timm2015

Chapter 21
Clitellata: Oligochaeta
Tarmo Timm
Institute of Agricultural and Environmental Sciences, Centre for Limnology, Estonian University of Life Sciences, Rannu, Tartumaa, Estonia
Patrick J. Martin
O.D. Taxonomy and Phylogeny, Royal Belgian Institute of Natural Sciences, Brussels, Belgium
Chapter Outline
Introduction529 Physiological Constraints 542
General Systematics 529 Feeding Behavior 543
Phylogenetic Relationships 531 Predators and Parasites 543
Distribution and Diversity 533 Other Ecological Aspects of Oligochaeta 544
General Biology 535 Collecting, Culturing, and Specimen Preparation 544
External Anatomy 535 Collecting544
Internal Anatomy 537 Rearing545
Physiology540 Preparation for Identification 545
Reproduction and Life History 541 References548
General Ecology and Behavior 542
Macrohabitat Distribution and Microhabitat Selection 542
INTRODUCTION sediments. Classifying the families into orders is difficult

and problematic, especially in the case of aquatic forms. To
General Systematics
date, there is no consensus on the classification that should
Oligochaeta is a paraphyletic stem group (traditionally be adopted in this group. One of the main factors contribut-
treated as a subclass) of the class Clitellata that is separate ing to this situation is the advent of molecular methods that
from the advanced, sucker-bearing clitellates: Hirudinea, enabled DNA sequencing of gene fragments. By giving an
Acanthobdellida, and Branchiobdellida. They are some- access to new characters, DNA sequences have led to a fun-
times called “earthworms” after their bigger and better- damental reappraisal of current classifications (see Adoutte
known terrestrial representatives (the so-called megadriles). et al., 2000). In 2006, Jamieson and Ferraguti (2006) pro-
However, many of them are small worms, from about posed a revision of the phylogenetic classification of oli-
1 mm to a few centimeters in length (microdriles), living in gochaetes, which integrates the most recent molecular data
aquatic and terrestrial habitats (Figure 21.1). The nickname available at that moment. However, such a classification
“sludge worms” has been coined for some species of the remains uncompleted and unstable, due to constant prog-
family Tubificidae abundant in polluted watercourses. Up to ress in the molecular field. Molecular studies have also con-
the 1960s, the freshwater polychaetes Aphanoneura (fami- firmed the long-suspected paraphyly of the Oligochaeta if
lies Aeolosomatidae and Potamodrilidae) were also classi- the group does not include branchiobdellids and leeches, so
fied in the Oligochaeta (Brinkhurst and Jamieson, 1971). that Clitellata has become synonymous with “Oligochaeta”
The Oligochaeta includes about 5000 valid nominal (Martin, 2001; Siddall et al., 2001; Martin et al., 2008).
species distributed between 30 or so families. More than Another complication in the nomenclature of aquatic
1100 species of 13 families live in freshwater (Martin et al., oligochaetes arose after the family Naididae was included
2008), while the remainder inhabits terrestrial soil or marine into Tubificidae as a subfamily (Erséus et al., 2002), while
Thorp and Covich’s Freshwater Invertebrates. http://dx.doi.org/10.1016/B978-0-12-385026-3.00021-8
Copyright © 2015 Elsevier Inc. All rights reserved. 529
530 SECTION | IV Phylum Annelida
FIGURE 21.1 Examples of freshwater Oligochaeta (live pictures): (a) Stylaria lacustris (Naididae; note a budding zone in the midbody); (b) Ilyodrilus tem-
pletoni (Tubificidae; note the clitellum); and (c) Lumbriculus variegatus (Lumbriculidae). Scale: a–b = 1 mm, c = 5 mm. Photo by Patrick Martin. Copyright ©
2015 Dr Patrick Martin. Published by Elsevier Inc. All rights reserved.
Chapter | 21 Clitellata: Oligochaeta 531
the name Naididae appeared to be a senior synonym of the present in polychaetes. Also, a certainly nonadaptive, rudi-
Tubificidae (Erséus et al., 2008). Translating phylogenetic mentary upper tooth occurs in the paired sigmoid chaetae of
analyses into biological nomenclature can make the latter the Lumbriculidae and even some Haplotaxidae. As a rule,
impracticable for many purposes (Timm, 2012). For this the Haplotaxidae are considered to contain the most primi-
reason, the senior author is in favor of maintaining para- tive oligochaetes known (Kathman and Brinkhurst, 1998).
phyletic taxa in this chapter, for the sake of a workable However, this interpretation is now questionable. This fam-
classification, namely the traditional family Tubificidae in ily, with “simple” anatomy, was recently shown to have no
its former sense (as the stem group for the Naididae, Pris- basal position within the clitellates, and was confirmed as
tinidae, and Opistocystidae), and the whole subclass Oligo- the closest taxon to the Crassiclitellata, although as a para-
chaeta (hence clitellates exclusive of branchiobdellids and phyletic assemblage (Martínez-Ansemil et al., 2012). More
leeches). generally speaking, the displacement of taxa long thought
to represent successive grades of complexity at the base of
Phylogenetic Relationships a tree to much higher positions inside the tree is probably
one of the salient results obtained with genetic data. This
Oligochaeta have been treated as successors to marine
can be illustrated by the Metazoan example in Adoutte et al.
polychaetes that adapted to life in freshwater and soil by
(2000). Since then, this observation was repeatedly made in
developing a clitellum-secreted cocoon for protection their
other groups; the Haplotaxidae is just another example of the
eggs and embryos, adopting hermaphroditism, concentrat-
obligation to reconsider our older evolutionary reasoning.
ing the reproductive organs into a few segments (thereby
According to alternative opinion shared, for example by
testes always located anterior to the ovaries), and losing the
Timm (1981), the “first oligochaete” likely had hair chaetae
parapodia, cirri, and nuchal organs. However, all these char-
and sigmoid, bifid crotchets like many extant polychaetes
acters exist separately in some marine polychaetes and may
and aquatic oligochaetes. This is supported by the indepen-
have served as preadaptations. On the other hand, many
dent, secondary loss of hair chaetae and the gradual loss
extant polychaetes have invaded freshwater or soil without
of the upper tooth of sigmoid chaetae in many lower taxa.
similar anatomical changes. Two more characters—the dor-
The weak points of this theory are the reduced number of
sal position of pharyngeal pad and the shift of brain back-
gonads (mostly to two pairs) in the extant aquatic oligo-
ward from prostomium—are shared by oligochaetes and
chaetes other than haplotaxids, as well as the trend toward
the terrestrial polychaete (?) Hrabeiella, once assumed to
paired sigmoid chaetae, which have independently arisen
be their sister taxon (Purschke, 2003), a phylogenetic rela-
in several clades. The latter characteristic is established in
tionship not supported by later molecular studies (Jördens
the Lumbriculidae, Haplotaxidae, “true earthworms,” and
et al., 2004; Rousset et al., 2007). A recent phylogenomic
some other taxa, and appears to be developing in the Enchy-
study by Struck et al. (2011) has recovered the Clitellata
traeidae. In all probability, the “ancestral oligochaete” had
within polychaetes with strong support, and thus rendered
a variable number of chaetae of different types and a set of
the Polychaeta paraphyletic. The name Pleistoannelida was
four pairs of gonads. All modern combinations of chaetae
coined for a major clade of annelids by Struck (2011), split-
and gonads can be derived from this condition by reduction
ting into the sister taxa Errantia and Sedentaria sensu Struck
of separate elements. A review of different theories, and a
et al. (2011). The Clitellata are now nested within the Sed-
modern scheme of the phylogeny of Clitellata that takes
entaria, a clade characterized by adaptations to a sedentary
into account gene sequences, was developed by Erséus
lifestyle by reductions of head and body appendages and
(2005). Jamieson and Ferraguti (2006) generated their own
the position of the chaetae being in closer proximity to the
classification, as a result of their synthesis of current mor-
body wall than Errantia. Interestingly, the genetically most
phological and molecular knowledge of oligochaetes. In a
ancient extant oligochaete families, Capilloventridae and
conservative approach, the classification below developed
Randiellidae, live in marine habitats (Erséus, 2005), as do
is an attempt to reflect the most consensual point of view
the vast majority of polychaetes.
in the community of oligochaete specialists, although it is
Brinkhurst (1984, 1994) developed an elegant theory
clearly provisional, pending future revision. The main large
of oligochaete phylogeny based on their reproductive sys-
groupings of Oligochaeta can be defined as follows (see
tem. According to this, the original number of gonads was
also Figure 21.2):
four pairs (two pairs of both testes and ovaries) in segments
X–XIII, as preserved in the typical representatives of the 1. T
he order Tubificida contains the sole clade with hair
family Haplotaxidae. The haplotaxids reveal also the sim- chaetae (although the latter often being lost). The number
plest male ducts. This theory treats the paired, simple- of gonads is usually two pairs, either in X–XI or XI–XII,
pointed chaetae typical of the Haplotaxidae and many other, while spermathecae are aligned to gonadal segments. The
mostly burrowing oligochaetes as an ancestral character. typical representatives are the burrowing Phreodrilidae
However, it ignores the resemblance of the multiple hair and and Tubificidae, and derived from the latter, phytophi-
bifid chaetae typical of many aquatic oligochaetes to those lous Naididae, Pristinidae, and Opistocystidae, with
FIGURE 21.2 Location of reproductive organs in different families of Oligochaeta. Redrawn after Martin and Aït Boughrous, 2012.
prevailing vegetative reproduction and shifted position earthworms” or the suborder Crassiclitellata (with char-
of the reproductive system. The hair chaetae, if pres- acteristic multilayered clitellum), as well as the small,
ent, are usually delimited to the dorsal bundles, while freshwater “microdrile” suborder Alluroidida, with the
two small families, Capilloventridae and Parvidrilidae, families Alluroididae and Syngenodrilidae. Their chae-
contain also ventral hair chaetae. Male ducts are plesio- tae are paired, sigmoid, and simple-pointed (except
porous and mostly equipped with atria, but are without the perichaetine chaetae of some tropical earthworms,
them in the most primitive group, Capilloventridae, which are numerous and not arranged into bundles).
where also a “sterile” segment between the testicular 6.
