony nasal openings that tran in pedal digit IV. Other Hermits display minor
sect the craniofacial hinge as a derived condition variations of the skeleton, most notably the pres
of Trochilines (Table 3). According to Bleiweiss ence of corrugations on the humeral head in the
(1998), divergence of Hermits and Trochilines Pygmornis group of Phaethornis. Especially in
occurred in the Miocene. Inferences about po Glaucis, Threnetes, and Ramphodon, the temporal
larity of morphological characters rely mainly fossa is extensive, its defining crests well devel
on structure of extant outgroups (Hemiprocni- oped, and the postorbital and zygomatic pro
dae and Apodidae) that probably diverged from cesses widely separated. These features reflect
a hummingbird line in the Oligocene. Even if the larger size and strength of the superficial
Eurotrochilus should prove to be the oldest mandibular adductor muscles, and a presumed
known member of the hummingbird clade, its stronger bite— functions that may support
visible character states are not necessarily perti insect gleaning from bark and epiphytes. The two
nent to polarity of modern character states that genera of Topazes differ in form of the rostral and
distinguish Hermits from Trochilines. Eventually, medial concha, ossification of the hypophysial
Table 4. Derived character states of genera or generic groups within major clades of Trochilidae.
Character Genera Major clade
Vomeral body spatulate E u toxeres Hermits

Nuchal crest present R am phodon Hermits
Corrugations on humerus Subset of P h a eth o rn is a Hermits
Four phalanges in digit IV E u toxeres Hermits
A m a z ilia group b Emeralds
Zygomatic process short and broad-based A n d ro d o n Mangoes
Frontal fenestra present A n th ra c o th o ra x group c Mangoes
Rostral concha lacks ventral wing F lorisu g a Topazes
A n th ra c o th o ra x group c Mangoes
A m a z ilia group b Emeralds
Pneumatic foramena distally on humerus B o isson n eau a Brilliants
Ventral groove on ventral wing of rostral L am p orn is, L am p ro la im a Mountain Gems
concha
a Phaethornis atrimentalis, P. striigularis, P. griseogularis, P. ruber, and P. stuarti.

b Chlorestes through Hylocharis in Appendix 1.
c Polytmus through Eulampis in Appendix 1.

wall, symmetry of nasal region, carinal shape, complexes— those of the nasal region, trunk, foot,
and humeral pneumaticity. Mangoes are a highly and syrinx—may constitute other adaptations,
diversified clade showing extremes of varia although morphologies divorced from specific
tion in shape of the caudal rim of the bony nasal adaptation are not ruled out.
opening, structure of the nasal conchae, size of Hummingbirds' specializations for hovering
the rostral mandibular fenestra, craniocaudal po and nectarivory provide them a unique eco-space.
sition of the lateral part of the palatinum, many Within that eco-space, relatively simple changes in
features of the braincase, bill length and shape, bill length and shape almost certainly contribute
relative length of the epibranchiales, shape of the to establishment of hierarchies of coexistence (Col
sternal carina, pattern of humeral pneumatic fo- well 2000, Temeles and Kress 2003, Temeles et al.
ramena, and number of phalanges in pedal digit 2010). On a broader scale, Bleiweiss (1990) has
IV. Brilliants show considerable difference in bill argued that the generalized feeding ecology and
length and shape, size of the rostral mandibu high vagility of Trochilines (as opposed to Her
lar fenestra, features of the cranium and palate, mits) predisposed them to exploit diverse habitats
relative length of the epibranchiales within Helio- and nectar sources, leading to speciation, special
doxa, and number of phalanges in pedal digit IV. ization in feeding, and increased diversity. The use
Within Coquettes there is variation in bill length of clades to represent phylogenetic diversity of
and shape, development of the ventral wing of hummingbird communities in different ecological
the rostral concha, size of the rostral mandibular and biogeographic contexts (Graham et al. 2009)
fenestra, and degree of pneumatic inflation of the may provide a template for future analysis of
cranium. Mountain Gems show some variation in morphological variation and adaptation in hum
the cranium and in number of phalanges of pedal mingbird communities. One difficulty for future
digit IV. Bees exhibit variation in rostral concav analyses is that the named clades of humming
ity of the ectethmoidale and in tendinal ossifica birds are not equivalent in age or diversity.
tion associated with the humeral ventral process.
Variation among Emeralds includes shape of the C onclusions
rostral concha (T-bar versus J-bar), presence or
absence of a vertical lamella, shapes of interor This monograph has identified special problems in
bital margins, and number of phalanges of pedal the morphology of hummingbirds, notably those
digit IV. listed below. Detailed descriptions of kinematics
Parallelism.—As one would expect when con and functional analyses of articulations are key to
siderable diversity exists within major clades of many of these problems. Fortunately, humming
a family, parallelisms occur. Examples among birds are relatively amenable to captivity, and many
hummingbirds, in the context of the McGuire et al. new anatomical methods remain to be applied.
(2007) phylogeny, are shown in Table 5. (1) Functional significance of syringeal structures
Structural adaptation and community ecology.— unique to hummingbirds, requiring observation
Although synapomorphies of the upper jaw, and cinematography of syrinx during vocalization.
palatum, mandibula, hyobranchial apparatus, (2) Functional analysis of holorhinal and schizo-
and wing that distinguish Trochilidae within rhinal prepalatal upper jaws, including measure
Apodiformes probably represent basic adap ment of bending of tip of upper jaw while drinking,
tations for feeding and hovering flight, varia and movement of entire upper jaw when opened
tions within these complexes may represent widely, with special attention to differences be
finer-grade adaptations within Trochilidae. For tween Hermits and Trochilines.
example, observations on bill structure, flower (3) Comparative study of posthatching de
structure, and feeding ecology of captive and velopment of upper jaw in Hermits as well as
free-living birds have engendered and con Trochilines, with special attention to nasale and
firmed hypotheses on ecological causation of craniofacial hinge.
sexual dimorphism and on coadaptation (e.g., (4) Functional anatomy of the jaw articulation
Snow and Snow 1980; Temeles et al. 2000, 2002; in relation to cranial kinesis and streptognathism.
Temeles and Kress 2003), and Stiles (2008) has Precise motions of the quadrate and mandible
explored adaptations of the flight mechanism for with respect to each other would be necessary.
life at higher elevations within major humming Measurement of torsion in the free rami of the
bird clades. Variations in poorly known skeletal mandibula and electromyography of jaw muscles

during cranial kinesis and mandibular strepto-

o o gnathism would be instructive.
& (5) Apparent conflict between developmental
restructuring of prepalatal upper jaw for nectar
transport and the effectiveness of rhynchokinesis
r- U** for bill-tip motion. Measurement of movement
.5 CQ of ventral and dorsal bars during kinesis would
« n-t
be crucial, and elasticity of connective tissue con
necting the two bars should be measured. Any
difference between motion of dorsal and ventral
portions of ventral bar should be determined.
(6 ) Analysis of motion and transmission of
forces throughout pterygopalatine arch and pre
palatal upper jaw during cranial kinesis. Powered
by jaw muscles, the kinetic mechanism consists of
several kinematic chains that include also jugal
arch and mandibula, quadromandibular articula
tion, and associated ligaments.
(7) Measurement of calcium content of bone
& su
o in flexible portions (hinges) of jaws compared to
U Qa adjacent portions.
(8 ) Functional significance of inflation of the cau
dal part of mandibular ramus. Precise description
of jaw muscle insertions and ligaments on species
with different morpholgies of the caudal part of
mandibular ramus are needed. Torsion in the cau
Table 5. Parallel occurrence of selected characters among major clades of Trochilidae.
dal portion of mandibular rami may be a factor.

(9) Further analysis and ecological significance
of jaw mechanisms of Hermits and Trochilines. If
differences between Hermits and Trochilines are
found in the above studies 2-7, field work might
:§ CL 8 reveal correlated differences in uses of mandibles.
o
60 O 0 co i i (10) Mechanism and possible role of mandibu
cT
O S fe u $o 'ts £
Q s ^ lar downbending during insect capture. Measure
s downbending precisely, and determine precise mo
tion of mandibular ramus at jaw articulation during
downbending. Measure torsion in mandibular rami.
(11) Evaluate hypothesis of two hyobranchial
Oh mechanisms, one for tongue lapping and another
e2 for full protrusion of tongue. Observe and mea
sure details of tongue protrusion during feeding
under different levels of nectar volume and avail
ability at feeders and flowers. Electromyography
of intrinsic and extrinsic muscles of the hyobran-
s s < £
w UJ chial apparatus would be important.
(12) Functional and ecological significance
of variation in epibranchial lengths within
TO .s -C Heliodoxa. Measure maximum protrusion of
-0 = §? tongue in species with proportionally different
-8 o> '0
lengths of the epibranchiales. Field studies are
JS p> to o»
.fi 8 X hÒ U needed throughout the range of each species,
0
S * % Oh
2 3 — 1u
O 0J
3Oh 1U!« x concentrating on flower structure and nectar
rS c/5 at
o Oh O 3 Í? 3
O ^3 O m
u 04 Uh Uh Uh reservoirs.

(13) Functional analysis of nasal region and its (24) Posthatching and postfledging developmen
various morphologies. Measure airflow in vari tal changes and rates for all structural complexes
ous parts of the nasal region during breathing and associated behavioral changes related to pa
and singing. Determine location of flower mites rental feeding, nectarivory, tongue protrusion, and
in nasal region of live birds in the field. hovering. For example, is the prokinetic upper jaw
(14) Analysis of influences on cranial shape, of nestling Trochiline hummingbirds especially
including, at least, variation in bill length, eth efficient for wide-mouthed food begging?
moidal region, and overall cranial pneumaticity. In a broader perspective, new techniques for
Size and orientation of eye, and bill length and three-dimensional imaging and measurement of
shape, may be important correlates of cranial anatomical complexes applied to skeletons and
pneumaticity and ectethmoidale shape. spirit specimens of hummingbirds may allow more
(15) Role of neck in special positioning of head rigorous study of angular relationships of cra
during nectarivory and insect capture. Laboratory nium and jaws, eye-size and orientation, lengths
and field observations and slow-motion cinema of hyobranchial elements and tongue, length and
tography during feeding would be needed. functional properties of neck segments, and other
(16) Function of lateral displacement of cora- parameters in taxon-rich comparisons. Such data
coidal facets of sternum in some species. Look for would relate directly to efficiency of access to co
other parameters of shoulder girdle that relate to rollas and nectar, and indirectly to community
coracoidal separation. Field study of Campylop- ecology. Using traditional techniques, these ana
terus might suggest its significance. tomical topics have been explored in other fami
(17) Significance of different numbers of free lies of birds by Marinelli (1928), Boas (1929), Duijm
thoracic vertebrae. Look for functional correlates. (1951), and Zusi (1962), among others.
(18) Functional significance of general trends This monograph documents developmental
and sexual dimorphism in numbers of true com change in the prepalatal upper jaw essential for
plete ribs. Increase sample sizes of specimens efficient nectar eating in hummingbirds. Similarly,
and species measured. Analyze rib function and the tongue develops its terminal, nectar-gather
explore behavioral differences in the sexes that ing lamellae and adult length only after fledging
are related to respiration. (Scharnke 1931a). Although growth of a long bill
(19) Detailed kinematics of shoulder and hume and tongue is constrained within the egg, there is
rus during flight. Precise motions of wing elements, no obvious reason why rotation of the ventral bars
incuding axial rotation, should be determined at could not have occurred before hatching. Growth
each wing joint for different forms of hovering. of the epibranchiales may also be delayed and oc
Determine the relation of capital tuberculum to cur within a short period, but measurements of the
glenoid socket during the wingbeat. hyobranchial elements of known-age fledglings are
(20) Functional significance of notched humeral lacking and the role of the epibranchiales in necta-
ventral process and its associated muscles. In com rivory has not been firmly established. Feeding of
bination with study 16 above, electromyography fledglings by the adult female probably provides
of muscles to ventral process of humerus would the necessary supplemental energy before the nec
be valuable. tar-eating mechanism is maximally efficient:
(21) Function of corrugations on humeral head in
the Pygmornis group of Phaethornis. Determine the When they are flying well, often shortly after the
relation of the insertion tendon of m. pectoralis to fifth day after fledging, the female prolongs the
feeding intervals, teaching the young by loud
corrugations during normal and extreme hovering,
calls to come for food.... Between feeding bouts,
and between species with and without corrugations.
young hummingbirds are often seen to probe at
(22) Functional significance of synostosis of twigs or red parts of l e a v e s . . This exploratory
phalanges in digit IV of the foot. Detailed obser behaviour is maintained throughout adoles
vation of positions of phalanges of all digits dur cence and ultimately leads them to new nectar
ing perching and clinging. Are there functional sources. (Schuchmann 1999:513-514)
differences between the four- and five-phalanx
versions of digit IV? Further comparisons of the developmental rates
(23) Relate functional findings on wing skel of feeding and hovering adaptations are needed,
eton to different parameters of feathered wing, as well as comparisons of changes in behavior
and to different behavioral parameters. and physiology during maturation. Also lacking