The family Moniligastridae (the only family of the
and ovarial segment can occur. Spermathecae also lie order Moniligastrida) reveals basically microdrile inter-
further forward in Capilloventridae. The Tubificida are nal anatomy but with testes closed in special capsulae
aquatic, either freshwater or marine. together with male funnels, and terrestrial “earthworm”
2. The order Enchytraeida contains the mostly terres-
appearance and way of life.
trial (with few marine and freshwater genera) family 7.
A monospecific, South American family, Narapidae,
Enchytraeidae, with simple-pointed chaetae in variable apparently belongs to its own order Narapida and con-
number per bundle, two pairs of gonads in XI–XII, ple- sists of tiny riverine worms without chaetae, with testes
sioporous male ducts without true atria (but often with a in the V segment, and with ovaries and spermathecae
complex penial apparatus), and spermathecae located far in the VII segment; in addition, the plesioporous male
forward from the gonadal segments. Two small, aquatic ducts include atria and penes.
families may be phylogenetically related to the root of
Thus, the Clitellata may have derived from an aquatic,
Enchytraeidae: the freshwater Propappidae, differing
sediment-dwelling, polychaete-like ancestor characterized
from the enchytraeids by bifid chaetae and a sterile seg-
by possession of variable number and shape of chaetae and
ment XII separating the testicular and ovarial segment;
by plesiopore male ducts. A trend toward loss of hair chae-
and the marine Randiellidae, with one to two pairs of
tae and the upper tooth of the bifid sigmoid chaetae, as well
testes and with very simple male ducts.
as a trend toward paired chaetae or toward a gradual loss
3. The order Haplotaxida contains the freshwater family
of chaetae, can be observed in many separate genera and
Haplotaxidae, typically with four pairs of gonads (but
families. Atria, prostatic glands, and penial structures seem
partially reduced in some species), very simple male
to be convergently arisen in different clades, as well as the
ducts, spermathecae in variable number and position
alignment of spermathecae to other genital pores.
anteriad to the gonadal segments, and paired or single
sigmoid, usually simple-pointed chaetae per bundle. The
monospecific family Tiguassuidae (with single pairs of
Distribution and Diversity
testes and ovaries) can also be related to Haplotaxida.
The Haplotaxidae were treated as paraphyletic to most Oligochaeta is a cosmopolitan group, and so are some of its
other oligochaete families by Brinkhurst (1984) but freshwater families. The Naididae is probably the most cos-
only to Crassiclitellata by Timm (1981). Jamieson et al. mopolitan freshwater oligochaete family, being present in
(1987), Erséus et al. (2010), and Martínez-Ansemil all biogeographic regions, including sub-Antarctic islands,
et al. (2012) also placed the Haplotaxidae closer to as is the subfamily Rhyacodrilinae within the Tubificidae.
Crassiclitellata (and Lumbriculida) than to Tubificida. Species of the family Haplotaxidae are known on all conti-
4. The order Lumbriculida appears paraphyletic, if
nents except Antarctica.
you exclude the advanced, carnivorous, leech-like The family Tubificidae is most diverse in the Northern
Branchiobdellida, Acanthobdellida, and Hirudinea Hemisphere, although several endemic genera are known in
(which are treated in separate chapters of this book). Australia and South America. In the last few centuries, sev-
They can be characterized by prosoporous or semiproso- eral anthropochorous tubificids of Holarctic origin have been
porous male ducts. The freshwater family Lumbriculidae introduced and became common in the southern temperate
reveals strictly paired chaetae, either simple-pointed or zone. Tubificids are not so diverse and common in the trop-
with a rudimentary upper tooth, while the male ducts ics, being represented there mainly by the architomic genera
are equipped with atrium and prostate glands; there like Aulodrilus and Bothrioneurum. The only tubificid spe-
are three or two pairs of gonads, and spermathecae are cies reproducing exclusively by sexual means, and common
aligned to gonadal segments. A puzzling, small family, also in tropical countries, are Limnodrilus hoffmeisteri and
Dorydrilidae, is similar to the lumbriculids in all fea- Branchiura sowerbyi. The first of them originates from the
tures but their (secondarily?) plesioporous male ducts. temperate zone but is able to reproduce also at persistently
5. The order Opisthopora is a large, monophyletic clade high temperatures, while the second one even breeds more
with opisthoporous male ducts and includes the numer- effectively at temperatures over 20 °C. Humans have unin-
ous “megadrile” families of the mostly terrestrial “true tentionally spread these two taxa among many equatorial
regions. Anthropochorous exchange of tubificids between the last several million years. The Baikalian fauna is rather
Europe and North America has been intensive in the twen- saturated; and, in light of this rift lake’s special physical
tieth century, as demonstrated, for example, by the recent conditions, the ecosystem is considered inhospitable for
appearance of Potamothrix spp. and many other European possible newcomers from the “common” Palaearctic water
species in the Great Lakes, as well as by the presence of bodies (Semernoy, 2004). Most of the Baikalian oligochaete
Quistadrilus multisetosus, V arichaetadrilus harmani, and species and many genera are endemic; species flocks are
several American Limnodrilus species in Western Europe. even recognizable or suspected (Martin, 1996). The most
Many older exchanges between Nearctic and Palaearctic diverse families are Lumbriculidae (particularly the genera
fauna may have occurred. The original homeland of the Lamprodrilus, Rhynchelmis, and Stylodrilus), Tubificidae
peregrine Tubifex tubifex is obscure, but it may have been (Baikalodrilus, Isochaetides, Rhyacodrilus, etc.), and Nai-
derived from the Western Palaearctic, because this species didae (Nais, Amphichaeta, and Chaetogaster). An evolu-
is absent from the natural water bodies of extreme north- tionary radiation is in progress there, which was originally
eastern Asia. based on a limited number of founding species coming from
The families of Naididae and Pristinidae, with their pre- surrounding waters. This modern radiation, rather than the
vailing asexual reproduction (and thus not so affected by relict character of fauna as once assumed by Michaelsen
lack of seasonally cooler temperatures), are common both (1902), may be the reason of the richness of the Baikalian
in the tropical and in temperate zones. The gill-bearing gen- oligochaete fauna. However, discovery of some rare species
era Dero and Aulophorus are particularly diverse in the hot in Europe that are congeneric with Baikalian endemics (in
regions. However, many naidids common in the temperate the genera Pseudorhynchelmis and Rhyacodriloides) can be
climate (e.g., Stylaria lacustris) are lacking in the tropics. explained by their relict character. A possible source of the
Most naidid species of the temperate zone of southern con- Baikalian cool-water oligochaetes, besides the open water
tinents like Australia and South America were probably bodies, may be the groundwater fauna, as suggested by the
introduced from the Holarctic. occurrence of Phallobaikalus gladiiseta in this lake, a rep-
The family Lumbriculidae is certainly Holarctic, with resentative of a primarily marine tubificid subfamily, the
most endemic species living in the cool subarctic or alpine Phallodrilinae, which is known to be occasionally present in
water bodies or in groundwaters. Only a few species are groundwaters as well (Creuzé des Châtelliers et al., 2009);
widely distributed in the summer-warm open waters; and unfortunately, the groundwater fauna is virtually unstudied
only one of them, the architomic Lumbriculus variegatus, in Siberia. The smaller lakes of the Baikalian Rift (Lake
is not dependent on sexual reproduction. Humans have suc- Hubsugul, Lake Oron, etc.) reveal a few endemic species
cessfully distributed that oligochaete on several temperate related to the Baikalian ones.
regions of the Southern Hemisphere. Several smaller Holarctic ancient lakes like Tahoe,
The terrestrial/amphibious/marine family Enchytraeidae Ohrid, Issyk-kul, and Biwa have each developed a small
is cosmopolitan. Their intrusions from soil into fresh water selection of their own endemic oligochaetes. The Lauren-
occur independently on all continents. tian Great Lakes of North America are comparable with the
The small freshwater families of Propappidae and Baikal in their ecological conditions, but they have arisen
Dorydrilidae are Palaearctic in distribution, while the Par- only in the Holocene and are therefore too young to have
vidrilidae occur also in North America. In contrast, the formed an endemic fauna. On the contrary, they are rather
family Opistocystidae is architomic and, therefore, able to hospitable for immigration of lacustrine oligochaetes from
live in tropical waters, where it is limited to the Americas Europe. The oligochaete fauna of the great African lakes
and Africa. The family Capilloventridae was originally (Tanganyika, Malawi, etc.) is very scarce, although these
described from sea but later found also from Austra- lakes are hardly younger than Lake Baikal. This is partly
lian freshwaters. The family Phreodrilidae, an ecological due to an obvious lack of studies, but it is probably also
equivalent of Tubificidae but of Gondwanan origin, occurs because these lakes provide a less favorable environment
in Australia, South America, Asia (Sri Lanka and the Ara- for most aquatic oligochaete groups (too warm, profundal
bian Peninsula), and southern Africa, with a relict species region anoxic) (Martin, 1996).
(Astacopsidrilus naceri) in North Africa and some recent Another special hot spot for the evolution of the Palaearc-
introductions in Ireland and Japan. tic freshwater Oligochaeta is the Ponto-Caspian Subregion
Lake Baikal is an extraordinary hot spot of diversity (the Black, Azov, and Caspian Seas together with lagoons
for Oligochaeta as well as for some other animal groups. and estuaries). The great water bodies of this basin have been
Indeed, it has even been treated as a separate freshwater alternatively fresh, brackish, and saline, and they have been
zoogeographic region! This large rift lake has existed in one connected with each other or separated for long geologi-
form or other for at least 20 million years. Its waters are cal periods beginning with the Tethys Ocean. Many local
typically cool and well supplied with oxygen down to its endemic tubificid and naidid species have arisen there and
maximum depth (∼1.6 km) (Martin et al., 1998) for at least are able to survive in both brackish and fresh waters. On the
other hand, at least three species of the otherwise strongly is characterized by many naidids and tubificids apparently
freshwater family Lumbriculidae (Stylodrilus cernosvitovi, introduced from the north and often dominating over the
S. parvus, and Trichodrilus pauper) have adjusted to the local ones. Phreodrilidae can also be diverse but are mostly
brackish water of the Caspian Sea. In the Holocene and in Australia. In tropical countries, the freshwater oligochaete
after the retreat of the continental ice from northern Europe, fauna is usually represented by some genera of the families
several Ponto-Caspian species of the genera Potamothrix, Naididae (particularly Dero, Aulophorus, and Allonais), Pris-
Psammoryctides, etc. successively colonized the emerging tinidae, and a very limited number of Tubificidae. However,
new freshwater bodies—a process accelerated by humans in species of other families can sometimes dominate, such as
the last few centuries (Milbrink and Timm, 2001). Narapa bonettoi and Haplotaxis aedeochaeta on the unvege-
Since 2000s, a cluster of endemic Potamothrix spp. tated sand bottom in the Paraná River system, South America.
(probably related to the Ponto-Caspian ones) was discovered
in the well-oxygenated profundal of the deep mountain Lake
Fuxian (southern China). They may represent relicts of the GENERAL BIOLOGY
other, eastern end of the Tethys Ocean. Lake Fuxian is too
warm and located too far south for colonization by any Lum-
External Anatomy
briculidae characteristic of Lake Baikal. Oligochaetes are bilateral, segmented, vagile annelids sharing
Subterranean fauna of the regions not glaciated in Holo- with polychaetes two types of chaetae (hairs and crotchets)
cene is characterized by many small endemic oligochaetes, and their location in four bundles, but lacking the parapodia
mainly tubificids and lumbriculids. These have been most and paired head appendages. The size of freshwater oligo-
extensively studied in Europe, but they have also been chaetes varies usually between 1 mm and several centime-
investigated in arid southwestern Australia, where many ters. Their body is mostly soft and smooth, but in some taxa
endemic phreodrilids occur. The Holarctic Parvidrilidae it can be covered with armor formed by epidermal papillae
can be considered the most representative oligochaete fam- and/or secretion and adhered particles. The first segment, or
ily in groundwater, with all its nine constitutive species peristomium, surrounding the mouth, is always devoid of
restricted in distribution to such habitats (Martínez-Ansemil chaetae. Roman numerals are conventionally used for mark-
et al., 2012). Occasionally, subterranean oligochaetes occur ing the segments, and Arabic numerals for the intersegmental
in springs together with epigean species. A succession furrows or dissepiments (e.g., 3/4 is the furrow between seg-
of the oligochaete fauna along the river from headwaters ments III and IV). In addition to a basic segmentation that
downstream can be observed, with the most oxyphilous corresponds to the succession of metameres, a secondary
species living in the cool, stony rhitral and more tolerant, annulation is sometimes present in some of the anterior seg-
psammo- or pelophilous ones in the potamal sections of ments: the segments are divided into annuli that may make
the river. Many rheophilous oligochaetes can exist also in it difficult to determine the limits of the segments. A small
the well-aerated surf zone of lakes. A few species, e.g., the tactile appendage, the prostomium, is attached to the peristo-
genus Lamprodrilus (Lumbriculidae), occur only in stand- mium above the mouth; sometimes it can be extended into an
ing water bodies. In North America, a particularly diverse, unpaired proboscis. A pair of pigmented eyespots can occur
endemic oligochaete fauna occurs in the running waters of on the prostomium in some Naididae. Only a few oligo-
the western mountain ranges, as well as in the southeastern chaetes have external gills: those in Branchiodrilus cover the
United States. anterior hair chaetae; segmental finger-like gills are present
The most diverse oligochaete fauna in the northern tem- dorsally and ventrally on the hind body of B. sowerbyi and
perate zone, which consists mostly of the naidids, tubificids, laterally in Phreodrilus branchiatus; and a limited number
and lumbriculids (phreodrilids can occur in similar habitats of gills and/or palps surround the anus in Dero, Aulophorus,
in Australia), occurs in the vegetation-rich shallows of lakes, and members of the family Opistocystidae. Chaetae (called
small streams, and rivers where a successful bottom grab or also setae) are present in four bundles (two ventral, two dor-
pond net sample can often reveal 10–12 species. This number sal or dorsolateral) on each segment except the first. They are
usually declines in deeper river habitats due to more monot- sometimes absent on the genital and some other segments,
onous (unvegetated) sediment, and in the lake profundal but they are seldom entirely lacking. Two basic types of
because of low dissolved oxygen levels. Lake Baikal serves chaetae are present: sigmoid and hair chaetae (Figure 21.3).
as an exception to this latter pattern because its sediment is Short, mostly S-shaped (sigmoid) chaetae or crotchets
well oxygenated at all depths. Consequently, Lake Baikal are characterized by a more or less median swelling (the
has far more than 200 species of Oligochaeta, most of them nodulus) and a bifid distal tip. The two teeth (or prongs) of
endemic (Semernoy, 2004). For comparison, the well-studied the ectal end are called the upper (distal) and lower (proxi-
temperate Lake Peipsi-Pihkva and Lake Võrtsjärv, in Esto- mal) teeth. The bifid chaetae, modified with presence of
nia, have only 59 and 54 oligochaete species, respectively. intermediate denticles or a wavy web between the two
Freshwater oligochaete fauna of the southern temperate zone teeth, are called pectinate or comb-like chaetae. The teeth
The second basic type of chaetae in many aquatic Oli-

gochaeta of the order Tubificida is hair chaetae (also called
simply “hairs”). They are long and gradually thinning dis-
tally, without any nodulus, and usually with a fine simple-
pointed tip. The hair chaetae can be irregularly covered by
fine hairs (then called hirsute or pilose chaetae). The latter
can be distributed in one or two longitudinal rows (on ser-
rate or plumose hair chaetae, respectively). Most often, the
hair chaetae look smooth in a light microscope. However,
scanning electron microscope photos demonstrate a fine
pilosity in many apparently smooth hair chaetae, as well
as the presence of occasional fine intermediate denticles
in apparently bifid crotchets. Lack of the hair and pecti-
nate chaetae in ventral bundles was regarded as a character
discriminating Oligochaeta from the nonoligochaete Aeo-
losomatidae bearing hair chaetae in all bundles. However,
ventral hair chaetae are present in the recently discovered
small oligochaete families Capilloventridae and Parvid-
rilidae. The function of the hair and pectinate chaetae is
unclear and apparently not always vital, since they have
been replaced by bifid crotchets in separate species of the
same genus and sometimes even within a species. Chaetae
can be more numerous and diverse in the anterior portion
of the worm, while becoming gradually more scarce and
uniform in the tail portion.
The clitellum is an external, often conspicuous repro-
ductive organ present during sexual maturity in all oli-
gochaetes and other Clitellata (Figure 21.1(b)). This is
FIGURE 21.3 Types of chaetae in Oligochaeta:(1–5) hair chaetae: 1, a muff-like or saddle-shaped, glandular thickening of the
smooth; 2, pilose; 3, feathered; 4, serrated; 5, with supporting chaetae;
mucous epithelium of body wall. It typically covers several
(6–17) short chaetae: 6, common bifid crotchet with equal teeth; 7, with
shorter lower tooth; 8, with shorter upper tooth; 9, simple-pointed; 10, pec- segments, usually including those bearing male and female
tinate; 11, palmate; 12, needle chaeta with equal teeth; 13, with shorter genital pores, but it may be located several segments pos-
upper tooth; 14, simple-pointed crotchet without nodulus; 15, stick-shaped teriorly of the genital pores in some earthworms (suborder
chaeta; 16, furrowed spermathecal chaeta; 17, obtuse penial chaeta; Crassiclitellata).
(18–27) chaetal bundles: 18, dorsal bundle with hair and bifid (or pecti-
Genital pores are usually present on the ventral side of
nate) chaetae; 19, dorsal bundle with a single hair and needle chaeta; 20,
bundle of bifid crotchets; 21, paired simple-pointed crotchets; 22, bundle these worms. Male pores are often prominent, lying on a
of penial chaetae with converged distal tips; 23, Mesenchytraeus-type; 24, glandular protuberance or (seldom) on an external penis.
Lumbricillus-type; 25, Enchytraeus-type; 26, Fridericia-type; 27, paired The pores are either on segments XII, XI, or X (or IX–X)
stick-shaped chaetae. Original drawing by Tarmo Timm. in most aquatic oligochaetes but further back in terrestrial
earthworms. Female pores (mostly one pair, but two pairs
in some Haplotaxidae) are inconspicuous and located in
can be of uneven length and thickness; in particular, the intersegmental furrows either immediately posterior to the
upper tooth may be reduced or even disappears. Chaetae male pores or one segment caudally (but before the male
in some species can be spade-like, brush-like, or of some pores in most “earthworms”). Spermathecal pores can
other form. Most terrestrial groups bear simple-pointed lie immediately before and/or after the male and female
chaetae (sigmoid, or straight and stick-shaped), and may pores, or several segments anteriorly. They are present
lack a nodulus. In some aquatic taxa, the dorsal bifid chae- either ventrally, laterally, or dorsally, and are sometimes
tae are modified as straight, sharp-tipped needles, which unpaired. Spermathecal pores are often distinct like the
are either bifid or simple-pointed. A trend expressed in male pores. Ventral chaetae at the male and spermathecal
several oligochaete groups is the assumed reduction of the pores can be modified into genital chaetae (penial or sper-
originally indefinite number of chaetae per bundle to two mathecal, respectively). Penial chaetae are usually blunt-
(the paired chaetae) and, seldom, to one or no chaetae. The tipped; when several are present in a bundle, their distal
ventral chaetae located at genital pores can be modified as tips converge. They seem to be used for attachment and
genital chaetae (see below). sperm transfer into the spermathecae of the concopulant.