is a detailed account of the development of tech Rowland, and P. Ronald measured specimens, and
niques for insect capture by fledglings. B. C. Livezey, S. Hamilton, and L.-A. Hayek helped
The growing fields of developmental physiol with selected morphological analyses. C. Hughes
ogy and genetics have provided valuable insights described and illustrated the wrist of a humming
into mechanisms that produce adult morphologies bird and swift. For their excellent illustrations,
from single cells. In addition, they elucidate the I thank C. Lyons (Figs. 8 , 14A, 24B, 26, 32, and 33),
bases for both morphological stasis and variability D. Roney (Figs. 13, 14C, 16, and 19), and C. Hughes
and promise to reshape our views on adaptation (Figs. 17C and 18). R. L. Zusi drew the remaining
and natural selection (see Badyaev 2011, and figures. B. K. Schmidt converted all illustrations
references therein). Although hummingbirds have and labels to digital form for publication.
not yet been the subjects of such investigations, Over the many years of this study at NMNH, my
even the minimal data on developmental anatomy department chairs W. R. Heyer and G. D. Johnson
offered in the present study elucidate gross aspects showed great patience. Among those with whom
of the origin of unique features of the bill that I had beneficial discussions related to humming
pertain to nectarivory in adult hummingbirds. birds, G. R. Graves, J. V. Remsen, Jr., R. Bleiweiss, E. J.
Ultimately, regardless of the analytical approach Temeles, G. D. Bentz, B. C. Livezey, R. C. Banks, P. F.
applied or the source of data employed, explication Cannell, and T. A. Parker III were especially help
of evolutionary history will benefit from a broadly ful. Support during this study came from awards to
comparative approach. the author from Smithsonian Research Foundation
grants 460137 and 71702123 (1975-1977), NMNH
A cknowledgments Research Awards Program (1979-1980), and
AMNH Collections Study Grant (1996).
First, I thank the curators, collections managers, Finally, G. R. Graves, D. L. Altshuler, and an
field collectors, data managers, and specimen pre- anonymous reviewer were instrumental in improv
parators for their roles in developing scientifically ing the manuscript.
valuable anatomical collections of hummingbirds
in recent decades. The following institutions were L iterature C ited
instrumental in this study (identification of ac
ronyms in Appendix 1): USNM, LSU, AMNH, A ltshuler, D. L., and R. Dudley. 2002. The ecologi
FMNH, UMMZ, UKMNH, MVZ, SDSNH, YPM, cal and evolutionary interface of hummingbird
LACM, ROM, CAS, CMNH, UWBM, DMNH, BC, flight physiology. Journal of Experimental Biology
ANSP, UWZM, MG, IRSNB, and BMNH. Special 205:2325-2336.
thanks go to curators and collection management A ltshuler, D. L., and R. Dudley. 2003. Kinematics of
personnel of NMNH and LSU for their cooperation hovering hummingbird flight along simulated and
in this project and for obtaining critical specimens. natural elevational gradients. Journal of Experi
Others who procured specimens were E. O. Willis, mental Biology 206:3139-3147.
A ltshuler, D. L., R. Dudley, and J. A. M cGuire . 2004.
H. M. F. Alvarenga, M. B. Robbins, C. T. Collins, and
Resolution of a paradox: Hummingbird flight at
A. R. Phillips. My visits to museums were enriched
high elevation does not come without a cost. Pro
by the hospitality of J. V. Remsen, Jr., J. P O'Neil, R. ceedings of the National Academy of Sciences USA
M. Zink, K. I. Warheit, G. Zusi, and J. Nadifi. During 101:17731-17736.
collecting trips to Ecuador, Brazil, and Dominica, I A ltshuler, D. L., K. C. Welch, Jr., B. H. Cho, D. B.
benefited from the assistance of G. D. Bentz, F. Or- Welch , A. F. Lin, W. B. Dickson, and M. H. Dick
tiz-Crespo, L. Zusi, G. R. Graves, and M. J. Hamas. I inson. 2010. Neuromuscular control of wingbeat
thank D. Bridge, M. L. and P. R. Isler, C. Milensky, J. kinematics in Anna's Hummingbirds (C aly p te an n a).
Saucier, J. Farrand, Jr., C. T. Collins, J. J. Becker, T. R. Journal of Experimental Biology 213:2507-2514.
Chesser, and many others for providing specimen A merican Ornithologists' U nion . 1998. Check-list
of North American Birds, 7th ed. American Orni
data, field notes, videos, or literature, and S. Renner,
thologists' Union, Washingon, D.C.
A. Illner, K. Clark, M. Crary, and L. Zusi for criti
A mes, P. L. 1971. The morphology of the syrinx in pas
cal translations from German and Italian. For their serine birds. Peabody Museum of Natural History,
work on special anatomical preparations, I thank H. Bulletin No. 37.
Wimer (histology), H. F. James, M. Rowland, and G. Badyaev, A. V. 2011. How do precise adaptive features arise
R. Zug (cleared and stained specimens), and A. Ross in development? Examples with evolution of context-
(excellent skeleton preparation). H. F. James, M. specific sex ratios and perfect beaks. Auk 128:467-474.

Bang, B. G. 1971. Functional anatomy of the olfactory Bock, W. J. 1964. Kinetics of the avian skull. Journal of
system in 23 orders of birds. Acta Anatomica 79 Morphology 114:1-42.
(Supplement 58):1-76. Bock, W. J. 1999. Functional and evolutionary morphol
Baumel, J. J., A. S. King, J. E. Breazile, H. E. Evans, and ogy of woodpeckers. Ostrich 70:23-31.
J. C. Vanden Berge, Eds. 1993. Handbook of Avian Bock, W. J., and J. Farrand, Jr. 1980. The number of
Anatomy: Nomina Anatomica Avium, 2nd ed. species and genera of recent birds: A contribution
(J. J. Baumel, Ed.). Publications of the Nuttall Orni to comparative systematics. American Museum
thological Club, no. 23. Novitates, no. 2703.
Baumel, J. J., and R. Raikow. 1993. Arthrologia. Pages Böker, H. 1927. Die biologische Anatomie der Flugar
133-187 in Handbook of Avian Anatomy: Nomina ten der Vögel und ihre Phylogenie. Journal für
Anatomica Avium, 2nd ed. (J. J. Baumel, Ed.). Pub Ornithologie 75:304-370.
locations of the Nuttall Ornithological Club, no. 23. Brackenbury, J. H. 1982. The structural basis of voice
Baumel, J. J., and L. W itmer . 1993. Osteologia. Pages production and its relationship to sound charac
45-132 in Handbook of Avian Anatomy: Nomina teristics. Pages 53-73 in Acoustic Communication
Anatomica Avium, 2nd ed. (J. J. Baumel, Ed.). Pub in Birds, vol. 1 (D. E. Kroodsma, E. H. Miller, and
lications of the Nuttall Ornithological Club, no. 23. H. Ouellet, Eds.). Academic Press, New York.
Beddard, F. E. 1886. On the syrinx and other points in Brackenbury, J. H. 1989. Functions of the syrinx and
the anatomy of the Caprimulgidae. Proceedings of the control of sound production. Pages 193-220 in
the Zoological Society of London 11:147-153. Form and Function in Birds, vol. 4 (A. S. King and
Beddard, F. E. 1898. The Structure and Classification of J. McLelland, Eds.). Academic Press, London.
Birds. Longmans, Green, London. Brown, R. E. 1999. Avian respiration: Isolation of ventila
Biewener, A. A., K. P. Dial, and G. E. Goslow, Jr. 1992. Pec- tion and flight? Pages 114-123 in Proceedings of the
toralis muscle force and power output during flight in 22nd International Ornithological Congress (N. J.
the starling. Journal of Experimental Biology 164:1-18. Adams and R. H. Slotow, Eds.). BirdLife South
Blake, C. H. 1939. The flight of hummingbirds. New Africa, Johannesburg.
England Naturalist 3:1-5. Bruderer, B., and E. Weitnauer. 1992. Migrating swifts
Bleiweiss, R. 1990. Ecological causes of clade diver mostly combine several wing beats into bursts of
sity in hummingbirds: A neontological perspective variable length, followed by relatively long gliding
on the generation of diversity. Pages 354-380 in phases. Revue Suisse de Zoologie 79:1190-1200.
Causes of Evolution: A Paleontological Perspective Bühler , P 1970. Schädelmorphologie und Kiefer
(R. M. Ross and W. D. Allmon, Eds.). University of mechanik der Caprimulgidae (Aves). Zeitschrift für
Chicago Press, Chicago, Illinois. Morphologie der Tiere 66:337-399.
Bleiweiss, R. 1998. Tempo and mode of hummingbird Bühler , P 1981. Functional anatomy of the avian jaw
evolution. Biological Journal of the Linnean Society apparatus. Pages 439-468 in Form and Function in
65:63-76. Birds, vol. 2. (A. S. King and J. McLelland, Eds.).
Bleiweiss, R. 2002. Patagial complex evolution in hum Academic Press, London.
mingbirds and swifts (Apodiformes): A molecular Buri, R. O. 1900. Zur Anatomie des Flügels von M ic ro
phylogenetic perspective. Biological Journal of the p u s m elb a und einigen anderen Coracornithes;
Linnean Society 77:211-219. zugleich Beitrag zur Kenntnis der systematischen
Bleiweiss, R., S. L. Hendrickson, M. E. Berres, Y. O. Stellung der Cypselidae. Jenaischen Zeitschrift für
Willis, and E. O. Willis. 2003. Affinities of the Naturwissenschaft 33:361-610.
Saw-billed Hermit (R am phodon naevius) determined Campbell, B., and E. L ack, Eds. 1985. A Dictionary of
by cytochrome-fc sequence data. Wilson Bulletin Birds. Buteo Books, Vermillion, South Dakota.
115:1-10. Cannell , P F. 1986. Syringeal complexity and the ordi
Bleiweiss, R., J. A. W. Kirsch, and J. C. Matheus. 1994. nal relationships of "higher" birds. Ph.D. disserta
DNA-DNA hybridization evidence for subfamily tion, City University of New York.
structure among hummingbirds. Auk 111:8-19. Carpenter, F. L. 1976. Ecology and evolution of an
Bleiweiss, R., J. A. W. Kirsch, and J. C. Matheus. 1997. Andean hummingbird. University of California
DNA hybridization evidence for the principal lin Publications in Zoology 106:1-74.
eages of hummingbirds (Aves: Trochilidae). Molec Chai, P, and R. Dudley. 1995. Limits to vertebrate
ular Biology and Evolution 14:325-343. locomotor energetics suggested by hummingbirds
Boas, J. E. V. 1929. Biologisch-anatomische Studien über hovering in heliox. Nature 377:722-725.
den Hals der Vögel. Det Königlich Danske Viden- Chai, P., and R. Dudley. 1996. Limits to flight energet
skabernes Selskabs Skrifter, Naturvidenskabelig og ics of hummingbirds hovering in hypodense and
Mathematisk Afdeling, Series 9, 1:105-222. hypoxic gas mixtures. Journal of Experimental
Bochenski, Z., and Z. M. B ochenski. 2008. An Old Biology 199:2285-2295.
World hummingbird from the Oligocene: A Chavez-R amirez, F., and M. Dowd. 1992. Arthropod
new fossil from Polish Carpathians. Journal of feeding by two Dominican hummingbird species.
Ornithology 149:211-216. Wilson Bulletin 104:743-747.

Chesser, R. T., R. C. Banks, F. K. Barker, C. Cicero, J. L. the European Starling (S tu rn u s vu lgaris). Journal of
Dunn, A. W. Kratter, I. J. Lovette, P. C. R asmussen, Morphology 207:327-344.
J. V. Remsen, Jr., J. D. Rising, and others. 2012. Fifty- Dickinson, E. c ., Ed. 2003. The Howard and Moore
third supplement to the American Ornithologists' Union Complete Checklist of the Birds of the World, 3rd ed.
Check-list o f N orth A m erican Birds. Auk 129:573-588. Princeton University Press, Princeton, New Jersey.
C hubb, A. L. 2004. Nuclear corroboration of DNA-DNA Duijm , M. 1951. On the head posture in birds and its
hybridization in deep phylogenies of humming relation to some anatomical features. I and II. Ver
birds, swifts, and passerines: The phylogenetic handlungen der Koninklijke Nederlandse Akad
utility of ZENK (II). Molecular Phylogenetics and emie van Wetenschappen (Série C), 54:202-211,
Evolution 30:128-139. 260-271.
Clark, G. A., Jr . 1993. Anatomia Topographica Externa. Duncker, H.-R. 1971. The Lung Air Sac System of
Pages 7-16 in Handbook of Avian Anatomy: Nomina Birds. Springer-Verlag, Berlin
Anatomica Avium, 2nd ed. (J. J. Baumel, Ed.). Pub Dunning, J. B., Jr. 2008. CRC Handbook of Avian Body
lications of the Nuttall Ornithological Club, no. 23. Masses, 2nd ed. CRC Press, Boca Raton, Florida.
C ohn, J. M. W. 1968. The convergent flight mechanism of E lemans, C. P. H., I. L. Y. Spierts, U. K. Müller, J. L.
swifts (Apodi) and hummingbirds (Trochili) (Aves). van L eewen , and F. Goller . 2004. Bird song: Super
Ph.D. dissertation, University of Michigan, Ann Arbor. fast muscles control dove's trill. Nature 431:146.
C ollins, B. G., and D. C. Paton. 1989. Consequences E stades, C. F., M. A. Vukasovic, and J. A. Tomasevic.
of differences in body mass, wing length and leg 2008. Giant Hummingbirds (P a tag on a g ig as) ingest
morphology for nectar-feeding birds. Australian calcium-rich minerals. Wilson Journal of Ornithol
Journal of Ecology 14:269-289. ogy 120:651-653.
C ollins, C. T. 1983. A reinterpretation of pamprodac- E wald, P. W., and W. A. Williams . 1982. Function of
tyly in swifts: A convergent grasping mechanism in the bill and tongue in nectar uptake by humming
vertebrates. Auk 100:735-737. birds. Auk 99:573-576.
C olwell, R. K. 1985. Stowaways on the hummingbird F edde, M. R. 1987. Respiratory muscles. Pages 3-37 in
express. Natural History 7:56-63. Bird Respiration, vol. 1 (T. J. Seller, Ed.). CRC Press,
C olwell, R. K. 2000. Rensch's rule crosses the line: Boca Raton, Florida.
Convergent allometry of sexual size dimorphism in F leischer, R. C., H. F. James, and S. L. Olson. 2008.
hummingbirds and flower mites. American Natu Convergent evolution of Hawaiian and Australo-
ralist 156:495-510. Pacific honeyeaters from distant songbird ances
C olwell, R. K., and S. N aeem . 1993. Life-history patterns tors. Current Biology 18:1927-1931.
of hummingbird flower mites in relation to host F ritsch, E., and K.-L. Schuchmann . 1988. The muscu-
phenology and morphology. Pages 23-44 in Ecology lus splenius capitis of hummingbirds Trochilidae.
and Evolutionary Analysis of Life History Patterns Ibis 130:124-132.
(M. A. Houck, Ed.). Chapman and Hall, New York. Fürbringer, M. 1888. Untersuchungen zur Morpholo
C ory, C. B. 1918. Catalogue of Birds of the Americas, gie und Systematik der Vögel, zugleich ein Beitrage
part 2, no. 1. Field Museum of Natural History, zur Anatomie der Stutz- und Bewegungsorgane,
Publication 197, Zoological Series, vol. 8. vols. 1 and 2. T.J. Van Holkema, Amsterdam.
C racraft, J. 1968. The lacrimal-ectethmoid bone com Gadow, H., and E. Selenka . 1891. Vögel, I Anato
plex in birds: A single character analysis. American mischer Theil. Pages 1-1008 in Dr. H. G. Bronn's
Midland Naturalist 80:316-359. Klassen und Ordnungen des Thier-Reichs, vol. 6.
C racraft, J. 1988. The major clades of birds. Pages C.F. Winter'sche Verlagshandlung, Leipzig.
339-361 in The Phylogeny and Classification of the Garrod, A. H. 1873a. On certain muscles of the thigh of
Tetrapods, vol. 1: Amphibians, Reptiles, Birds (M. J. birds and on their value in classification. Proceedings
Benton, Ed.). Clarendon Press, Oxford. of the Zoological Society of London 1873: 626-644.
Cracraft, J., F. K. Barker, M. J. Braun, J. Harshman, G. J. Garrod, A. H. 1873b. On the value of classification of a
Dyke, J. Feinstein, S. Stanley, A. Cibois, P Schikler, peculiarity in the anterior margin of the nasal bones
P Beresford, and others. 2004. Phylogenetic rela of certain birds. Proceedings of the Zoological Soci
tionships among modern birds (Neornithes): Toward ety of London 1873:33-38.
an avian tree of life. Pages 468-489 in Assembling the Garrod, A. H. 1875. On the form of the trachea in cer
Tree of Life (J. Cracraft and M. J. Donoghue, Eds.). tain species of storks and spoonbills. Proceedings
Oxford University Press, New York. of the Zoological Society of London 1875:297-301.
Davis, T. A. W. 1958. The displays and nests of three for George, W. G. 1971. Foliage-gleaning by Chimney
est hummingbirds of British Guiana. Ibis 100:31-39. Swifts (C h aetu ra p ela g ica ). Auk 88:177.
Dial, K. P 1992. Avian forelimb muscles and nonsteady Gerwin , J. A., and R. M. Z ink . 1989. Phylogenetic pat
flight: Can birds fly without using the muscles in terns in the genus H elio d o x a (Aves: Trochilidae): An
their wings? Auk 109:874-885. allozymic perspective. Wilson Bulletin 101:525-544.
Dial, K. Pv G. E. Goslow, Jr., and F. A. Jenkins, Jr. Gerwin , J. A., and R. M. Z ink . 1998. Phylogenetic pat
1991. The functional anatomy of the shoulder in terns in the Trochilidae. Auk 115:105-118.