The penial chaetae (as well as unmodified ventral chaetae)

are usually lacking at male pores when internal chitinous
penial sheaths exist; these probably have a similar function
in facilitating sperm transfer into the spermathecae during
copulation. The spermathecal chaetae are mostly sharp-
tipped, with a longitudinal furrow, and are often equipped
with a distinct gland at their base. In all probability, they
act as piercing chaetae, whose principal role is a mechani-
cal or chemical stimulation, the latter via the inoculation of
secretions into the partner’s body at copulation (Cuadrado
and Martínez-Ansemil, 2001). In some rare cases, modified
chaetae of spermathecal type can occur both at the sperma-
thecal and male pores (e.g., in the tubificid genus Haber).
A forward shift of the whole genital system occurs indi-
vidually after regenerating the anterior end in those genera
or species capable of asexual reproduction by architomy,
or fragmentation.
Internal Anatomy
Internally, the body cavity of each segment is usually sepa-
rated from that of neighboring segments by muscular–
epithelial dissepiments (septa); coelom of every segment
is, in turn, divided into left and right parts by a mesentery.
Coelomic corpuscles of various sizes and structures—the
so-called coelomocytes—can float freely in the coelom
fluid of several oligochaete taxa.
The digestive tract of Oligochaeta is a strict longitudinal
tube consisting of five to six consecutive sections. A simple
mouth cavity is followed by a pharynx, which is charac- FIGURE 21.4 Scheme of blood circulation system of the tubificid
terized by a dorsal, muscular-glandular roof called pharyn- Tubifex tubifex, by d’Udekem (1853), from Wesenberg-Lund (1939).
geal pad. This pad can be everted for collecting small food
particles. Bodies of paired pharyngeal glands can reach for pulsating “hearts,” while transverse vessels in the posterior
several segments backwards and are then also called “sep- segments can be turned into blind appendages of the dorsal
tal glands” because they attach to the dissepiments. Both vessel (Figure 21.5). In addition, a blood sinus is common
the pharyngeal pad and glands tend to degenerate in preda- inside the intestinal wall; and in larger worms, other smaller
tory oligochaetes like Chaetogaster and Phagodrilus whose vessels may be present. Dissolved erythrocruorin gives the
pharynx is entirely muscular. A narrow esophagus follows blood a red or pink appearance in many oligochaetes when
the pharynx and enlarges into a midgut or intestine after the worm is alive.
several segments. Sometimes the beginning of midgut is The excretory system includes a number of paired meta-
dilated and then called stomach. The midgut nearly fills the nephridia, or segmental organs, located in many segments
coelom cavity of most body segments, narrowing whenever except the genital and some anterior segments. A metane-
piercing a dissepiment. The midgut, as well as the poste- phridium consists of a ciliated funnel on the anterior surface
rior portion of esophagus, is covered with a layer of darker of a dissepiment, with a duct piercing the dissepiment and
cells, the chloragogen tissue. The simple hindgut occupies winding in the cavity of the next segment before opening
a few hindmost segments. Different appendages and modi- through a ventral pore.
fied portions of the wall can occur at the esophagus or the The central nervous system consists of a ventral nerve
beginning of intestine, in some taxa. cord (with a pair of merged ganglia in every segment except
The blood circulatory system always includes at least the foremost ones), dorsal brain, and circumpharyngeal
one dorsal and one ventral longitudinal vessel. The dorsal nerve ring linking the brain and cord. The brain is located
vessel pulsates, pumping blood forward. The two vessels slightly posterior to the prostomium, usually in the segments
are interconnected in some segments by pairs of transverse I–III. Three giant nerve fibers in the ventral nerve cord
vessels (Figure 21.4). A pair or two of these transverse ensure a quick information exchange between the brain and
vessels in the forebody can be modified into muscular, tail and rapid contraction in response to mechanosensory
FIGURE 21.5 Branched, blind, lateral blood vessels on the posterior segments of Lumbriculus variegatus (live picture). Scale = 200 μm. Photo by
Patrick Martin. Copyright © 2015 Dr Patrick Martin. Published by Elsevier Inc. All rights reserved.
irritation. External sense organs are represented by incon- Male ducts include a ciliated sperm funnel at the posterior
spicuous sensory papillae, which are more abundant on wall of the testicular segment and a sperm duct or vas
the prostomium. In armored species, the papillae are more deferens piercing the dissepiment and usually winding in
prominent and penetrate through the armor. Light-sensible the coelom of the next segment. Vas deferens can open
sensors are present in the body wall of most oligochaetes, through a simple male pore in the body wall, as in Haplo-
but pigmented eyespots on the prostomium occur only in taxidae or Crassiclitellata. More often, the invaginations
some Naididae. of body wall have formed various terminal elements of
The presumably ancient condition of four pairs of the male duct, called atria and penes in Lumbriculidae,
gonads—with testes in segments X and XI and ovaries in Tubificidae, and some others, or penial bulbs in Enchy-
XII and XIII—has been preserved in most Haplotaxidae. traeidae. The atrium is a spacious chamber with glandu-
This number is reduced to one to two pairs of testes and lar walls, serving for collecting sperm before copulation.
one pair of ovaries in other families (Figure 21.6). Most The bodies of the gland cells of the atrial wall are called
often the single pairs of testes and ovaries are located in prostatic glands when bulging into the coelom. They
their original segments XI and XII, respectively (Enchy- can cover the outer surface of atrium (diffuse prostate)
traeidae, Phreodrilidae, many Lumbriculidae, etc.), or or form aggregations sending their secretions into atrial
in X and XI (Tubificidae and some others). Developing lumen by a common narrow stalk (compact prostates; not
gametes usually float freely in the coelom of the gonadal to be confused with the homonymous prostates of many
segments. To provide sufficient space for them, the poste- megadriles, which are different, separate organs located
rior (or also anterior) wall (dissepiment) of a gonadal seg- near the male genital pores). When the distal end of the
ment will bulge into a neighboring segment(s) to form a atrium is modified for protrusion during copulation, it is
sperm or egg sac. The posterior egg sac always surrounds called pseudopenis. The atrium can also terminate with a
the sperm sac, and the ripe eggs lie usually caudad from true penis, surrounded by a penial sac when not protruded
the sperm mass. These sacs can reach for many segments (seldom is a penis permanently external, e.g., in Stylodri-
behind the clitellum. The accumulation of gonadal prod- lus heringianus). Sometimes there is a narrow ejaculatory
ucts in sacs gives a milky-white appearance in the region duct between the atrium and penis. The penis can be either
adjacent to the clitellum, and is the most conspicuous ele- completely soft or surrounded by a more or less chitinized
ment of the reproductive system in superficial observa- penial sheath. Male pores, located near or instead of the
tion. Gonoducts are almost always paired like the gonads. ventral chaetal bundles of the respective segment(s), are
FIGURE 21.6 Reconstruction of reproductive organs of one side in the tubificid Embolocephalus velutinus. at = atrium; de = ejaculatory duct; ff = female
funnel; mf=male funnel; o =ovary; pa = penial apparatus; pr = prostate gland; st = spermatheca; sts = spermathecal chaeta; t = testis; vd = vas deferens. From
Holmquist (1978).
FIGURE 21.7 Types of male duct in Oligochaeta. From Martin and Aït Boughrous (2012).
usually the most prominent external genital organs beside segment and make a loop before piercing again its dissepi-
the clitellum. ment, or only cling to its anterior surface before joining the
Michaelsen (1929) coined three useful terms to describe atrium. Sometimes the male pores of the left and right side
the types of male gonoduct (Figure 21.7): plesiopore (with can open into a common, median copulatory chamber, or
external pores in the segment following the testicular one, there can be a single, unpaired atrium receiving all vasa
as in most aquatic oligochaetes), prosopore (with pores in deferentia. Female ducts consist only of a ciliated funnel
the same segment with the testes, as in Lumbriculidae and at the posterior wall of the ovarial segment and a vestigial
many of their leech-like relatives), and opisthopore (with canal penetrating the dissepiment, with an inconspicuous
the male pore several segments backwards, as in the Crassi- female pore in the intersegmental furrow, in the line of
clitellata). Many Lumbriculidae display a semiprosopore ventral chaetal bundles. Spermathecae are another impor-
condition when the first pair of vasa deferentia lack their tant element of the reproductive system because they retain
own atria and join atria of the second pair (thus being, in the partner’s sperm after copulation and before egg lay-
fact, plesiopore). Prosoporous vasa deferentia of the tes- ing. Their number and location vary among taxa, from one
ticular segment can either penetrate in the posttesticular single spermatheca to many pairs, and from being in the
immediate neighborhood of the male and female pores and and Cognettia). A limited, species-specific number of seg-
clitellum (e.g., in the segment preceding them in Tubifici- ments is always regenerating anteriorly on the anterior end,
dae and Naididae, before or after them in Lumbriculidae) and the single or first pair of testes is then developing in
to many segments before them (e.g., in Enchytraeidae and the last regenerated segment (Hrabě, 1981). In paratomic
Lumbricidae). They can be simple sacs inverted from the families of Naididae and Pristinidae, such a relatively ante-
body wall, or be differentiated into spermathecal ampulla rior position of the genitalia (with testes in IV, V, or VII) is
and external duct. The ampulla can bear diverticula, and the genetically fixed. The extensive backward shift of the whole
duct can be covered with a glandular layer or bear separate genital system in some of the paratomic Opistocystidae has
glands. The sperm contained in the ampulla or diverticula no reasonable explanation.
can be amorphous or arranged into bundles or even sper-
matozeugmata (characteristic of most Tubificinae, but also
rarely present in the Limnodriloidinae, Phallodrilinae, and Physiology
Rhyacodrilinae). A tubificine spermatozeugma consists of The basic mode of locomotion in the sediment-dwelling
fertilizing and nonfertilizing spermatozoa, the latter form- oligochaetes is slow peristaltic crawling. Every external
ing a cortex for the former ones with some sort of cementing vibration or other tactile irritation will result in a momen-
agent (Figure 21.8). In some groups, particularly among the tous contraction of the whole animal. Most oligochaetes are
Enchytraeidae, an internal duct connects the ampulla with thigmotactic, which is why tubificids gather into balls when
the digestive tube, apparently for absorbing the remains of extracted from sediment. Some species of Lumbriculus and
sperm not used for fertilizing eggs. External pores of the Rhynchelmis (Lumbriculidae), as well as most Naididae,
spermathecae can lie in different parts of the respective seg- that spend at least some time among aquatic vegetation can
ment: ventrally, laterally, or dorsally within a segment or in swim short distances with wriggling or spiral movements.
an intersegmental furrow. Spermathecae can be lacking in Most oligochaetes are negatively phototactic, with light-
parthenogenetic individuals of some taxa and also in taxa sensitive cells dispersed in the whole body wall. However,
that attach external sperm packets (spermatophores) to the some Naididae have a pair of primitive eyespots, which they
partner’s body surface. use for orientation.
A forward shift of the whole genital system occurs indi- Oligochaetes transpire (exchange gases) through their
vidually after regenerating the anterior end in genera or mucous body wall and, in rarer cases, with external gills.
species able to reproduce asexually by architomy, or frag- Another important respiratory organ is the ciliated hindgut,
mentation (e.g., Lumbriculus, Aulodrilus, Bothrioneurum, which explains why burrowing tubificids expose their hind
FIGURE 21.8 Spermatozeugmata in spermathecae of Potamothrix hammoniensis. Scale = 100 μm. Photo by Patrick Martin. Copyright © 2015 Dr
Patrick Martin. Published by Elsevier Inc. All rights reserved.
end in the water layer and even try to create vertical water Some other species can live several years without reproduc-
circulation, with “swimming” movements of their tail. For tion unless “hibernation” enables them to undergo the nor-
a similar reason, other worms such as L. variegatus and mal sexual process (Timm, 1987). Most species reproduce
Criodrilus lacuum stretch their tails horizontally along the once a year and then reabsorb the whole system appara-
air–water interference when living in anaerobic mud under tus (except gonads) and apparently become immature until
a thin water layer. the next sexual cycle. Oligochaetes are hermaphrodites,
Gases and various materials are circulated internally, mostly protandric, with the partners exchanging sperm dur-
primarily by the vascular system and secondarily by coe- ing copulation. The clitellum and some special cutaneous
lomic fluid. Blood is especially rich in erythrocruorin in structures, sometimes in combination with penial chaetae
species such as Potamothrix hammoniensis or T. tubifex liv- (Cuadrado and Martínez-Ansemil, 2001; Caramelo and
ing in sediment that is poor in oxygen or even periodically Martinez-Ansemil, 2012), help to hold the partners together
anoxic. Most aquatic oligochaetes are more sensitive to the during this process. The alien sperm is stored in sperma-
scarcity of oxygen and, therefore, inhabit cleaner and/or thecae either as amorphous mass, organized into bundles
cooler water bodies. of different complexity, or as spermatozeugmata consisting
Digestion in oligochaetes depends in part on their inter- of two kinds of spermatozoa, the latter characteristic of the
nal microbial flora. Some bacteria can propagate in their subfamily Tubificinae (see Jamieson and Ferraguti, 2006).
gut and may contribute to the digestive process by helping When spermathecae are absent, the spermatophores are then
decompose high-molecular organic compounds. Assimila- attached to the outside of the partner’s body; this occurs in
tion of dissolved organic material by the body wall has been the tubificids Bothrioneurum and Paranadrilus, the crassi-
demonstrated in some mud-dwelling tubificids. clitellate Criodrilus, and some others. Both the egg(s) and
Metanephridia (or segmental organs) are the primary alien sperm will be laid into a cocoon secreted by clitellum.
excretory organs. In addition, solid excretory products The mother worm sheds the cocoon by crawling backwards,
accumulate in the chloragogen cells covering the intestine. after which the cocoon’s shell will harden and the ends will
These cells darken over time and are partially eliminated by contract into a sealed plug. Eggs are fertilized within the
the seemingly drastic process of autotomy (pinching off) of cocoon, and development is direct. After some weeks, the
the old tail. This is followed by regeneration of a new tail young worms will leave the cocoon. “Microdrile” aquatic
that replaces the old, waste-laden chloragogen cells with worms lay large, yolk-rich eggs. In contrast, the eggs of
new tissue. “megadriles” are smaller, and embryonic growth depends
Growth occurs primarily in the caudal end of oligo- on nutritious fluid secreted into the cocoon by the mother’s
chaetes. New segments are adding one by one to the pos- clitellum. Spermatogenesis occurs earlier than oogenesis and
terior end (anterior to the pygidium), both in the case of at relatively lower temperatures. This explains the observa-
regular growth and in tail regeneration. When the anterior tion that in a moderate, seasonal climate many aquatic oligo-
of the worm requires regeneration, a small unsegmented chaetes mature and copulate in winter or early spring and lay
outgrowth appears initially and then differentiates into a eggs in the beginning of the warmer period.
species-specific number of segments. The number of regen- Although oligochaetes may reproduce only once per
erated segments is often less than the number of lost seg- year in seasonally cool aquatic systems, some species
ments. Genital segments usually do not regenerate (except (e.g., L. hoffmeisteri) can mature rapidly in warmer water
in the species with asexual reproduction). For this reason, and produce several generations per year. Some species
regeneration of anterior segments is limited. (e.g., T. tubifex and Ilyodrilus templetoni) can produce par-
thenogenetic eggs, as confirmed by lack of spermathecae in
many individuals. Some rare taxa also lack the male appa-
Reproduction and Life History ratus, as in Tubifex pomoricus. Parthenogenesis is a way
The individual lifetime of tubificids and lumbriculids in to avoid the temperature problem with spermatogenesis
aquaria often lasts several years and may include several and to produce several generations a year, as in the case of
reproduction cycles. Some individuals of T. tubifex and Spi- T. tubifex and L. hoffmeisteri. However, fecundity gradually
rosperma ferox have reached an age of 10 or more years. decreases over several parthenogenetic generations.
The oldest recorded age was for an individual of C. lacuum Another form of asexual reproduction that completely
(an aquatic “earthworm”), which lived 46 years in an aquar- avoids the resource- and time-consuming sexual process and
ium, although without reproducing. The actual lifetime of egg-laying is vegetative reproduction, either by architomy
the same species in nature is undoubtedly shorter due to or paratomy. Architomy means enhanced ability to regener-
predation. The facultative parthenogenetic species T. tubifex ate a complete animal from separate pieces, after either a
can survive and reproduce in aquaria for many years, even violent attack or spontaneous fragmentation. Architomy is
at a persistent room temperature, as can the architomic almost obligatory in L. variegatus but common also in some
clones of the tubificids Bothrioneurum and Aulodrilus. Tubificidae (e.g., Bothrioneurum, Aulodrilus, Potamothrix
bedoti) and Enchytraeidae (Cognettia and some others). to the surface of plants. Some heavily armored (with papil-
At least in these tubificids, architomy is characteristic of lae) Baikalodrilus spp. (Tubificinae) in Lake Baikal are
warmer periods, whereas at lower temperatures, the process assumed to crawl or roll on the sandy bottom on this lake
ceases and at least some part of the population becomes (Semernoy, 2004).
sexually mature. In Lamprodrilus mrazeki (Lumbriculidae), A few freshwater oligochaetes live on or inside other
architomy occurs in cysts formed in summertime when animals. Some Australian species of Astacopsidrilus (Phre-
pools dry up. odrilidae) live as commensals within the gill chamber of
A more advanced method of asexual reproduction is crayfishes. Chaetogaster limnaei (Naididae) has two sub-
paratomy: the production of a chain of zooids by longitu- species, one as a commensal epibiont on aquatic snails and
dinal budding. This characterizes whole families of Naidi- the other parasitizing their kidneys. All species of the tropi-
dae, Pristinidae, and Opistocystidae. Paratomy can prevail cal genus Allodero (Naididae) are known from the excre-
during favorable seasons, while sexually mature individu- tory organs of tree frogs.
als appear and produce cocoons mostly before a colder or
drought period. The parents then usually die after forming
Physiological Constraints
cocoons.
Distribution of oligochaetes is limited primarily by avail-
ability of dissolved oxygen above and within the sediment.
GENERAL ECOLOGY AND BEHAVIOR The abundance of erythrocruorin in blood is characteristic
Macrohabitat Distribution and Microhabitat of mud dwellers like the tubificids and phreodrilids but not
of the vegetation dwellers like the naidids and pristinids.