Gill , F. B. 1985. Hummingbird flight speeds. Auk Phaethornithinae). Studies on Neotropical Fauna
102:97-101. and Environment 32:142-163.
Gill, F. B., and J. A. Gerwin. 1989. Protein relationships H udson, G. E. 1937. Studies on the muscles of the pel
among hermit hummingbirds. Proceedings of the Acad vic appendage in birds. American Midland Natu
emy of Natural Sciences of Philadelphia 141:409-421. ralist 18:1-108.
Graham, C. H., J. L. Parra, C. Rahbek, and J. A. M cGuire. H uxley, T. H. 1867. On the classification of birds; and on
2009. Phylogenetic structure in tropical hummingbird the taxonomic value of the modification of certain of
communities. Proceedings of the National Academy of the cranial bones observable in that class. Proceedings
Sciences USA 106 (Supplement 2):19673-19678. of the Zoological Society of London 1867:415-472.
Grant, V., and E. J. Temeles . 1992. Foraging ability J ohansson, U. S., T. J. Parsons, M. Irestedt, and P G. P.
of Rufous Hummingbirds on hummingbird flow Ericson. 2001. Clades within the 'higher land
ers and hawkmoth flowers. Proceedings of the birds', evaluated by nuclear DNA sequences. Jour
National Academy of Sciences USA 89:9400-9404. nal for Zoological, Systematic, and Evolutionary
Graves, G. R. 1993. Relic of a lost world: A new spe Research 39:37-51.
cies of sunangel (Trochilidae: H elian g elu s) from Karhu, A. A. 1988. A new family of swift-like birds
"Bogotá." Auk 110:1-8. from the Paleogene of Europe [translated from Rus
Graves, G. R. 2007. Jamaican hummingbirds ingest calcar sian]. Paleontological Journal 3:78-88.
eous grit. Journal of Caribbean Ornithology 20:56-57. Karhu, A. A. 1992. Morphological divergence within
Graves, G. R. 2009. Skeletal correlates of body weight the order Apodiformes as revealed by the structure
in the Black-billed Streamertail (T rochilus scitu lu s) of the humerus. Pages 379-384 in Papers in Avian
of Jamaica. Caribbean Journal of Science 45:69-72. Paleontology Honoring Pierce Brodkorb (K. E.
Graves, G.R., and R.L. Zusi. 1990.Anintergeneric hybrid Campbell, Jr., Ed.). Natural History Museum of Los
hummingbird (H eliod ox a lea d bea teri x H elia n g elu s Angeles County Science Series, no. 36.
a m eth y stico llis) from northern Colombia. Condor Karhu, A. A. 1999. A new genus and species of the
92:754-760. family Jungornithidae (Apodiformes) from the late
Greenewalt, C. H. 1962. Dimensional relationships for Eocene of the northern Caucasus, with comments
flying animals. Smithsonian Miscellaneous Collec on the ancestry of hummingbirds. Pages 207-216 in
tions 144:1-46. Avian Paleontology at the Close of the 20th Cen
Greenewalt, C. H. 1975. The flight of birds. Transac tury: Proceedings of the 4th International Meeting
tions of the American Philosophical Society (New of the Society of Avian Paleontology and Evolution.
Series) 65:5-67. Smithsonian Institution Press, Washington, D. C.
H ackett, S. J., R. T. Kimball, S. Reddy, R. C. K. Bowie, Karhu, A. A. 2001. Convergence in the shoulder joint
E. L. Braun, M. J. Braun, J. L. C hojnowski, W. A. structure of hummingbirds, galliforms and tina-
C ox, K.-L. H an, J. H arshman, and others. 2008. mous. Pages 118-132 in Achievements and Prob
A phylogenetic study of birds reveals their evolu lems of Ornithology of Northern Eurasia on a
tionary history. Science 320:1763-1768. Boundary of Centuries (E. Kurochkin and I. Rak-
H ainsworth , F. R. 1986. Why hummingbirds hover: A chimov, Eds.). Magarif, Kazan, Russia.
commentary. Auk 103:832-833. King, A. S. 1989. Functional anatomy of the syrinx. Pages
H ainsworth , F. R. 1991. Discriminating between for 105-192 in Form and Function in Birds, vol. 4 (A. S.
aging rules and why hummingbirds hover. Animal King and J. McLelland, Eds.). Academic Press, London.
Behaviour 41:902-903. King, A. S. 1993. Apparatus respiratorius (Systema respirato-
H artman, F. A. 1954. Cardiac and pectoral muscles of rium). Pages 257-299 in Handbook of Avian Anatomy:
trochilids. Auk 71:467-469. Nomina Anatomica Avium, 2nd ed. (J. J. Baumel, Ed.).
H artman, F. A. 1961. Locomotor mechanisms of birds. Publications of the Nuttall Ornithological Club, no. 23.
Smithsonian Miscellaneous Collections 143:1-91. Kingsolver, J. G., and T. L. D aniel. 1983. Mechanical
H edrick, T. L., B. C heng, and X. Deng. 2009. Wingbeat determinants of nectar feeding strategy in hum
time and the scaling of passive rotational damping mingbirds: Energetics, tongue morphology, and
in flapping flight. Science 324:252-255. licking behavior. Oecologia 60:214-226.
H enningsson, P, G. R. Spedding, and A. H eden L'H erminier , F. J. 1827. Recherches sur l'appareil ster
strom. 2008. Vortex wake and flight kinematics of nal des oiseaux, considéré sous le double rapport
a swift in cruising flight in a wind tunnel. Journal of de l'ostéologie et de la myologie; suivies d'un essai
Experimental Biology 211:717-730. sur la distribution de cette classe de vertébrés, basée
Hinkelmann, C. 1990. Biogeographie und Systematik sur la considération du sternum et de ses annexes.
tropischer Kolibris (Trochilidae). Pages 25-30 in Cur Mémoires de la Société Linnéenne de Paris 6:3-39.
rent Topics in Avian Biology (R. van den Elzen, K.-L. Linnaeus, C. 1758. Systema Naturae. Tomus 1. Editio
Schuchmann, and K. Schmidt-Koenig, Eds.). Verlag decima. Laurentii Salvii, Holmiae.
Deutschen Ornithologen-Gesellschaft, Stuttgart. Livezey, B. C. 2003. Avian spirit collections: Attitudes,
H inkelmann, C., and K.-L. Schuchmann . 1997. Phy- importance and prospects. Bulletin of the British
logeny of the hermit hummingbirds (Trochilidae: Ornithologists' Club 123A:35-51.

Livezey, B. C., and R. L. Z usi. 2006. Higher-order phy- M cGuire , J. a ., C. C. W itt, D. L. A ltshuler, and J. V.
logeny of modern birds (Theropoda, Aves: Neor- Remsen, Jr . 2007. Phylogenetic systematics and
nithes) based on comparative anatomy. I. Methods biogeography of hummingbirds: Bayesian and
and characters. Bulletin of the Carnegie Museum of maximum likelihood analyses of partitioned data
Natural History, no. 37. and selection of an appropriate partitioning strat
Livezey, B. C., and R. L. Z usi. 2007. Higher-order phy- egy. Systematic Biology 56:837-856.
logeny of modern birds (Theropoda, Aves: Neor- M cGuire, J. A., C. C. Witt, J. V Remsen, Jr., R. Dudley, and
nithes) based on comparative anatomy. II. Analysis D. L. Altshuler. 2009. A higher-level taxonomy for
and discussion. Zoological Journal of the Linnean hummingbirds. Journal of Ornithology 150:155-165.
Society 149:1-95. M eyers, R. A., and R. P. Meyers. 2005. Mandibular
Lorenz, K. 1933. Beobachtetes über das Fliegen der Vögel bowing and mineralization in Brown Pelicans.
und über die Beziehungen der Flügel- und Steuerform Condor 107:445-449.
zur Art des Fluges. Journal für Ornithologie 81:107-236. M iller , R. S. 1985. Why hummingbirds hover. Auk
L ouchart, A., N. Tourment, J. C arrier, T. R oux, 102:722-726.
and C. M ourer-C hauviré. 2007. Hummingbird M obbs, A. J. 1971. Notes on the Reddish Hermit. Avicul
with modern feathering: An exceptionally well- ture Magazine 77:160-163.
preserved Oligocene fossil from southern France. M obbs, A. J. 1979. Methods used by the Trochilidae
Naturwissenschaften 95:171-175. (hummingbirds) when capturing insects. Avicul
L owe, P. R. 1939. On the systematic position of the swifts ture Magazine 85:26-30.
(suborder Cypseli) and hummingbirds (suborder M obbs, A. J. 1989. Hummingbirds. Some lesser known
Trochili), with special reference to their relation to facts. AFA Watchbird 16:26-28.
the order Passeriformes. Transactions of the Zoologi M oller, W. 1930. Über die Schnabel- und Zungen
cal Society of London 24:307-349. mechanik blütenbesuchender Vögel, I: Ein Beitrag
Lucas, F. A. 1891. On the structure of the tongue in zur Biologie des Blumenvogels. Biologia Generalis
humming birds. Proceedings of the U.S. National 6:651-726.
Museum 14:169-172. M oller, W. 1931. Bemerkungen zu Scharnke's Mit
Lucas, F. A. 1895. Additional characters of the Macrop- teilung "Die Nektaraufnahme mit der Kolibri
terygidae. Auk 12:155-157. zunge." Ornithologische Monatsberichte 39:135-138.
Lucas, F. A. 1897. The tongues of birds. Report of the M ontgomerie, R. D. 1984. Nectar extraction by hum
National Museum for 1895:1001-1019. mingbirds: Response to different floral characters.
M anchi, S. S., and R. Sankaran. 2010. Foraging habits Oecologia 63:229-236.
and habitat use by Edible-nest and Glossy swiftlets M ontgomerie, R. D., and C. A. Redsell . 1980. A nest
in the Andaman Islands, India. Wilson Journal of ing hummingbird feeding solely on arthropods.
Ornithology 122:259-272. Condor 82:463-464.
M arinelli, W. 1928. Über den Schädel der Schnepfe. M orioka, H. 1974. Jaw musculature of swifts (Aves,
Palaeobiologica 1:135-160. Apodidae). Bulletin of the National Science
M arshall, M. E. 1906. Studies on avian anatomy. II. Museum, Tokyo 17:1-16.
G eococcy x , B u b o and A eron au tes. Transactions of the M orony, J. J., W. J. Bock, and J. Farrand, Jr . 1975.
Texas Academy of Science 9:19-41. Reference List of the Birds of the World. American
M ayr, G. 2002. Osteological evidence for paraphyly of Museum of Natural History, New York.
the avian order Caprimulgiformes (nightjars and Müller , J. 1878. On certain variations in the vocal
allies). Journal für Ornithologie 143:82-97. organs of the Passeres that have hitherto escaped
M ayr, G. 2003a. A new Eocene swift-like bird with a notice. Clarendon Press, Oxford, United Kingdom.
peculiar feathering. Ibis 145:382-391. N ewton, A., and H. Gadow. 1893-1896. A Dictionary
Mayr, G. 2003b. Phylogeny of early Tertiary swifts and of Birds. Adam and Charles Black, London.
hummingbirds (Aves: Apodiformes). Auk 120:145-151. N itzsch, C. L. 1816. Über die Bewegung des Oberkief
M ayr, G. 2004. Old World fossil record of modern-type ers der Vögel. Deutsches Archiv für die Physiologie
hummingbirds. Science 304:861-864. 2:361-380.
M ayr, G. 2005. The Paleogene fossil record of birds in N itzsch, C. L. 1817. Zweiter Nachtrag zu Nitzsch's Abhan
Europe. Biological Reviews 80:515-542. dlung über die Bewegung des Oberkiefers der Vögel.
M ayr, G. 2007. New specimens of the early Oligocene Deutsches Archiv für die Physiologie 3:384-388.
Old World hummingbird E u rotroch ilu s in ex p ectatu s. N orberg, U. M. 1990. Vertebrate Flight: Mechanics,
Journal of Ornithology 148:105-111. Physiology, Morphology, Ecology and Evolution.
M ayr, G., and D. S. Peters. 1999. On the systematic Springer-Verlag, Berlin.
position of the Middle Eocene swift A eg ia lo rn is szar- O rnelas, J. F. 1994. Serrate tomia: An adaptation for
sk ii Peters 1985 with description of a new swift-like nectar robbing in hummingbirds? Auk 111:703-710.
bird from Messel (Aves, Apodiformes). Neues Jahr Parker, W. K. 1878. On the skull of the aegithognathous
buch für Geologie und Paläontologie, Monatshefte birds. Part II. Transactions of the Zoological Society
1999(5):312-320. of London, vol. 10, part 6:251-314.

Parker, W. K. 1879. On the structure and development of Scharnke, H. 1931b. Die Nektaraufnahme mit der Kolibri
the bird's skull. Part II. Transactions of the Linnean zunge. Ornithologische Monatsberichte 39:22-23.
Society of London, Zoology, series 2, vol. 1:99-154. Schuchmann, K.-L. 1987. First record of the Grey-
Paton, D. C., and B. G. C ollins. 1989. Bills and tongues of chinned Hermit (P h aeth o rn is g riseo g u la ris) west of
nectar-feeding birds: A review of morphology, func the Colombian Andes, with notes on the displays
tion and performance, with intercontinental compari of the species. Wilson Bulletin 99:122-124.
sons. Australian Journal of Ecology 14:473-506. Schuchmann, K.-L. 1992. Neue Beobachtungen am
Peters, J. L. 1945. Check-list of Birds of the World, vol. 5. Zahnschnabelkolibri (A n d rod on a eq u atorialis) in
Harvard University Press, Cambridge, Massachusetts. Südwestkolumbien. Tropische Vögel 13:129-131.
Piacentini, V. de Q., A. A leixo, and L. F. Silveira. 2009. Schuchmann, K.-L. 1999. Family Trochilidae (Hum
Hybrid, subspecies, or species? The validity and mingbirds). Pages 468-535 in Handbook of the Birds
taxonomic status of P h aeth orn is lon g u em areu s aetho- of the World, vol. 5 (J. del Hoyo, A. Elliott, and J. Sar-
p y g a Zimmer, 1950 (Trochilidae). Auk 126:604-612. gatal, Eds.). Lynx Edicions, Barcelona, Spain.
Pizo, M. A. 2012. Lek behavior of the Plovercrest (Steph- Sclater, P L. 1865. Notes on the genera and species of
a n o x is lalan d i , Trochilidae). Wilson Journal of Orni Cypselidae. Proceedings of the Zoological Society
thology 124:106-112. of London 1865:593-617.
Price, J. J., K. P. Johnson, S. E. Bush, and D. H. Sclater, P L., Ed. 1867. Nitzsch's Pterylography. [Trans
Clayton. 2005. Phylogenetic relationships of the lated from the German.] Robert Hardwicke, London.
Papuan Swiftlet A ero d ra m u s p ap u en sis and implica Shufeldt, R. W. 1885. Contribution to the comparative
tions for the evolution of avian echolocation. Ibis osteology of the Trochilidae, Caprimulgidae, and
147:790-796. Cypselidae. Proceedings of the Zoological Society
Prum, R. O. 1990. A test of the monophyly of the mana- of London 1885:886-915.
kins (Pipridae) and of the cotingas (Cotingidae) based Sibley, C. G., and J. E. A hlquist. 1972. A comparative
on morphology. Occasional Papers of the Museum of study of the egg white proteins of non-passerine
Zoology, University of Michigan, no. 723. birds. Bulletin No. 39, Peabody Museum of Natural
Pyke, G. H. 1981. Why hummingbirds hover and honey- History, Yale University.
eaters perch. Animal Behaviour 29:861-867. Sibley, C. G., and J. E. A hlquist. 1990. Phylogeny and
Remsen, J. V, Jr., C. D. Cadena, A. Jaramillo, M. N ores, Classification of Birds: A Study in Molecular Evolu
J. F. Pacheco, J. Pérez-E man, M. B. Robbins, F. G. tion. Yale University Press, New Haven, Connecticut.
Stiles, D. F. Stotz, and K. J. Zimmer . 2007. A clas Simonetta, A. 1967. Cinesi e morfologia del cranio negli
sification of the bird species of South America. Ameri Uccelli non passeriformi. Studio su varie tendenze
can Ornithologists' Union. Part 4. Available at www. evolutive. Part II. Striges, Caprimulgiformes ed
museum.lsu.edu / ~Remsen/ SACCBaseline04.html. Apodiformes. Archivio Zoologico Italiano 52:1-36.
Remsen, J. V., Jr., F. G. Stiles, and P. E. Scott. 1986. Skutch, A. F. 1951. Life history of Longuemare's Her
Frequency of arthropods in stomachs of tropical mit hummingbird. Ibis 93:180-195.
hummingbirds. Auk 103:436-441. Snow, B. K. 1973a. Social organization of the Hairy Her
Richardson, F. 1972. Accessory pygostyle bones of Fal- mit G lau cis h irsu ta. Ardea 61:94-105.
conidae. Condor 74:350-351. Snow, B. K. 1973b. The behavior and ecology of Hermit
Rico-Guevara, A., and M. A. Rubega. 2011. The hum hummingbirds in the Kanaku Mountains, Guyana.
mingbird tongue is a fluid trap, not a capillary tube. Wilson Bulletin 85:163-177.
Proceedings of the National Academy of Sciences Snow, B. K. 1974. Lek behaviour and breeding of Guy's Her
USA 108:9357-9360. mit hummingbird P haethornis guy. Ibis 116:278-297.
Roy, M. S., J. C. Torres-Mura, and F. Hertel. 1998. Evolu Snow, D. W. 1968. The singing assemblies of Little Her
tion and history of hummingbirds (Aves: Trochilidae) mits. Living Bird 7:47-55.
from the Juan Fernandez Islands, Chile. Ibis 140:265-273. Snow, D. W., and B. K. Snow. 1980. Relationships
Rydzewski, W. 1935. Badania nad notarium u ptakow. between hummingbirds and flowers in the Andes
Études sur le notarium chez les Oiseaux. Acta Orni- of Colombia. Bulletin of the British Museum (Natu
thologica Musei Zoologici Polonici 1:403-427. ral History), Zoology Series 38(2):105-139.
Savile, D. B. O. 1950. The flight mechanism of swifts Stanislaus, M. 1937. Untersuchungen an der Kolibri
and hummingbirds. Auk 67:499-504. lunge. Zeitschrift für Morphologie und Ökologie
Sazima, I., S. Buzato, and M. Sazima. 1995. The Saw-billed der Tiere 33:261-289.
Hermit R am phodon naevius and its flowers in southeast Steinbacher, G. 1935a. Der Trinkakt der Kolibris. Orni
ern Brazil. Journal für Ornithologie 136:195-206. thologische Monatsberichte 43:11-15.
Scharnke, H. 1930. Ueber den Bau der Kolibrizunge. Steinbacher, G. 1935b. Funktionell-anatomische Unter
Ornithologische Monatsberichte 38:150-151. suchungen an Vogelfüßen mit Wendezehen und
Scharnke, H. 1931a. Beiträge zur Morphologie und Rückzehen. Journal für Ornithologie 83:214-282.
Entwicklungsgeschichte der Zunge der Trochili- Stiles, F. G. 1995. Behavioral, ecological and morphologi
dae, Meliphagidae und Picidae. Journal für Orni cal correlates of foraging for arthropods by the hum
thologie 4:425-491. mingbirds of a tropical wet forest. Condor 97:853-878.

Stiles, F. G. 2008. Ecomorphology and phylogeny of Warrick, D. R., B. W. Tobalske, and D. R. Powers.
hummingbirds: Divergence and convergence in 2005. Aerodynamics of the hovering hummingbird.
adaptations to high elevations. Ornitologia Neo Nature 435:1094-1097.
tropical 19 (Supplement):511-519. Warrick, D. R., B. W. Tobalske, and D. R. Powers.
Stiles, F. G., and L. L. Wolf. 1979. Ecology and evolu 2009. Lift production in the hovering humming
tion of lek mating behavior in the Long-tailed Hermit bird. Proceedings of the Royal Society of London,
hummingbird. Ornithological Monographs, no. 27. Series B 276:3747-3752.
Stolpe, M., and K. Z immer . 1939. Der Schwirrflug des Weymouth, R. D., R. C. Lasiewski, and A. J. Berger.
Kolibri im Zeitlupenfilm. Journal für Ornithologie 1964. The tongue apparatus in hummingbirds. Acta
87:136-155. Anatomica 58:252-270.
Stresemann, E., and K. Z immer. 1932. Ueber die Fre W NET-N ature. 2010. Hummingbirds: Magic in the
quenz des Flügelschlages beim Schwirrflug der Koli Air. [DVD.] Questar, Chicago, Illinois.
bris. Ornithologische Monatsberichte 40:129-133. W olf, L. L., and F. R. H ainsworth. 1977. Temporal
Suarez, R. K. 1992. Hummingbird flight: Sustaining the patterning of feeding by hummingbirds. Animal
highest mass-specific metabolic rates among verte Behaviour 25:976-989.
brates. Experientia 48:565-570. W ood, D. S., and G. D. Schnell . 1986. Revised World
Sutton, F. G. 1927. Roosting Chimney Swifts. Bird Lore Inventory of Avian Skeletal Specimens, 1986.
29:264-265. American Ornithologists' Union, Washington, D.C.
Sy, M. 1936. Funktionell-anatomische Untersuchungen Yanega, G. M., and M. A. Rubega. 2004. Hummingbird
am Vogelflügel. Journal für Ornithologie 84:199-296. jaw bends to aid insect capture. Nature 428:615.
Taylor, P. M. 1972. Hovering behavior by House Y oung, A. M. 1971. Foraging for insects by a tropical
Finches. Condor 74:219-221. hummingbird. Condor 73:36-45.
Temeles, E. J., and W. J. Kress. 2003. Adaptation in a Z ehntner, L. 1890. On the development of the feet of
plant-hummingbird association. Science 300:630-633. C y p selu s m elba. Ibis 6:196-200.
Temeles, E. J., Y. B. L inhart, M. Masonjones, and H. D. Zusi, R. L. 1962. Structural Adaptations of the Head and
Masonjones. 2002. The role of flower width in Neck in the Black Skimmer R yn chops n igra Linnaeus.
hummingbird bill length-flower length relation Publications of the Nuttall Ornithological Club, no. 3.
ships. Biotropica 34:68-80. Z usi, R. L. 1967. The role of the depressor mandibulae
Temeles, E. J., J. S. M iller, and J. L. Rifkin . 2010. Evolu muscle in kinesis of the avian skull. Proceedings of
tion of sexual dimorphism in bill size and shape of the U.S. National Museum 123:1-28.
hermit hummingbirds (Phaethornithinae): A role for Z usi, R. L. 1984. A functional and evolutionary analysis
ecological causation. Philosophical Transactions of of rhynchokinesis in birds. Smithsonian Contribu
the Royal Society of London, Series B 365:1053-1063. tions to Zoology, no. 395.
Temeles, E. J., I. L. Pan, J. L. Brennan, and J. N. H orwitt. Z usi, R. L., and G. D. Bentz. 1982. Variation of a mus
2000. Evidence for ecological causation of sexual cle in hummingbirds and swifts and its systematic
dimorphism in a hummingbird. Science 289:441-443. implications. Proceedings of the Biological Society
Tidman, R. [photographer]. 2007. Bird photograph of the of Washington 95:412-420.
year 2007 [A pus swift, p. 489]. British Birds 100:455-516. Z usi, R. L., and G. D. Bentz. 1984. Myology of the
Tobalske, B. W., D. L. A ltshuler, and D. R. Powers. Purple-throated Carib (E u la m p is ju g u la ris ) and
2004. Take-off mechanics in hummingbirds (Trochili- other hummingbirds (Aves: Trochilidae). Smithso
dae). Journal of Experimental Biology 207:1345-1352. nian Contributions to Zoology, no. 385.
Tobalske, B. W., A. A. Biewener , D. R. Warrick, T. L. Z usi, R. L., and F. B. Gill . 2009. The marvelous tail of
H edrick, and D. R. Powers. 2010. Effects of flight L od d ig esia m ira b ilis (Trochilidae). Auk 126:590-603.
speed upon muscle activity in hummingbirds. Zusi, R. L., and M. J. H amas. 2001. Birds and bats as poten
Journal of Experimental Biology 213:2515-2523. tial pollinators of three species of M arcgravia lianas on
Tobalske, B. W., D. R. Warrick, C. J. Clark, D. R. Pow Dominica. Caribbean Journal of Science 37:274-278.
ers, T. L. H edrick, G. A. Hyder, and A. A. Biewener. Z usi, R. L., and B. C. Livezey. 2006. Variation in the os
2007. Three-dimensional kinematics of hummingbird palatinum and its structural relation to the pala
flight. Journal of Experimental Biology 210:2368-2382. tum osseum of birds (Aves). Annals of Carnegie
Vanden Berge, J. C., and G. A. Z weers. 1993. Myolo- Museum 75:137-180.
gia. Pages 189-247 in Handbook of Avian Anatomy: Z usi, R. L., and K. I. Warheit. 1992. On the evolution
Nomina Anatomica Avium, 2nd ed. (J. J. Baumel, Ed.). of intraramal mandibular joints in pseudodontorns
Publications of the Nuttall Ornithological Club, no. 23. (Aves: Odontopterygia). Pages 351-360 in Papers in
Vazquez, R. J. 1992. Functional osteology of the avian Avian Paleontology Honoring Pierce Brodkorb (K. E.
wrist and the evolution of flapping flight. Journal Campbell, Jr., Ed.). Natural History Museum of Los
of Morphology 211:259-268. Angeles County Science Series, no. 36.
Videler , J. J., E. J. Stamhuis, and G. D. E. Povel. Z usi, R. L., D. S. Wood, and M. A. Jenkinson. 1982.
2004. Leading-edge vortex lifts swifts. Science Remarks on a world-wide inventory of avian ana
306:1960-1962. tomical specimens. Auk 99:740-757.