Selection Body length can limit the vertical distribution of tubifi-
The most typical habitat of freshwater oligochaetes is the cids in anoxic sediment because worms need to be able
uppermost (several centimeters thick) layer of sediment to reach with their tail end to the overlying aerated water.
where the worm occupies a “tube” (the genus name Tubifex Oxygen deficiency also limits the distribution of oligo-
is derived from this behavior). Tubes are slime-lined walls chaetes into deeper zones of lakes. Oligochaete richness in
of a burrow in soft sediments from which the “head” and Lake Baikal at all depths is greatly due to good aeration
tail may protrude above the sediment surface. Oligochaetes of its whole water mass and the uppermost sediment layer
may reside temporarily in a deeper, anoxic layer of muddy (Martin et al., 1998, 1999). Depth (water pressure) per se
sediment while feeding on bacteria and avoiding predators. has no importance for oligochaetes. Most of them do not
The egg cocoons are also often laid inside sediment. In the need light within their sedimentary burrows and even avoid
interstitial spaces of stony or gravel bottoms, especially in it. Some vegetation-dwelling naidids equipped with eyes
the well-aerated hyporheic zone of the torrent streams, the are an exception to this pattern.
depth distribution of oligochaetes can reach several meters. Many oligochaetes are eurythermic and able to survive
This is a transition zone to the groundwater. The latter is both low (near-zero) and high (above 20 °C) temperatures;
inhabited partially by invaders from surface waters, par- some are even adapted to seasonal freezing, like the tubificid
tially by stenothermic species specific to this habitat, which Alexandrovia ringulata in Arctic tundra lakes. Most of the
are often endemic. Lumbriculidae prefer persistent low temperatures, inhabit-
Some oligochaetes, particularly of the family Enchy- ing either the Arctic, alpine, or underground water bodies.
traeidae, can live equally in freshwater sediment and moist The groundwater species can be stenothermic. The annual
terrestrial soil. temperature regime can delimit distribution of many surface-
Several oligochaete groups have independently adapted water species via the reproduction. For example, the lumbri-
to another habitat—the underwater “forests” of macroveg- culid Lamprodrilus isoporus survives the warm summer but
etation and algae. Here they crawl around on the plants and reproduces only in winter in Lake Peipsi (Estonia). In general,
the sediment surface rather than residing in subsurface bur- maturation, spermatogenesis, and copulation require lower
rows. These include most Naididae, Pristinidae, and Opisto- temperatures than oogenesis and the laying and incubation of
cystidae, and at least some species of the lumbriculid genera eggs. Asexual reproduction by paratomy or architomy is sup-
Lumbriculus and Rhynchelmis. Some species can even pressed by temperatures lower than 10–15 °C. The thermal
swim short distances. For example, small naidids equipped regime (and scarcity of dissolved oxygen at higher tempera-
with long hair chaetae (e.g., Stylaria and Ripistes) have tures) may be the reason for the limited number of aquatic
been observed floating or swimming in the open water. Nai- oligochaete genera in the tropical waters. For example, only
dids, although able to swim (Dero, Aulophorus, Ripistes), L. hoffmeisteri, B. sowerbyi, some naidids, and pristinids were
also build temporary, slimy hiding tubes, which they attach found in the tropical, persistently warm (19–31 °C) ponds in
to aquatic plants. Other naidids, e.g., Uncinais uncinata Mumbai, India. The presumably ubiquitous T. tubifex was
and Piguetiella blanci, prefer the surface of sand bottoms lacking there but was found in the nearby Ooty Hills, where
the winter air temperatures range between −4 and + 15 °C beds. Masses of tubificids inhabiting organic-rich but badly
(Naveed, 2012). In aquaria, T. tubifex has laid viable eggs aerated sediment will often hold themselves in a vertical
at + 25 °C and even at +30 °C; however, these eggs may be position, with anterior end (and mouth) in deeper sediment
parthenogenetic and not supporting a sustainable population. but the tail end held high over the bottom surface so they
Water current supports the life of oligochaetes primarily can simultaneously feed and respire.
because of its role in aeration. Many species characteristic of The phytophilous Naididae most often graze on vari-
flowing water can also inhabit surf littoral of large lakes per- ous epiphytic algae, bacteria, and protists, digesting selec-
sistently washed by waves. Flowing water is avoided mostly tively some algae (particularly diatoms) but egesting others.
by inhabitants of plant thickets but also by some open- Curiously, Ripistes parasita uses its extra-long hair chaetae
bottom species (e.g., the lumbriculid L. isoporus), possibly for food filtration, while U. uncinata ingests sand grains,
because of their vulnerability to drifting away in currents. digesting their biofilm.
Different aquatic oligochaete taxa are adapted to either A few oligochaetes have adapted to predatory feeding.
fresh, brackish, or saline (marine) water. A few eury- Chaetogaster spp. (Naididae) have developed a voluminous
haline species (Nais elinguis) can live both in freshwa- pharynx able to suck in various smaller animals or diatoms.
ter and in marine littoral. Some freshwater species (e.g., Phagodrilus and Agriodrilus (Lumbriculidae) feed mostly on
P. hammoniensis and Psammoryctides barbatus) occur also other oligochaetes by grabbing them with their very muscu-
in the brackish Baltic Sea at salinities up to 5–7 ppt. A salt tol- lar pharynx, much like some leeches. Haplotaxis gordioides
erance up to 10 ppt was established for the freshwater species (Haplotaxidae) is assumed to grip its prey oligochaetes with
L. hoffmeisteri and I. templetoni taken from a tidal water estu- its extended prostomium and peristomium and then constrict
ary (Chapman and Brinkhurst, 1980). In the Ponto-Caspian the prey boa-like with its very long body and sickle-shaped
basin, which has endured many salinity fluctuations during ventral chaetae. The internal parasites of excretory organs
its geological history, many endemic species have arisen, (C. limnaei waghini and Allodero spp.) feed on epithelium
thriving equally well in brackish water estuaries and fresh- cells of their hosts. The ectocommensal Astacopsidrilus
water bodies. An extreme example is the Caspian Sea (with spp. (Phreodrilidae) is probably a micropredator, cleansing
average salinity of 11 ppt), where three species of the other- microorganisms from the gill chamber of their crayfish hosts.
wise freshwater family of Lumbriculidae occur: the endemic
Trichodrilus pauper and Stylodrilus cernosvitovi, and the
Predators and Parasites
otherwise freshwater S. parvus. Several genera of the basi-
cally marine tubificid subfamily Phallodrilinae (as well as Oligochaetes serve as an easy and nutritious prey for preda-
of some other marine groups) include separate species in tory chironomid larvae, leeches, and other invertebrates.
freshwater, e.g., Thalassodrilus hallae in the Great Lakes The numerous stiff and sharp chaetae in some species like
of North America and many representatives of Aktedrilus Nais barbata or Vejdovskyella comata (Naididae) may pro-
and Abyssidrilus in the European underground waters. The vide some protection against predators. Oligochaetes are
inland saline lakes are usually devoid of oligochaetes, except certainly an important food object for benthophagous fishes,
for some single species of Enchytraeidae. Tissue desiccation but they are difficult to count or weigh in the contents of
after drying of the surrounding water body is lethal for the fish intestine because they are digested very rapidly, leaving
most aquatic oligochaetes. The ubiquitous L. variegatus and only chaetae. For this reason, the role of Oligochaeta in the
T. tubifex have been observed dormant in a slimy cyst in the diet of fishes is often underestimated. Fishes can feed on the
sediment of temporary pools. The ability of the hard-shelled mud-dwelling tubificids not only by devouring them com-
cocoons of Naididae to survive in an aerial environment has pletely but also by picking their waving tails stretched out
been discussed but never proved. Some Pristina species and of sediment. Fortunately for the worms, their tails are soon
the phreodrilid Schizodrilus have been described living in regenerated (Wiśniewski, 1978).
humid soils, and the tubificids Rhyacodrilus falciformis and Sessile ciliates often attach to the posterior ends of tubi-
Bothrioneurum grandisetosum are known to thrive even in ficids, using them as a substrate that is mostly exposed to
mesic soil. aerated water. Parasitic rotifers Drilophaga are known to
attach to the body surface of oligochaetes, while the rotifers
Albertia and Balatro can live either in the worm intestine or
Feeding Behavior
coelom. Various unicellular parasites (ciliates, gregarines,
Burrowing species ingest large amounts of fine sediment microsporidians, etc.), as well as nematodes and trema-
particles of suitable size, selectively digesting some organic todes, are known from the interior of oligochaetes.
components but defecating most of the ingested material. In the 1980s, the actinosporean internal parasites of
Tubificidae digest a species-specific selection of bacteria, Oligochaeta were identified as a regular stage in the life
whereas Enchytraeidae presumably prefer soil fungi but can cycle of Myxozoa, the economically important fish para-
thrive also on bacterial cultures or on the biofilm of sewage sites (Kent et al., 2001). Another group of fish parasites,
cestodes of the family Caryophyllaeidae, spend their larval chemical pollution, particularly by heavy metals. T. tubifex
(procercoid) stage mostly in the coelom of tubificids. Some is broadly used for the laboratory tests of water pollution
of them (Archigetes) can reach sexual maturity and repro- biology (Rodriguez and Reynoldson, 2011).
duce in oligochaetes too.