A ppen d ix i
Taxa Studied , C ollection Sources , and Spec im en N umbers
The species of hummingbirds and outgroups studied for this monograph are listed below, grouped
by the major trochilid clades recognized by McGuire et al. (2007). Order of the species follows Remsen
et al. (2007) and American Ornithologists' Union (1998), except where genera are clustered to reflect
similarity in anatomical characters (Anthracothorax group: Polytmus through Eulampis; Amazilia group:
Chlorestes through Hylocharis). All species of a major clade are grouped together. Reference numbers
and acronyms of source collections for anatomical specimens are as follows:
1. —USNM (National Museum of Natural History; Washington, D.C.)
2. —LSU (Lousiana State University Museum of Natural History; Baton Rouge)
3. —AMNH (American Museum of Natural History; New York)
4. —FMNH (Field Museum of Natural History; Chicago)
5. —UMMZ (University of Michigan Museum of Natural History; Ann Arbor)
6 . —UKMNH (University of Kansas Museum of Natural History; Lawrence)
7. —MVZ (Museum of Vertebrate Zoology, University of California; Berkeley)
8 . —SDSNH (San Diego Society of Natural History)
9. —YPM (Yale Peabody Museum; New Haven)
10. —LACM (Los Angeles County Museum)
11. — ROM (Royal Ontario Museum; Toronto)
12. —CAS (California Academy of Sciences; San Francisco)
13. —CMNH (Carnegie Museum of Natural History; Pittsburgh)
14. —IRSNB (Institut Royal des Sciences Naturelles de Belgique)
15. —UWBM (University of Washington Burke Museum; Seattle)
16. — DMNH (Delaware Museum of Natural History; Wilmington)
17. — BC (Pierce Brodkorb collection, University of Florida; Gainesville)
18. —MG (Museu Paraense Emelio Goeldi; Belem, Brazil)
19. —ANSP (Academy of Natural Science of Philadelphia)
20. —UWZM (University of Wisconsin Zoological Museum; Madison)
21. — BMNH (Natural History Museum; Tring, UK)
In the species list below, numbers following "S" (skeleton) identify the numbered collections, listed above,
from which skeletal data were obtained. Numbers following "A " (alcohol or spirit specimen) similarly
identify collections rather than specimens. In both cases, museum numbers of specimens examined for
multiple characters are enclosed in parentheses, following the collection number. A subset of these species,
identified by inclusion of a capitalized species acronym, was used in the frequency matrix (Appendix 2).
Museum numbers of specimens examined for only a few selected characters are not given here. Asterisks
indicate species included in the molecular phylogeny of McGuire et al. (2007).
a e g o t h e l id a e
Aegotheles insignis (Feline Owlet-nightjar) AEGOCRIS. S: 9 (6906).

A. crinifrons (Moluccan Owlet-nightjar). S: 1.
A. albertisi (Mountain Owlet-nightjar). S: 9 (6904-5).
A. cristatus (Australian Owlet-nightjar). S: 1 (560816, 612637, 612708, 620228); 4 (337190); 7 (143441,
149017). A: 1 (542627).
h e m ip r o c n id a e
Hemiprocne coronata (Crested Treeswift). S: 1 (320840).

H. longipennis (Gray-rumped Treeswift). S: 1.
H. comata (Whiskered Treeswift) HEMICOMA. S: 1 (488343, 488940); 9. A: 1 (510349).
H. mystacea (Moustached Treeswift). S: 1 (558294, 560829); 9 (7039, 7040); 22.

APODIDAE
Cypseloides niger (Black Swift) CYPSNIGE. S: 1 (290999, 555770). A: 1 (511010).

C. phelpsi (Tepui Swift). S: 1.
C. senex (Great Dusky Swift). S: 9.
Streptoprocne rutila (Chestnut-collared Swift). S: 1 (614122); 12.
S. zonaris (White-collared Swift). S: 1 (614120, 490031); 4; 9; 12 (71845-7).
S. semicollaris (White-naped Swift). S: 1; 12 (62883, 63221). A: 1 (512823).
Collocalia esculenta (Glossy Swiftlet). S: 1. A: 1 (506737).
C. troglodytes (Pygmy Swiftlet). S: 1.
Aerodramus francicus (Mascarene Swiftlet). S: 1.
A. spodiopygius (White-rumped Swiftlet). S: 1.
Hirundapus caudacutus (White-throated Needletail). S: 1.
Chaetura spinicaudus (Band-rumped Swift). S: 1.
C. vauxi (Vaux's Swift). S: 12 (42764, 70803, 71851).
C. pelagica (Chimney Swift). S: 1 (431936, 492655); 12 (71663). A: 1 (512808).
Aeronautes saxatalis (White-throated Swift). S: 1; 8 .
Tachornis phoenicobia (Antillean Palm Swift). S: 1.
T. squamata (Fork-tailed Palm Swift). S: 1.
Cypsiurus parvus (African Palm Swift). S: 1.
Apus apus (Common Swift). S: 1.
A. pallidus (Pallid Swift) APUSPALL. S: 1 (582349, 582352-4, 582357). A: 1 (540245).
A. caffer (White-rumped Swift). S: 1.
A. affinis (Little Swift). A: 1.
t r o c h il id a e
h e r m it s
Eutoxeres aquila*+ (White-tipped Sicklebill) EUTOAQUI. S: 1 (428580, 430611, 432173, 500607, 560020,
613297); 2 (86388, 89732); 3 (6078). A: 1 (510579); 2 (117911).
E. condamini* (Buff-tailed Sicklebill). S: 2 (74844, 79757, 118197); 6 (80543); 8 (37585). A: 1 (511929,
512283).
Ramphodon naevius+ (Saw-billed Hermit) RAMPNAEV. S: 1 (562754, 562759, 612046-9). A: 1.
Glaucis aeneus* (Bronzy Hermit). S: 1 (612305); 2 (48563, 50745, 77731, 77733).
G. hirsutus*+ (Rufous-breasted Hermit) GLAUHIRS. S: 1 (344138-9, 492298, 492346, 500586, 555682
3, 562547, 562735); 2 (70194); 9. A: 1 (641471).
Threnetes ruckeri* (Band-tailed Barbthroat). S: 1 (500583, 500585, 611575, 611582-3, 611586, 611588,
612317, 613372, 613377); 2. A:1 (510573).
T. leucurus* (Pale-tailed Barbthroat) THRELEUC. S: 1 (492278-9, 492327, 429378-9, 500500, 560023,
560042); 2; 9 (8064).
Phaethornis squalidus (Dusky-throated Hermit). S: 1 (612040).
P. longuemareus (Little Hermit). S: 1 (560160-1, 562500-1); 5 (156545, 158230).
P. atrimentalis* (Black-throated Hermit). S: 2 (75536, 86386, 106988, 111171).
P. striigularis (Stripe-throated Hermit). S: 1 (430590, 430942, 490208, 612310, 613382-4); 2 (31864,
108740); 4 (337121); 5 (153097); 6 (29235); 7 (156637).
P griseogularis* (Gray-chinned Hermit). S: 3 (18143); 11 (114822). A: 2 (91476).
P. ruber* (Reddish Hermit) PHAERUBE. S: 1 (345257-8, 562453, 562757); 2 (101262-3, 131463-4); 3:
(19420, 19421); 4 (320687). A: (616329, 641470).
P stuarti (White-browed Hermit). S: 2 (70199, 101264).
P subochraceus (Buff-bellied Hermit). S: 2 (125716-7); 4 (334395).
P. augusti* (Sooty-capped Hermit). S: 1 (344553); 11 (128034).
P. pretrei (Planalto Hermit). S: 1 (202037, 562755, 612041); 2 (125715).

P eurynome (Scale-throated Hermit). S: 1 (555946-7, 556425-6, 558793).

P anthophilus* (Pale-bellied Hermit). S: 16 (61817, 62990).
P. hispidus* (White-bearded Hermit). S: 2 (111159, 111161, 121004); 5 (200598).
P yaruqui* (White-whiskered Hermit) PHAEYARU. S: 1 (492395-6, 500467, 610457); 2 (68728, 68731).
A: 1 (505460).
P guy* (Green Hermit). S: 1 (560018, 562498-9, 613288 613295); 2 (63180, 86691, 106984, 118182).
P syrmatophorus* (Tawny-bellied Hermit). S: 2 (89424, 89727, 97462); 3 (8232).
P. koepckeae* (Koepcke's Hermit). S: 2 (118190, 118192); 4 (320664-5).
P philippii* (Needle-billed Hermit). S: 2 (93875, 118335); 3 (10241-2). A: 2 (131777).
P bourcieri* (Straight-billed Hermit). S: 2 (111162-3); 3 (18001); 4 (318733).
P longirostris* (Long-billed Hermit). S: 1 (500581, 500584, 612308-9).
P superciliosus (Long-tailed Hermit) PHAESUPE. S: 1 (492254, 492314, 492336, 562441, 562444-6,
621397). A: 1.
P. malaris* (Great-billed Hermit). S: 2 (111139, 111149, 125710-1).
to pa zes
Topaza pella* (Crimson Topaz) TOPAPELL. S: 11 (107531, 112538). A: 1 (505574).

T. pyra (Fiery Topaz). S: 4 (318845). A: 1 (505573).
Florisuga mellivora* (White-necked Jacobin) FLORMELL. S: 1 (344142-3, 430918, 501331, 554690,
611569); 2 (50750); 9 (7921-3). A: 1 (505502).
F. fusca (Black Jacobin) FLORFUSC. S: 1 (552560, 562760); 4 (105686); 14 (37763).
m an go es
Doryfera ludovicae* (Green-fronted Lancebill) DORYLUDO. S: 1 (491584); 2 (63176, 64840, 64925,

106949). A: 1 (511956, 512143).
D. johannae* (Blue-fronted Lancebill). S: 2 (89714-5, 118178-9).
Schistes geoffroyi* (Wedge-billed Hummingbird) SCHIGEOF. S: 1 (560034); 2 (68832, 83979, 86390,
89850); 4 (291776). A: 2 (98030).
Augastes lumachella (Hooded Visorbearer). S: 8 (155178); 10.
Colibri delphinae* (Brown Violetear). S: 1 (344144, 428699, 428728); 2 (50763, 118204). A: 1 (505506).
C. thalassinus* (Green Violetear). S: 2 (64844, 70203, 81209); 8 (37780).
C. coruscans* (Sparkling Violetear) COLICORU. S: 1 (428732, 428764, 428847, 559970); 2; 8 (36296);
10 (89178). A: 1 (505505).
C. serrirostris (White-vented Violetear). S: 7 (155174).
Androdon aequatorialis* (Tooth-billed Hummingbird) ANDRAEQU. S: 2 (104613); 16 (57988, 57990).
A: 16 (63070).
Heliactin bilophus* (Horned Sungem) HELIBILO. A: 18 (4214).
Heliothryx auritus (Black-eared Fairy) HELIAURI. S: 1 (344145); 4 (315397); 6 (71534); 9 (7612, 8288);
11 (125774-5). A: 1 (541604).
H. barroti* (Purple-crowned Fairy). S: 2; 5.
Polytmus guainumbi* (White-tailed Goldenthroat) POLYGUAI. S: 2 (125744); 4 (289178, 334406); 11
(109532). A: 1 (505527).
P. milleri (Tepui Goldenthroat). S: 3.
P theresiae* (Green-tailed Goldenthroat). S: 5 (156141); 6 (34841). A: 18 (3342).
Chrysolampis mosquitus* (Ruby-topaz Hummingbird) CHRYMOSQ. S: 1 (555695); 13: (8484); 4
(105393, 105395). A: 1 (318125).
Anthracothorax viridigula (Green-throated Mango). S: 1 (345259, 345260); 4 (104251-2). A: 13 (1448).
A. prevostii (Green-breasted Mango). S: 2 (31866); 11 (112891).
A. nigricollis* (Black-throated Mango). S: 1 (555686-7, 555695, 562502); 2 (64994); 6 (34825).
A. dominicus (Antillean Mango) ANTHDOMI. S: 1 (501714, 501755, 501760, 501851, 501857, 501901,
554619, 555779, 555783, 555785-6). A: 1 (506174).
A. viridis (Green Mango). S: 1 (501785, 501798, 501827, 501830).