COLLECTING, CULTURING, AND

Other Ecological Aspects of Oligochaeta SPECIMEN PREPARATION
Competition between the tubificids and another abundant
group of freshwater mud dwellers, the chironomid larvae,
Collecting
would seem likely but has never been proved. On the con- Oligochaetes can be collected with any standard dip net,
trary, the years of maximum abundance of the Chirono- corer, or bottom grab used for sampling most zoobenthos.
mus plumosus in Lake Võrtsjärv (Estonia) also coincided A great deal of material is obtained in the course of rou-
with the greatest densities of the dominating tubificid tine ecological surveys. Washing the sediment often causes
P. hammoniensis. This oligochaete may thrive well when maiming of these soft worms. Elutriation of the sediment
fish feed primarily on this midge competitor. The ecologi- (particularly in the case of coarse sediments) and using
cally similar mud-dwelling tubificids and some others (e.g., rayon rather than metal sieves can mitigate this danger.
the lumbriculid S. heringianus) ingest large amounts of sedi- Sorting of sieve residue alive on an enameled dish, either
ment, selectively digesting some species-specific strains of in field or in laboratory, is preferable; however, without
bacteria but accelerating the growth of some others. In this magnification, some smaller individuals can be missed.
way, different species of oligochaetes can “feed” each other Unfortunately, postponing the sorting can cause selective
and thrive better in mixed populations. Indeed, mixed popu- mortalities of the species more sensitive to higher tempera-
lations of these worms are common in nature. It has been tures and lowered oxygen concentration. To save time in
demonstrated that T. tubifex and L. hoffmeisteri thrive better field, the sediment samples can be preserved as a whole
in mixed than in pure cultures. However, at least two ubiq- and later washed and sorted in laboratory. In this case the
uitous aquatic oligochaetes, the sediment-dwelling T. tubifex quantitative account of specimens can be more accurate,
and the phytophilous N. elinguis, are typically most abundant and even the smallest individuals will be found, particularly
in the extreme trophic conditions (N. elinguis also in brackish if the samples are sorted under a dissecting microscope.
water) where the other, related species are scarce or lacking. Small amounts of a stain like phloxine B or rose bengal
Their assumed sensitivity to competition is a possible expla- can be helpful for finding the small worms while sorting
nation of this. preserved samples. Such dyes should be avoided, however,
Significant ecological impacts of the phytophilous if oligochaetes are intended for molecular analyses, as they
Naididae grazing on periphyton communities are possible might affect the process of DNA sequencing. An easy pre-
but have never been quantitatively evaluated. Neither has servative for bulk samples is 10% buffered formalin (4%
potentially significant impact on diatoms and other protists formaldehyde solution), although a lower concentration
been demonstrated for the micropredatory Chaetogaster can also work. Higher concentrations make most animals
spp. The commensal of gastropods, C. limnaei limnaei, can brittle, while too low ones do not prevent rapid degrada-
render a service to its hosts as a cleaner, while their kidney tion of fragile worms. As formalin is an acidic solution, it
parasite C. limnaei vaghini is certainly pathogenic. may be useful to neutralize it by adding 20 g/l sodium bicar-
The burrowing activity of oligochaetes mixes and aer- bonate crystals (baking soda) or blackboard chalk. This is
ates the uppermost sediment layer and accelerates its oxida- vital for some other animal groups having calcified shells.
tion while simultaneously returning biogenic elements and Hence, it is advisable in the course of general surveys to use
contaminants accumulated in sediment back to the water a buffered 7–10% formalin solution as the “default” fixa-
layer. tive. One can carry 40% formalin in the field and then add
The widespread assertion that Oligochaeta as a group the appropriate amount to the aqueous sample to produce a
are indicators of heavy organic pollution is based on the concentration of 10% or less formalin. Preservation of bulk
ability of two ubiquitous tubificid species, L. hoffmeisteri samples with alcohol (ethyl or isopropyl) enables collectors
and T. tubifex, to develop en masse in α-mesosaprobic or to avoid inhaling toxic formalin vapor, but large amounts
even polysaprobic conditions. Many other tubificids and of 95% alcohol are required to reach a minimal concentra-
naidids thrive in either β-mesosaprobic or oligotrophic tion of 70% in a preserved sample, except if the sample
conditions. Their communities, rather than separate spe- is elutriated prior and its volume reduced to a minimum.
cies, can indicate the trophic conditions in a water body Seventy percent ethanol is the best medium for fixing live
(Milbrink, 1978; Uzunov et al., 1988). Organic enrichment oligochaetes or storing them when originally fixed in for-
per se is not dangerous for oligochaetes as long as there malin. Care should be taken to avoid diluting the alcohol at
is good oxygen supply. However, they may be sensitive to sorting; the volume of alcohol must exceed at least tenfold
the volume of the worms fixed. It is also a good idea to Aquatic oligochaetes can serve as a live food for fish
change the fluid in the vial before final storage of a sample. fry and aquarium fishes. Successful attempts at commer-
In a crammed vial, the oligochaetes will macerate into a cial production of T. tubifex on a mixture of cow dung and
worthless pulp. The same can happen when a vial is not well sand, under permanently flowing water, were described by
sealed and a part of the fluid has evaporated. The worms Marian et al. (1989). The tubificid worms sold in aquarium
provided for DNA sequencing must be fixed and preserved shops as “Tubifex” (in fact, mostly L. hoffmeisteri) are
in strong alcohol (80–96%) but never in formalin or alco- often not cultivated but collected in polluted open waters
hol “denatured” with additives that might interfere with (Naveed, 2012). L. variegatus, with a commercial name
DNA. After fixation, worms intended for molecular analy- “black worm,” may be the most suitable object for culti-
ses should be kept as soon as possible at low temperatures vating in aquaria since it can reproduce by fragmentation
(−20 °C). When available, a portable cool box should be for an unlimited time.
used to temporarily store alcohol-preserved samples in the
field. The strong alcohol makes worms somewhat stiff and,
Preparation for Identification
therefore, less easy for subsequent mounting. Freezing the
entire sediment sample in the field for later defrosting in the Immature Oligochaeta are often unidentifiable; when avail-
laboratory should be avoided because the dead worms will able alive, they can be cultivated in small aquaria with natu-
start decaying immediately when defrosted. The worms col- ral substrate at 4–12 °C until sexual maturation (Bülow,
lected for histological studies could be fixed in some special 1957). Of course, the maturation can take several months,
media recommended in respective guides. and the results are not always positive. Cultivated individu-
Special methods can be used for qualitative research in als may be more suitable for reference collections because
some cases. Naididae and Pristinidae can rapidly propa- they tend to lack injuries (missing tails and broken chaetae)
gate by paratomy in an aquarium with macrovegetation and common after sampling in nature.
then be found crawling on the glass walls. Tubificidae and A microscopic study of live individuals is recom-
others can be extracted from sediment rich in plant debris, mended if possible, as is common in the studies on Enchy-
using the wet funnel method common for the studies of traeidae. The living worms are relatively transparent so
Enchytraeidae. A sediment sample can then be placed on that most internal organs are visible, as are their intestine
a screen over a container with pure water; after some time, peristaltics, blood vessels’ pulsation, and work of cilia in
the worms will leave the sediment and fall to the bottom of nephridia. Mobility of the live worms can impede continu-
the container. ous investigation, photographing, or even measuring any
structures. A slight pressure applied to the worm under a
cover slip can be helpful, but excessive pressure must be
Rearing avoided, as this will cause the worm to burst, leaving only
Many tubificids, as well as the lumbriculid S. heringianus chaetae well exposed. Different methods of immobiliza-
and the “aquatic earthworm” C. lacuum, have been suc- tion can be used for small oligochaetes, e.g., putting them
cessfully cultivated for scientific purposes in lacus- under a cover slip in a drop of carbonated water. This will
trine mud sieved to avoid any incidental species. They bring the worm to a standstill due to suffocation, but the
do not need additional feeding or even water aeration if worm can survive for tens of minutes. Any fixative makes
they are held in a sufficient amount of mud under a thin the body wall opaque so that the internal organs become
layer of water. The addition of a moderate amount of hardly distinguishable. Fixed oligochaetes can be studied
easily decayed organic matter, like yeast, fish food pel- in temporary mounts under a cover slip in glycerin, which
lets, algal culture, etc., will accelerate the growth of the makes their bodies soft and half-transparent. Glycerin is
population. Some other species, e.g., L. variegatus, do very soluble in water and alcohol, and temporary mounts
not thrive without such additional feeding. Many species can be made that will persist for several years (but not
raised in aquaria need at least seasonally lower tempera- forever) as long as the cover slip edges are sealed. After
tures for their sexual reproduction. This is not essential for sealing, the slide can be possibly stored in a vertical posi-
Lumbriculus, Aulodrilus, and Bothrioneurum, which tion in microscope slide boxes. The use of nail varnish for
reproduce by fragmentation, nor is it necessary for the sealing the slides should be avoided, although its use is
facultative parthenogenetic T. tubifex. The last species regularly advised in the literature. The varnish becomes
has been cultivated for laboratory material in pure sand fissured with time; being permeable to ambient air, the
enriched with yeast or lettuce. Rearing the phytophilous slide finally dries and the worm is lost. Some have been
Naididae and Pristinidae is more complicated because using synthetic media (e.g., DPX mounting medium) and
their paratomic clones, although reproducing rapidly, tend also Canada balsam for sealing purposes.
to fade over time. Bacterial film from hay or lettuce infu- Type and reference specimens should be maintained
sion can serve as a suitable food for them. in permanent whole mounts, e.g., in Canada balsam. For
this purpose, the worms can first be transferred from glyc- of a microscalpel, such as the ones used in ophthalmology
erin into dilute alcohol, then dehydrated through a series (iris knife-type) (Figure 21.9). The gut is then removed
of baths of increasing alcohol content (70%, 96%, 100%; in the sexual region of the body, taking care of genital
50:50 alcohol-xylene), shifted to xylene, put into a drop of organs adhering to the gut. Both dissected parts are then
Canada balsam, and finally placed under a cover slip. After stained, dehydrated, and mounted in Canada balsam. The
some days of desiccation of the slip edges, this mount is taxonomically valuable material is securely maintained
ready and can survive 100 years, if not more. when histological sections are made from the segments
The xylene makes worms and their chaetae hard and of interest, and internal organs are reconstructed after the
brittle, but this will be no problem with specimens flat- sections. This time-consuming procedure is not described
tened under a cover slip in glycerin. The larger oligo- here. A routine identification can always proceed using
chaetes (and also leeches) can be fixed, for this purpose, either live or whole-mounted oligochaetes. Taxonomically
at the same time by pressing them flat between two slides. puzzling specimens, if present, could be sent to an expert
Internal organs are better visible in the Canada balsam for a consultation.