A. mango* (Jamaican Mango). S: 1 (558870-1); 7 (149980).

Eulampis jugularis* (Purple-throated Carib) EULAJUGU. S: 1 (487942, 487945, 487948, 487969,
488010, 488035, 556601, 556603, 556633). A: 1 (542587).
E. holosericeus* (Green-throated Carib) EULAHOLO. S: 1 (487962-3, 488000, 488006, 555023, 555033,
557665). A: 1 (318101).
b r il l ia n t s
Haplophaedia aureliae* (Greenish Puffleg) HAPLAURE. S: 1 (428851, 428868, 560029, 560030); 2; 7

(141747); 10 (89183). A: 2 (104769).
H. lugens* (Hoary Puffleg). S: 3; 10 (105695). A: 3 (7239).
Eriocnemis nigrivestis (Black-breasted Puffleg). S: 3.
E. vestita* (Glowing Puffleg). S: 1 (501558-9); 2; 3 (8230, 8280); 10 (99894).
E. cupreoventris (Coppery-bellied Puffleg). A: 11 (105392).
E. luciani* (Sapphire-vented Puffleg) ERIOLUCI. S: 1 (559963-5); 2 (81222, 99328, 112877); 3 (7060).
A: 1 (505424).
E. mosquera* (Golden-breasted Puffleg). S: 1 (559962).
E. alinae* (Emerald-bellied Puffleg). S: 2 (107089, 129817-9). A: 2 (129522).
Aglaeactis cupripennis* (Shining Sunbeam) AGLACUPR. S: 1 (559972-4, 614842-3); 2; 3 (7053-4); 9
(7851). A: 1 (505439).
A. castelnaudii* (White-tufted Sunbeam). S: 2 (113660, 129791-2).
Coeligena coeligena* (Bronzy Inca). S: 1 (491510, 491752-3, 560035); 2 (97466, 129797); 7 (141746). A: 1
(512168).
C. wilsoni* (Brown Inca). S: 1 (501555, 610458); 8 (38331); 11 (118770).
C. torquata* (Collared Inca). S: 1 (428869, 428882, 560051); 2 (89772).
C. violifer (Violet-throated Starfrontlet). S: 2 (74857, 89792); 3 (7038, 7332).
C. iris (Rainbow Starfrontlet) COELIRIS. S: 2 (79771, 81223, 81225, 86476-7); 3; A: 3 (7262).
C. phalerata (White-tailed Starfrontlet). S: 8 (38332).
C. lutetiae* (Buff-winged Starfrontlet). S: 1 (501556); 2; 3 (6063, 6067, 6071). A: 3 (7267).
Lafresnaya lafresnayi* (Mountain Velvetbreast) LAFRLAFR. S: 1 (428898, 614844-5); 2 (75608, 97465,
129793) ; 3 (8228, 8270). A: 1 (505576, 615934).
Ensifera ensifera* (Sword-billed Hummingbird) ENSIENSI. S: 1 (428880, 501557); 2 (157292); 3 (8259,
8541). A: 1 (505429).
Pterophanes cyanopterus* (Great Sapphirewing) PTERCYAN. S: 1 (501561); 2 (79763-5, 101267, 113659,
129794) ; 3 (7056-7). A: 1 (505488).
Boissonneaua flavescens* (Buff-tailed Coronet). S: 1 (428897, 559988); 3 (6069, 8286); 9 (4136); 11 (118767).
A: 3 (7283).
B. matthewsii* (Chestnut-breasted Coronet) BOISMATT. S: 2 (74861, 93901, 107081-2); 5 (210493). A:
2 (91484).
B. jardini (Velvet-purple Coronet). S: 3 (17653).
Ocreatus underwoodii* (Booted Racket-tail) OCREUNDE. S: 1 (428754, 491583, 501647, 559990); 2; 3
(17651); 7; 8 (37446); 9 (2071). A: 1 (505457, 512389).
Urosticte benjamini* (Purple-bibbed Whitetip) UROSBENJ. S: 2 (118208, 157298); 3 (1764). A: 3 (4700).
Urochroa bougueri* (White-tailed Hillstar) UROCBOUG. S: 2; 3 (6075); 8 (36639, 36948, 37700-1); 11
(118774). A: 3 (9701).
Heliodoxa xanthogonys* (Velvet-browed Brilliant). S: 3 (18152, 18155, 18157-8); 4 (318840, 339638). A: 1.
H. gularis (Pink-throated Brilliant). S: 2 (89755-6).
H. branickii* (Rufous-webbed Brilliant). S: 1 (491590-1); 2 (107023); 4 (315387, 320908). A: 1 (512076).
H. schreibersii* (Black-throated Brilliant). S: 2 (118346); 3; 4 (315367, 320877). A: 3 (7234).
H. aurescens* (Gould's Jewelfront) HELIAURE. S: 2 (93889, 107015, 118345); 4 (315362, 320851). A: 1.
H. rubinoides* (Fawn-breasted Brilliant). S: 1 (501565; 2; 3 (6079, 8235, 8306); 8 (36726); 10. A: 1
(512157).
H. jacula* (Green-crowned Brilliant). S: 1 (500466, 501562-3); 2; 8 .

H. leadbeateri* (Violet-fronted Brilliant) HELILEAD. S: 1 (491567, 501564, 560016-7, 560031); 2 (68736,

83969); 6 (80847); 13 (2422). A: 1 (505623).
Clytolaema rubricauda (Brazilian Ruby). S: 1.
Sternoclyta cyanopectus (Violet-chested Hummingbird) STERCYAN. S: 1 (501646); 5 (210814). A: 1
(505039).
co q uettes
Heliangelus amethysticollis* (Amethyst-throated Sunangel) HELIAMET. S: 1 (559996); 2 (97480, 107084);

3 (6074, 6909); 10 (99893). A: 1 (511966).
H. strophianus (Gorgeted Sunangel). S: 1 (559984-5); 4 (106388).
H. exortis* (Tourmaline Sunangel). S: 1 (428884); 2 (97481-2); 3 (8238); 9. A: 13 (1974).
H. viola (Purple-throated Sunangel). S: 1 (491386); 8 (37664-5). A: 3 (7237).
Sephanoides sephaniodes* (Green-backed Firecrown) SEPHSEPH. S: 1 (322956); A: 1 (508250).
S. fernandensis* (Juan Fernandez Firecrown). S: 15 (35366); A: 1 (322907).
Discosura conversii* (Green Thorntail) DISCCONV. S: 3 (5744); 17 (927800). A: 3 (4771).
D. popelairii* (Wire-crested Thorntail). S: 1 (501567); 2 (157296).
D. langsdorffi (Black-bellied Thorntail). S: 2 (109390, 111176, 132099). A: 1 (616367, 616534).
Lophornis helenae (Black-crested Coquette) LOPHHELE. S: 2 (31867).
L. ornatus (Tufted Coquette). A: 1 (81493).
L. adorabilis (White-crested Coquette). S: 5 (133762, 153098-9).
L. gouldii (Dot-eared Coquette) LOPHGOUL. S: 1 (562447). A: 18 (5529).
L. magnificus (Frilled Coquette). S: 1; 4 (105685).
Phlogophilus hemileucurus* (Ecuadorian Piedtail) PHLOHEMI. S: 1 (560021); 2 (86389, 86692, 157299).
A: 2 (85958).
P. harterti (Peruvian Piedtail). S: 4 (320834-5, 320843).
Adelomyia melanogenys* (Speckled Hummingbird) ADELMELA. S: 1 (428896, 559582-3, 560036, 560050);
2 (93885, 129787-8). A: 1 (615317).
Aglaiocercus kingi* (Long-tailed Sylph) AGLAKING. S: 1 (428825, 428858); 2; 3 (429, 6065); 5 (213992);
8 ; 9 (4158). A: 1 (512427).
A. coelestis* (Violet-tailed Sylph). S: 1: 2 (95373, 101275); 3 (17648, 17650); 5 (209220); 8 (43861). A: 1
(227969).
Sappho sparganura (Red-tailed Comet) SAPPSPAR. S: 2 (95373, 101275); 3 (17648, 17650); 5 (209220),
8 (43861). A: 1 (227969).
Polyonymus caroli (Bronze-tailed Comet) POLYCARO. S: 2 (86481, 97479). A: 2 (86213).
Oreotrochilus estella* (Andean Hillstar) OREOESTE. S: 2 (93893, 114251, 120852); 3 (6070, 7049, 7050);
5 (212728). A: 1 (505434, 505451).
O. melanogaster (Black-breasted Hillstar). S: 2 (106938); 5 (156828).
Loddigesia mirabilis (Marvelous Spatuletail) LODDMIRA. A: 19 (192473, 192474).
Opisthoprora euryptera* (Mountain Avocetbill) OPISEURY. S: 2 (87579, 93938).
Lesbia victoriae* (Black-tailed Trainbearer) LESBVICT. S: 1; 2 (93903); 3 (6057, 8460); 5 (210492); 10
(89184). A: 1 (505447).
L. nuna* (Green-tailed Trainbearer). S: 2 (83977); 3 (7061-2); 6 (80901); 9 (7852).
Ramphomicron microrhynchum* (Purple-backed Thornbill) RAMPMICR. S: 1 (559975); 2 (71577,
129820, 157350); 3 (6061, 6066, 6068). A: 2 (113730).
Chalcostigma ruficeps* (Rufous-capped Thornbill). S: 2 (70215, 89849, 93936, 101278). A: 2 (79537).
C. olivaceum (Olivaceous Thornbill). S: 2 (114252-3). A: 2 (70610).
C. stanleyi (Blue-mantled Thornbill) CHALSTAN. S: 2 (79789, 93937). A: 1 (505476).
Oxypogon guerinii* (Bearded Helmetcrest) OXYPGUER. S: 3 (9500). A: 3 (4637).
Oreonympha nobilis* (Bearded Mountaineer) OREONOBI. S: 3 (7075); 4 (324113). A: 2 (79540).
Metallura tyrianthina* (Tyrian Metaltail). S: 1 (559966-8); 2 (81214-5, 129841, 129844); 3 (7074); 10
(99896). A: 1 (505444).
M. williami* (Viridian Metaltail). S: 1 (428821); 2; 3 (6058). A: 11 (112064).

M. odomae (Neblina Metaltail). S: 2 (89835).

M. theresiae (Coppery Metaltail) METATHER. S: 2 (81219, 89837, 93914, 113663, 120899, 120912-3,
120916). A: 2 (120716).
M. eupogon (Fire-throated Metaltail). S: 2 (129829, 129833-4, 129839); 3 (7064-5).
M. aeneocauda* (Scaled Metaltail). S: 2 (79776, 95374-6).
M. phoebe* (Black Metaltail). S: 2 (114260, 120835); 3 (7067, 7069).
pa ta go n a
Patagona gigas* (Giant Hummingbird) PATAGIGA. S: 1 (322105, 343093); 2 (120849); 3 (7063); 4

(324112); 5 (156737); 7 (158796). A: 1 (505465).
m o u n t a in g e m s
Eugenes fulgens* (Magnificent Hummingbird) EUGEFULG. S: 2 (62777, 63140, 64846, 131282); 3

(12735); 6 (30887); 7. A: 1 (5061130).
Panterpe insignis* (Fiery-throated Hummingbird) PANTINSI. S: 1 (613296); 2 (48570, 50757, 51328,
62776, 63138, 64845); 3 (12711-2); 7. A: 1 (542828); 2 (63690).
Heliomaster longirostris* (Long-billed Starthroat) HELILONG. S: 1 (500582, 559695, 612951); 2 (31891);
5 (133791, 153110, 218953). A: 3.
H. constantii (Plain-capped Starthroat). S: 2 (31890, 50764); 3 (10316); 7 (85772, 154290). A: 1 (506366).
H. furcifer (Blue-tufted Starthroat). S: 1 (556414); 2 (151657); 5 (202055). A: 3 (7231).
Lampornis clem nciae (Blue-throated Hummingbird). S: 2; 5(159127); 6 ; 8(37443); 10. A: 11 (118323).
L. amethystinus (Amethyst-throated Hummingbird). S: 4 (105158); 6 (30886); 7. A: 11 (113216).
L. viridipallens (Green-throated Mountain-gem). S: 1 (560217-9, 560220); 6 (69624, 69645); 9 (8141-2).
L. hemileucus* (White-bellied Mountain-gem). S: 5 (133784, 133787).
L. castaneoventris* (Variable Mountain-gem) LAMPCAST. S: 1 (613292-3); 2 (157295); 3 (12791); 5
(133783, 219567). A: 1 (542827).
Lamprolaima rhami (Garnet-throated Hummingbird) LAMPRHAM. S: 1 (611758); 6 (40549); 7 (85747).
A: 6 (040545).
bees
Myrtis fanny* (Purple-collared Woodstar) MYRTFANN. S: 2 (81213, 93939, 113666); 3 (7083-5); 5

(156833). A: 1 (505463).
Eulidia yarrellii (Chilean Woodstar). S: 1 (500846).
Myrmia micrura (Short-tailed Woodstar) MYRMMICR. S: 2 (93940). A: 2 (89429).
Rhodopis vesper* (Oasis Hummingbird) RHODVESP. S: 2 (100535); 3 (7076-8); 4 (105915). A: 3 (9775-7).
Thaumastura cora (Peruvian Sheartail) THAUCORA. S: 2 (65301, 114250, 157351); 3 (7079, 7080). A: 2
(114290).
Calothorax lucifer (Lucifer Hummingbird) CALOLUCI. S: 1 (559710, 560942); 5; 6 (29236). A: 11
(110097).
C. pulcher (Beautiful Hummingbird). S: 7 (154291).
Doricha enicura (Slender Sheartail) DORIENIC. S: 1 (11643); 6 (69654).
D. eliza (Mexican Sheartail). S: 15 (37715). A: 6 (89338).
Calliphlox evelynae (Bahama Woodstar) CALLEVEL. S: 1 (555533-4); 2 (71050, 71247, 80151, 86684);
17: (37570). A: 1 (505046).
C. mitchellii* (Purple-throated Woodstar). S: 20. A: 20.
C. amethystina (Amethyst Woodstar). A: 1 (505591); 21.
Chaetocercus mulsant (White-bellied Woodstar) CHAEMULS. S: 1 (559971); 2 (105820, 129848). A: 1
(505414).
C. bombus (Little Woodstar). A: 1.
C. jourdanii (Rufous-shafted Woodstar) CHAEJOUR. S: 1 (344155-6); 13 (2634).

Microstilbon burmeisteri (Slender-tailed Woodstar) MICRBURM. S: 1 (645254); 5 (157954). A: 1

(645151).
Tilmatura dupontii (Sparkling-tailed Woodstar). S: 1. A: 1 (541082).
Mellisuga minima (Vervain Hummingbird) MELLMINI. S: 1 (226929, 292586, 555789, 555790-1). A: 1
(225892, 225926, 291395, 318952).
M. helenae (Bee Hummingbird). S: 1; A: 1 (229945-8, 225950).
Archilochus colubris* (Ruby-throated Hummingbird) ARCHCOLU. S: 1 (347968, 498793, 502142,
553900, 560941, 610988, 612009); 2; 3 (11057). A: 1 (319894).
A. alexandri* (Black-chinned Hummingbird). S: 1 (17073, 226374-5, 346514-5, 555737).
Calypte anna* (Anna's Hummingbird). S: 2 (130850); 7 (41356, 69531, 77234, 120370).
C. costae* (Costa's Hummingbird) CALYCOST. S: 1 (20344, 499022, 553913, 555620, 621308); 2; 3
(5735, 8499, 13775); 10 (102419). A: 1 (23475).
Atthis heloisa (Bumblebee Hummingbird) ATTHHELO. S: 4 (343216); 5 (214389); 11 (109634). A: 1
(506367).
Stellula calliope* (Calliope Hummingbird) STELCALL. S: 1 (489879, 498990, 571158); 2 (95267); 3
(15979); 7 (69324-5). A: 1 (18651).
Selasphorus rufus* (Rufous Hummingbird) SELARUFU. S: 1 (558426, 558428, 558431-2, 610991,
621310); 2 (122561); 5 (204596); 7 (125538); 9 (2231); 12 (68669). A: 1 (81518).
S. sasin (Allen's Hummingbird). S: 2 (118768); 7 (125538); 9 (5753, 6279); 10 (103144); 12 (68989).
S. platycercus* (Broad-tailed Hummingbird). S: 1 (17076-7, 450076, 498881); 2 (122199); 3 (5457,
16639); 7 (41412, 153908).
S. flammula* (Volcano Hummingbird). S: 2 (48518, 48573, 64847); 3 (12697, 12724); 5 133794); 7.
S. scintilla (Scintillant Hummingbird). S: 5 (219569).
em erald s
Chlorostilbon canivetii (Canivet's Emerald). S: 1 (432179), 2 (118529, 1131465); 5 (153100); 7 (85738,

153912). A: 1 (541030).
C. mellisugus* (Blue-tailed Emerald) CHLOMELL. S: 1 (428762); 2 (118529, 131465); 3 (6064, 7035); 4
(317158); 9 (4143). A: 1 (505461); 13 (1350).
C. aureoventris (Glittering-bellied Hummingbird). S: 2; 4 (105325); 5 (200684, 202039, 202040); 10
(104434).
C. ricordii (Cuban Emerald). S: 1 (553356, 555178-9, 562473, 6122530); 4 (105612, 105747). A: 1 (542501).
C. bracei (Brace's Emerald). S: 1 (553485, 553488).
C. swainsonii (Hispaniolan Emerald). S: 1 (555787); 9 (6495, 12107). A: 1 (291045).
C. maugaeus (Puerto Rican Emerald). S: 1 (501773-4, 501786-7, 501813). A: 1 (504029).
Cynanthus sordidus (Dusky Hummingbird). S: 5 (210412, 210528); 7 (153913).
C. latirostris (Broad-billed Hummingbird) CYNALATI. S: 1 (489886); 4 (317859); 6 (19042, 29809,
30883, 35634); 7. A: 1 (226755).
Cyanophaia bicolor (Blue-headed Hummingbird) CYANBICO. S: 1 (487926, 487978, 488044). A: 1
(508024).
Orthorhyncus cristatus* (Antillean Crested Hummingbird) ORTHCRIS. S: 1 (487958, 487992, 555008,
555016, 555019, 555021, 558096, 558100, 612556). A: 1 (81180).
Klais guimeti* (Violet-headed Hummingbird) KLAIGUIM. S: 1 (559997); 2 (50765, 86440, 157297); 3
(17236); 4 (320773); 14 (37762). A: 2 (81180).
Stephanoxis lalandi (Plovercrest) STEPLALA. S: 1 (555948, 555950, 558794-5); 5 (200683); 9 (6432). A:
1 (505203).
Abeillia abeillei (Emerald-chinned Hummingbird) ABELABEI. S: 1 (560211-2); 6 (69643). A: 1 (540578).
Basilinna leucotis (White-eared Hummingbird) BASILEUC. S: 1 (500617); 2; 3 (8084, 8086-7, 13766);
5; 10 (89179). A: 1 (506361).
B. xantusii (Xantus's Hummingbird). S: 2 (127198); 7 (55204-5, 55207). A: 1 (87685).
Phaeochroa cuvierii (Scaly-breasted Hummingbird) PHAECUVI. S: 1 (430229); 2 (32041, 50751); 7
(155746).

Campylopterus curvipennis (Wedge-tailed Sabrewing). S: 2; 6 (28954); 9 (9887-8, 9890, 9892). A: 3

(7279).
C. largipennis* (Gray-breasted Sabrewing) CAMPLARG. S: 1 (492310, 492317, 492324, 492338, 620144-5); 2;
6 (71829, 72047); 9 (7872, 8286). A: 1 (511221).
C. rufus (Rufous Sabrewing). S: 12 (71555). A: 1 (506222).
C. hyperythrus* (Rufous-breasted Sabrewing). S: 3 (9495); 4 (339630-1). A: 1 (505622).
C. hemileucurus* (Violet Sabrewing). S: 1 (7050, 560209, 560210); 3 (10305, 15664); 5 (210638); 6 (29297);
7; 8 (25626); 12. A: 1 (506219).
C. ensipennis (White-tailed Sabrewing). S: 1 (344140-1).
C. falcatus (Lazuline Sabrewing). S: 1 (491751). A: 1 (615309, 615311).
C. villaviscensio* (Napo Sabrewing). S: 1 (501553, 560014); 2 (118200-1). A: 3 (7280).
C. duidae (Buff-breasted Sabrewing). S: 3 (18144, 18148, 18150-1); 4 (318777, 318781). A: 1 (505499,
505596).
Eupetomena macroura (Swallow-tailed Hummingbird) EUPEMACR. S: 1 (345894, 490018, 561285,
562761); 2 (125728); 4 (334990-1); 7; 14 (37775-6). A: 2 (85953).
Chlorestes notata* (Blue-chinned Sapphire) CHLONOTA. S: 1 (344149, 344150, 562503-4, 612946); 2; 4
(313624-5); 6 (71827, 71902). A: 1 (542677).
Chalybura buffonii* (White-vented Plumeleteer) CHALBUFF. S: 1 (428756, 490206, 610226-7); 2; 5
(218384-6). A: 1 (615313).
C. urochrysia* (Bronze-tailed Plumeleteer). S: 1 (428231); 5 (133779, 133782).
Thalurania colombica* (Violet-crowned Woodnymph). S: 1.
T. furcata* (Fork-tailed Woodnymph) THALFURC. S: 1 (344153, 345895, 345897, 501333, 560022,
562450-1, 613385, 613387-8); 2; 9 (8047-8). A: 1 (505523).
T. glaucopis (Violet-capped Woodnymph). S: 1; 7.
Trochilus polytmus (Red-billed Streamertail) TROCPOLY. S: 1 (502867, 502872, 502874, 502876, 558876,
558880, 559187). A: 1 (505181).
Eupherusa eximia* (Stripe-tailed Hummingbird) EUPHEXIM. S: 1 (490214, 560215-6); 4 (69629, 69671);
6 ; 12 (71908). A: 1 (542825).
E. nigriventris* (Black-bellied Hummingbird). S: 1 (613299, 613300); 3 (5661); 5 (133778).
Microchera albocoronata* (Snowcap). S: 5 (153107, 156028).
Elvira chionura* (White-tailed Emerald) ELVICHIO. S: 1 (613301); 2 (50762). A: 1 (542829).
E. cupreiceps* (Coppery-headed Emerald). A: 1 (510679).
Aphantochroa cirrochloris* (Sombre Hummingbird) APHACIRR. S: 8 ; 10 (89181).
Taphrospilus hypostictus* (Many-spotted Hummingbird) TAPHHYPO. S: 2 (116620); 4 (315355). A: 4
(291588).
Leucochloris albicollis (White-throated Hummingbird) LEUCALBI. S: 4 (105681, 105683-4); 5 (200694).
A: 1 (505195).
Leucippus fallax (Buffy Hummingbird). A: 1 (505528).
L. baeri (Tumbes Hummingbird). S: 1; 2 (75603, 77723, 93880); 3 (7039). A: 2 (75459).
L. taczanowskii (Spot-throated Hummingbird). S: 2 (981208, 93881); 3 (7040). A: 2 (75461).
L chlorocercus (Olive-spotted Hummingbird) LEUCCHLO. S: 2 (48763, 111172, 121020, 121023-4,
121030, 121032). A: 2 (120575).
Amazilia chionogaster* (White-bellied Hummingbird). S: 2 (70208, 73052, 125745, 125747, 125749,
125751); 3 (9145). A: 1 (19412).
A. viridicauda (Green-and-white Hummingbird). S: 2 (48762, 129785).
A. rutila* (Cinnamon Hummingbird). S: 1 (210524); 2 (31883, 50755, 51330); 3 (10313); 5 210524); 6
(36532); 7 (85757).
A. yucatanensis (Buff-bellied Hummingbird). S: 6 (24927, 30884); 11 (112895). A: 13 (1608).
A. tzacatl* (Rufous-tailed Hummingbird) AMAZTZAC. S: 1 (492394, 611570, 613401, 613403, 613405,
613407, 613409, 613411, 613414, 613416); 2. A: 1 (542822).
A. amazilia (Amazilia Hummingbird). S: 1 (492391); 2 (52686); 3 (7045-6). A: 2.
A. leucogaster (Plain-bellied Emerald). S: 3 (17661); 6 (34823, 72010, 72012).
A. versicolor* (Versicolored Emerald). S: 1 (555592, 555951, 558000); 4; 6 (318826).

A. brevirostris (White-chested Emerald). S: 1 (560162); 5 (158228).

A. franciae* (Andean Emerald). S: 1 (428758, 491387); 8 (36667, 38043); 13 (2427, 2419).
A. candida (White-bellied Emerald) AMAZCAND. S: 1 (288831-3, 288837); 2; 3 (7856, 12567). A: 3
(7294).
A. cyanocephala (Azure-crowned Hummingbird). S: 1 (560214); 2 (31878-9, 31880); 6 (29237).
A. violiceps (Violet-crowned Hummingbird). S: 6 (33143, 35439); 7 (153910-1); 10 (104411).
A. viridifrons (Green-fronted Hummingbird). S: 5 (159125); 6 (69628); 11 (118428, 118436).
A. fimbriata* (Glittering-throated Emerald). S: 1 (559698-9, 560052); 2; 3; 4 (337126); 11 (105981, 114838).
A. lactea (Sapphire-spangled Emerald). S: 2 (50754, 73208); 3 (7042-3) .
A. amabilis* (Blue-chested Hummingbird) AMAZAMAB. S: 1 (432603, 500460, 613389, 613983); 5
(133772-4). A: 1 (542239).
A. saucerrottei* (Steely-vented Hummingbird). S: 1 (347112); 2 (32032, 48572); 5 (153106).
A. cyanifrons (Indigo-capped Hummingbird). S: 1 (428766).
A. edward (Snowy-bellied Hummingbird). S: 1 (432108); 2 (32033, 50752).
A. cyanura (Blue-tailed Hummingbird). S: 2 (31881-2).
A. beryllina (Berylline Hummingbird). S: 3 (8089, 8090); 6 (34802-3, 69652).
A. viridigaster* (Green-bellied Hummingbird). S: 3 (15115, 18153-4). A: 1 (505543).
A. tobaci (Copper-rumped Hummingbird) AMAZTOBA. S: 1 (555688-9, 555690, 562505-6, 612949,
612950); 4 (104246). A: 1 (346751).
Chrysuronia oenone* (Golden-tailed Sapphire) CHRYOENO. S: 1 (560053); 2 (70207, 118206); 3 (7037);
4 (291760, 315346, 320808). A: 1 (615312).
Goethalsia bella (Pirre Hummingbird) GOETBELL. S: 1 (559696); 2 (104615, 104665, 108746).
Goldmania violiceps (Violet-capped Hummingbird) GOLDVIOL. S: 1 (432625); 5 (219563-5). A: 1 (432661).
Lepidopyga coeruleogularis* (Sapphire-throated Hummingbird) LEPICOER. S: 1 (432175, 490211,
610224-5); 3 (6510); 5 (490211). A: 1 (431209).
Damophila julie* (Violet-bellied Hummingbird) DAMOJULI. S: 1 (491263, 559703, 559708, 610220, 610222);
2; 8 (37379). A: 7 (4104).
Hylocharis eliciae* (Blue-throated Goldentail). S: 2 (32030-1); 5 (133771). A: 2 (99907).
H. sapphirina* (Rufous-throated Sapphire). S: 9 (7599).
H. cyanus* (White-chinned Sapphire) HYLOCYAN. S: 1; 2 (99591); 3 (11946); 5 (209492); 11 (107530).
A: 2 (131780).
H. chrysura (Gilded Hummingbird) HYLOCHRY. S: 1 (555949, 556412); 2; 4 (334400-1, 335011); 5; 6
(79270). A: 1 (505979).
H. grayi* (Blue-headed Sapphire). S: 11 (106267, 114826, 118756). A: 11 (112062).

A ppen d ix 2
C haracter L ist for F requency M atrix
1. Length of dorsal bar of prepalatal upper jaw between nasal crest and intermediate part, in
relation to length between nasal crest and craniofacial hinge: (a) longer, (b) similar, (c) shorter.
2. Dorsal bar of prepalatal upper jaw rostral to nasal roof, shape of transverse section: (a) ovate or
circular, (b) dorsoventrally compressed, (c) laterally compressed.
3. Maxillare, shape of ventral surface at level of junction with maxillary process of nasale: (a)
concave and rounded, (b) concave and angled.
4. Dorsal bar of prepalatal upper jaw rostral to nasal roof, shape in dorsal view: (a) sides parallel,
(b) sides diverging rostrally.
5. Mandibula, size of rostral mandibular fenestra: (a) absent or small, (b) medium, (c) large.
6. Mandibular ramus, degree of inflation of caudal part in relation to intermediate part in ventral
or dorsal view: (a) slight, (b) moderate, (c) marked.
7. Mandibula, shape of transverse section of intermediate part of ramus rostral to rostral mandib
ular fenestra: (a) lateromedially compressed with thicker dorsal and ventral margins, (b) oval.
8. Nasal part of upper jaw, conformation of transverse section of medial concha: (a) thin and
scrolled, (b) partially scrolled and thickened, (c) thick and unscrolled.
9. Nasal part of upper jaw, rostral concha, status and development of ventral wing: (a) well
developed along most or all of vertical wall, (b) weakly developed or reduced to angular ridge
in region of nasal crest, (c) absent.
10. Nasal part of prepalatal upper jaw, rostral concha, rostral portion of ventral wing in relation to ros
tral limit of vertical wall: (a) does not protrude, (b) protrudes moderately, (c) protrudes markedly.
11. Ossified nasal roof: (a) fused caudally with nasale, (b) separated caudally from nasale.
12. Nasal part of prepalatal upper jaw, rostral concha, rostral portion of vertical wall: (a) not flared
laterally, (b) moderately flared, (c) strongly flared.
13. Nasal operculum, status and development of tubercles or ridges internally, caudal to external
nasal opening: (a) absent, (b) weakly developed, (c) well developed.
14. Nasal part of prepalatal upper jaw, vestibular potion of nasal roof, status and dimensions of
ossification: (a) ossification absent, (b) ossification present, length equal to or less than width,
(c) ossification present, length greater than but less than twice width, (d) ossification present,
at least twice width.
15. Nasal part of upper jaw, rostral concha, status of laterally curved ridge and groove on rostro-
ventral surface of lateral wing: (a) absent, (b) present.
16. Nasal part of upper jaw, status and development of nasal crest, (a) complete, (b) lacking medi
ally, (c) absent or indistinct.
17. Nasal part of upper jaw, rostral limit of ossified nasal roof in relation to rostral limit of rostral
concha: (a) equal to, (b) moderately less than, (c) markedly less than.
18. Palatum, lateral part of palatinum, location: (a) on ventral choanal lamella, (b) between ventral
choanal lamella and rostral bar, (c) on rostral bar.
19. Palatum, anterior profile of vomeral body in ventral view: (a) rounded, (b) angled, (c) spiked.
20. Palatum, vomeral body length in relation to width: (a) shorter than, (b) equal to, (c) longer than.
21. Palatum, status and length of vomeral spine in relation to length of rostral bar of palatinum:
(a) spine absent, (b) longer than, (c) equal to, (d) shorter than.
22. Palatum, palatinum, shape of dorsomedial margin and its relation to pterygoid process
of vomer: (a) curved, smoothly merging with caudal half of pterygoid process, (b) curved,
meeting caudal third of pterygoid process at obtuse angle, (c) straight, meeting caudal end of
pterygoid process at acute angle.
23. Palatum, pterygoideum, status of intrapterygoid articulation: (a) present, (b) absent.
24. Palatum, pterygoideum, breadth of shaft in ventral view: (a) narrow throughout, (b) broader
caudally, (c) broad throughout.

25. Jugal arch, shape of rostral portion in ventral view: (a) gradually widened, (b) abruptly and
moderately widened, (c) abruptly and markedly widened.
26. Palatum, palatal process of maxillare, relation to rostral bar of palatinum: (a) fused and undif
ferentiated, (b) fused as dorsal and/or medial ridge, without caudomedial extension, (c) fused
as dorsal and/or medial ridge, with caudomedial extension.
27. Cranium, status of ossification of caudal wall of hypophysial recess: (a) absent or incomplete,
(b) complete bridge.
28. Cranium, supraoccipitale, dorsal margin of occipital condyle: (a) not thickened, (b) slightly
thickened, (c) prominently thickened.
29. Cranium, frontale, conformation of supraorbital rim in dorsal view: (a) angled, rounded, or
notched, (b) straight and approximately parallel to sagittal plane of cranium.
30. Cranium, ectethmoidale, conformation of caudal margin in dorsal view: (a) moderately angled
to sagittal plane of cranium, (b) nearly perpendicular to sagittal plane of cranium.
31. Cranium, surface of parasphenoidal rostrum between pterygoid processes of vomer in ventral
view: (a) flat to rounded, (b) with median ridge.
32. Cranium, mesethmoidale, orientation of rostroventral margin in relation to ventral contour of
parasphenoidal rostrum in lateral view: (a) markedly angled (~ 45°) to, (b) moderately angled
(10-40°) to, (c) approximately collinear with.
33. Cranium, degree of lateral inflation of skull base, parasphenoidal rostrum, and interorbital
septum: (a) none or slight, (b) moderate, (c) great.
34. Cranium, status of fonticulus in frontale: (a) absent, (b) present.
35. Cranium, caudal profile of cerebellar prominence in lateral view: (a) evenly curved, (b) truncate.
36. Cranium, parasphenoidal rostrum, conformation between pterygoid processes of vomer
in ventral view: (a) broad, (b) slightly narrowed on midportion, (c) markedly narrowed in
midportion.
37. Cranium, ectethmoidale, rostral profile in lateral view, status and extent of protrusion ventral
to nasolacrimal sulcus: (a) absent or slight, (b) moderate, (c) marked.
38. Cranium, ectethmoidale, portion of rostral surface lateral to olfactory chamber: (a) abruptly
convex, (b) approximately flat, (c) concave.
39. Cranium, extent of temporal fossa in relation to cerebellar prominence in caudal view: (a) distinctly
lateral to, (b) near or with slight encroachment, (c) considerable encroachment (approaching
midsagittal plane of cranium), (d) reaching midsagittal plane, forming nuchal crest.
40. Cranium, foramen of occipital ramus of ophthalmic artery: (a) single, (b) double and closely
spaced, (c) double and moderately spaced, (d) double and widely spaced.
41. Cranium, caudolateral wall of foramen for maxillomandibular nerve: (a) unossified, (b) slightly
ossified, (c) fully ossified.
42. Cranium, medial orbitonasal foramen: (a) double, (b) single.
43. Cranium, status and number of pneumatic foramena on otic pillar: (a) none, (b) few, (c) many.
44. Thoracic vertebrae, number rostral to synsacrum: (a) four (rarely five), (b) three (rarely two).
45. Cervical rib processes, length in relation to depth of vertebral body: (a) greater than, (b) equal
or less than.
46. Sternum, extent of lateral separation between coracoidal facets: (a) none, (b) slight, (c) moder
ate, (d) great.
47. Sternum, costal margin, modal number of sternocostal articular processes on each side (reflect
ing number of attached thoracic ribs): (a) four (or three), (b) five, (c) six (or seven).
48. Sternum, shape of carinal apex in lateral view: (a) short and rounded, (b) sharply pointed,
(c) dorsally convex and angled, (d) long and broadly rounded.
49. Humerus, status and extent of roof over recess of ventral process: (a) present and broad,
(b) present and narrow, (c) absent.
50. Humerus, status of pneumatic foramena near distal end of shaft: (a) absent, (b) present.
51. Humerus, status of pneumatic foramen (a) immediately distal to capital tubercle: (a) present,
(b) absent.

52. Humerus, status of pneumatic foramen caudally on base of deltopectoral crest: (a) absent, (b)
present.
53. Humerus, status and proximity of the tubercle of m. flexor digitorum profundus to the prona
tor tubercle: (a) present and strongly distal to, (b) present and moderately distal to, (c) closely
spaced or not distinguishable.
54. Humerus, position of process of extensor metacarpi radialis muscle in relation to midpoint of
long axis of humeral shaft: (a) proximal to, (b) even with or distal to.
55. Humerus, position of angle of tensor propatagialis brevis muscle in relation to midpoint of
humeral shaft between process of extensor metacarpi radialis muscle and the dorsal condyle:
(a) distal to, (b) even with, (c) proximal to.
56. Humerus, cranioproximal surface of head: (a) not corrugated, (b) corrugated.
57. Humerus, status and shape of notch on tip of ventral process: (a) absent, (b) present and sym
metrical, (c) present and asymmetrical.
58. Hindlimb, status of fusion of phalanges 2 and 3 of digit IV: (a) absent, (b) present.
59. Nasal region, position of caudal limit of bony nasal opening in relation to craniofacial hinge:
(a) rostral to, (b) reaches or transects craniofacial hinge.
60. Nasal part of upper jaw, rostral concha, degree of ossification: (a) unossified, (b) ossified.
F requency M atrix of C haracter States
The frequency matrix is available online at dx.doi.org/10.1525/om.2013.77.1.1. For identification of

species acronyms see Appendix 1.
A ppen d ix 3
Tensor P ropatagialis Brevis M uscle
Muscles.—M. tensor propatagialis, pars brevis (TPB), displays considerable variation within hum
mingbirds (Zusi and Bentz 1982). It originates from the head of the coracoid as a broad, strap-like
belly that terminates on the belly of m. extensor metacarpi radialis. From this attachment it sends a
tendon distally in association with m. extensor metacarpi radialis that fuses with the tendon of inser
tion of that muscle. This tendon varies from a poorly defined, aponeurotic sheet (Type I), to a well-
defined broad sheet (Type II), to a well-defined, narrow tendon (Type III). The distal tendon has not
been reported in other avian families. Taxonomic distribution of the three types corresponds exactly
to the Hermits (I), Topazes and Mangoes (II), and Neotrochilines (III) (Beiweiss 2002, McGuire et al.
2007). However, I found a weak development of the Type II tendon in one specimen of Eutoxeres aquila
(USNM 510579).
In addition, TPB sends a tendon in the opposite direction that inserts on the humeral tubercle of m.
tensor propatagialis, pars brevis. The humeral tendon crosses the aponeurosis of origin of m. extensor
metacarpi radialis on its way to insertion on the TPB angle. Where this tendon emerges from the belly
it may be free of the aponeurosis of origin of EMR, bound to it, or fused with it. The humeral tendons
of a few genera were said by Zusi and Bentz (1984) to be fused completely with that of EMR and to
attach on the EMR process (Type IV). However, additional dissections have revealed that in those
genera the humeral tendon is absent or vestigial. Vestigial tendons attach on the humerus distal to the
EMR process or lose definition without making attachment. The TPB angle is correspondingly poorly
defined or absent.
Species examined during the present study, but not included in Zusi and Bentz (1982), are listed
below, with genera not previously listed shown in bold.
Type I. (Hermits)— Eutoxeres aquila, Phaethornis griseogularis, P guy, P. superciliosus.
Type II. (Mangoes)—H eliactin bilophus, Heliothryx auritus, Polytmus theresiae, Anthracthorax viridi-
gula, Schistes geoffroyi.

Type III. (Brilliants)—Eriocnemis cupreoventris, E. alinae, Coeligena iris, C. lutetiae, B oisson n eau a fla-
vescens, B. matthewsii, U rosticte benjamini, U rochroa bougueri, Heliodoxa schreibersii, H. aurescens, H.
rubinoides, H. leadbeateri.
(Coquettes)—Heliangelus exortis, Sephanoides sephanoides, S. fernandensis, D iscosura conversii, D. lon-
gicaudus, Lophornis gouldii, P hlogophilu s hemileucurus, A d elom y ia melanogenys, P olyonym us caroli,
O reotrochilus estella, L oddigesia mirabilis, R am phom icron microrhynchum, C halcostigm a ruficeps, C.
olivaceum, C. stanleyi, Oxypogon guerinii, O reonym pha nobilis, Metallura williami, M. theresiae.
(Mountain Gems)—Heliomaster constantii, Lampornis clemenciae, L. amethystinus, L am p rolaim a rhami.
(Bees)— R hodopis vesper, T haum astura cora, D oricha eliza, M yrm ia micrura, Mellisuga helenae, Archi
lochus colubris, A tthis heloisa.
(Emeralds)—Chlorostilbon canivetti, C. mellisugus, C. ricordii, K lais guimeti, A beillia abeillei, B asilin n a
leucotis, B. xantusii, Chlorestes notata, Campylopterus curvipennis, C. largipennis, C. rufus, C. hyperythrus,
C. hemileucurus, C. falcatus, C. villaviscensio, E upetom ena macroura, Eupherusa eximia, Elvira chionura,
Taphrospilus hypostictus, Leucippus baeri, L. taczanowskii, L. chlorocercus, Amazilia chionogaster, A. yucata-
nensis, A. candida, A. tobaci, Hylocharis eliciae, H. cyanus, H. grayi.
Type IV. (Bees)— Calliphlox mitchellii, M icrostilbon burmeisteri, Tilm atura dupontii.
Type IV is actually an apomorphic modification of Type III. All of its species also possess plumage
features (white flank patches) not found in other Bees. Consequently, they are listed consecutively
(Calliphlox mitchellii through Tilmatura dupontii) in Appendix 1. If this hypothetical clade were substan
tiated, Calothorax would be polyphyletic.


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BioOne COMPLETE

Introduction to the Skeleton of Hummingbirds (Aves:

BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access

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INTRODUCTION TO THE SKELETON OF HUMMINGBIRDS

A bstract.— Historically, comparative study of the skeleton of hummingbirds has focused

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Introducción al Esqueleto de los Colibríes (Aves: Apodiformes: Trochilidae) en

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M ethods and M aterials families if the character in question is thought to be

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The larynx, trachea, syrinx, and bronchi of birds

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Table 1. Morphological comparisons of the syrinx in swifts and hummingbirds.

Location of syrinx Thorax Neck

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PREPALATAL UPPER JAW PALATUM

SYMPHYSIAL INTERMEDIATE NASAL

SYMPHYSAL NTERMED ATE CAUDAL

LOWER JAW (MANDIBULA)

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palatinum is dorsoventrally flattened, forming a hummingbirds has been interpreted as fused

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ELBOW >»" humerus

HEMIPROCNIDAE APODIDAE TROCHILIDAE

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The basal phalanx of the major digit is broader

S esamoids of the Tail

The rectricial bulb (bulbus rectricium) is a bilat

approximately horizontal (while hovering below In hummingbirds, exceptionally powerful exte

kinematics, as well as detailed functional anat

Fig . 30. Variation in length of rib processes of cervi