than in glycerin, particularly if the complete worms were When beginning identification of an oligochaete, it is
slightly stained before mounting. The specimens can necessary to first establish the anterior end; it is usually
be stained (e.g., with Mayer’s paracarmin or Ehrlich’s thicker, bears the mouth and prostomium, and has more
hematoxylin, always followed by cautious differentia- numerous and longer chaetae on several segments. The ori-
tion) before dehydration. An opposite problem can appear entation of chaetae also provides a good clue: as a rule, their
when chaetae become even too translucent in the balsam ectal tip is directed backwards. The tail is usually thinner
because their refractive index is more similar to balsam and longer, and it lacks many taxonomic characters (if not
(and xylene) than it is to glycerin or water. Use of dif- bearing gills). The next step is to distinguish the dorsal and
ferential interference contrast microscopy (DIC) seems to ventral side. Hair chaetae, when present, occur only dorsally
mitigate this problem. in all common taxa. The prostomium also lies dorsally of the
There exist several other clearing media for temporary mouth; it can be extended into unpaired proboscis, or bear
investigation, as well as synthetic resins for making per- a pair of simple eyespots. In contrast, genital pores, if pres-
manent mounts (e.g., Euparal, broadly used in entomol- ent, are almost always ventral. Next, the segments should
ogy); however, the persistence of the latter over decades be counted (bearing in mind that usually the chaetae begin
is not yet proved. Many researchers have used for pre- mostly in II but never in the I segment); the total segment
liminary studies the compound Amman’s lactophenol, number is not as important as the presence (or lack) and
as first employed by Brinkhurst (1960). It consists of position of the elements of the reproductive system (clitel-
glycerin, water, phenol, and lactic acid. Brinkhurst also lum, genital pores, internal reproductive organs sometimes
recommended polyvinyl lactophenol (Jones, 1946) for bulging from the body, and modified ventral chaetae). The
making semi-permanent whole mounts of aquatic Oligo- latter is most probably located in the region of the segments
chaeta. The polymerization of vinyl makes the mounting X–XIII. The male pores are often prominent as tubercles in
medium semi-rigid, in which the worm cannot be dis- the anterior portion of the clitellum, while the spermathe-
placed anymore. Phenol-based media are good for routine cal pores lie often (but not always) ahead of the clitellum.
identification since they make chaetae and other chitinous The female pores are usually inconspicuous. The sperm and
structures very distinct. Unfortunately, they are unsuitable egg sacs can reach for several segments rearward and will
for reference material, since all soft internal organs will be obvious as massive (in live worms, milky-white) bod-
merge in a continuous mass under a cover slip, and even ies above the intestine. The body wall is externally smooth
chaetae may swell after some years. in most oligochaetes but can be armored with cutaneous
A closer description of internal reproductive organs, papillae and/or adhered particles in some species. The tail
particularly the male ducts, is necessary for a detailed portion is usually devoid of specific characters, except the
taxonomic study. Unfortunately, these structures are often forms with external gills.
overshadowed by amorphous masses of sperm and pros- Now the characteristics of the chaetae should be noted.
tate glands in the whole mounts. For this purpose, the Are they of one sort or different (bifid, simple-pointed,
genital segments can be dissected, a part of the body wall and hair chaetae)? How many chaetae are in each bundle:
removed, and the male ducts and spermathecae extracted two, one, or in variable numbers? The chaetal number and
under a dissecting microscope, using sharp razor blades diversity are usually largest in the most anterior (precli-
and very fine needles. That is a difficult task because these tellar) segments while decreasing in the tail portion. The
organs are soft and can be easily lost. Moreover, it is even absolute length of chaetae is usually less important than
more difficult to mount dissected small objects. An excel- their relative lengths (and sometimes also their thickness)
lent alternative consists of cutting the anterior part of the in separate body regions. Variations of shape must be
worm into two halves, along the sagittal plane, by means observed in the hair (smooth, pilose, serrated?) as well
D E
F G
H I
J K
FIGURE 21.9 Dissection of a tubificid worm: (a) and (b) separation of anterior part of the worm containing genital segments; (c)–(e) with the worm
lying on its back, cutting along the sagittal plane; (f) separation of left and right halves; (g) and (h) removal of the gut in the area of genital organs. From
Martin and Aït Boughrous (2012).
as in the dorsal bifid chaetae (pectinate with intermedi- Some individuals, or at least their tail portions, could also
ate teeth, palmate?). In the ventral (and also dorsal) bifid be fixed in strong alcohol for possible DNA sequencing.
chaetae, the relative length of the upper and lower tooth
is important, as are position of the nodulus (proximal,
medium, or distal) and the thickness of chaetae; all these REFERENCES
characters can successively change along the body length. Adoutte, A., Balavoine, G., Lartillot, N., Lespinet, O., Prud’homme, B.,
The segments bearing male and/or spermathecal pores de Rosa, R., 2000. The new animal phylogeny: reliability and implica-
can lack ventral chaetae, or those can be replaced with tions. Proc. Natl. Acad. Sci. U.S.A. 97, 4453–4456.
modified genital chaetae (penial or spermathecal, respec- Brinkhurst, R.O., 1960. Introductory studies on the British Tubificidae
tively) in the sexually mature, maturing, or postrepro- (Oligochaeta). Arch. für Hydrobiol. 56, 395–412.
ductive individuals, even in those devoid of a clitellum. Brinkhurst, R.O., 1984. The position of the Haplotaxidae in the evolution
The bundles of penial chaetae, as well as chitinous penial of oligochaete annelids. Hydrobiologia 115, 25–36.
sheaths present in many taxa, are often hidden inside the Brinkhurst, R.O., 1994. Evolutionary relationships within the Clitellata: an
update. Megadrilogica 5, 109–112.
body and visible only in the living individuals or cleared
Brinkhurst, R.O., Jamieson, B.G.M., 1971. Aquatic Oligochaeta of the
whole mounts.
World. Oliver & Boyd, Edinburgh. 860 pp.
The digestive tract is the most apparent internal organ, Bülow, T. von, 1957. Systematisch-autökologische Studien an eulitoralen Oli-
traceable even in whole mounts and in immature speci- gochaeten der Kimbrischen Halbinsel. Kiel. Meeresforsch. 13, 69–116.
mens. The pharynx roof (pharyngeal pad) in II–III is more Caramelo, C., Martínez-Ansemil, E., 2012. Morphological investigations
or less thickened, covered with gland tissue, and fastened of microdile oligochaetes (Annelida, Clitellata) using scanning elec-
to the dorsal body wall with numerous muscles. A rela- tron microscopy. Turkish J. Zoology 36, 1–14.
tively thin esophagus follows through several subsequent Chapman, P.M., Brinkhurst, R.O., 1980. Salinity tolerance in some selected
segments, dilating into midgut (intestine) usually in some aquatic oligochaetes. Int. Rev. gesamten Hydrobiol. 65, 499–505.
of the anteclitellar segments. Different glands, append- Creuzé des Châtelliers, M., Juget, J., Lafont, M., Martin, P., 2009. Subter-
ages, and modified parts can occur at the pharynx, esopha- ranean aquatic Oligochaeta. Freshwater Biol. 54, 678–690.
gus, and anterior portion of the midgut, particularly in the Cuadrado, S., Martínez-Ansemil, E., 2001. External structures used during
attachment and sperm transfer in tubificids (Annelida, Oligochaeta).
Enchytraeidae. Dark chloragogen tissue covers the diges-
Hydrobiologia 436, 107–113.
tive tract, usually beginning with a certain esophageal
Erséus, C., 2005. Phylogeny of oligochaetous Clitellata. Hydrobiologia
segment. The dorsal and ventral blood vessels are usually 535/536, 357–372.
well distinguishable in whole mounts but usually of infe- Erséus, C., Källersjö, M., Ekman, M., Hovmöller, R., 2002. 18S rDNA
rior value for identification. The number and modifica- phylogeny of the Tubificidae (Clitellata) and its constituent taxa:
tions of commissural vessels in some segments (as dilated dismissal of the Naididae. Mol. Phylogenet. Evol. 22, 414–422.
“hearts,” or blind appendages, sometimes covered with Erséus, C., Wetzel, M.J., Gustavsson, L., 2008. ICZN rules – a farewell to
chloragogen tissue) can be more important. Nephridia Tubificidae (Annelida, Clitellata). Zootaxa 1744, 66–68.
are visible only in living or well-cleared specimens; their Erséus, C., Rota, E., Matamoros, L., DeWit, P., 2010. Molecular phylog-
structure and presence/absence in the anterior segments eny of Enchytraeidae (Annelida, Clitellata). Mol. Phylogenet. Evol.
57, 849–858.
is important, especially in Enchytraeidae. Spermathecae
Holmquist, C., 1978. Revision of the genus Peloscolex (Oligochaeta, Tubi-
are one of the most distinct elements of the reproductive
ficidae). Zool. Scr. 7, 187–208.
system in whole mounts since they are usually not hidden Hrabě, S., 1981. The freshwater Oligochaeta (Annelida) of Czechoslovakia.
by the clitellum. Their structure and segmental location, Acta Univ. Carol. Biol. 9, 1–166 (In Czech, with English Summary).
position of their pores on a segment (ventral, lateral, etc.), Jamieson, B.G.M., Erséus, C., Ferraguti, M., 1987. Parsimony analysis of
and arrangement of sperm in the spermathecae (amor- the phylogeny of some Oligochaeta (Annelida) using spermatozoal
phous, in bundles, or organized into spermatozeugmata) ultrastructure. Cladistics 3, 145–155.
are important. Testes, ovaries, sperm sac, and egg sac do Jamieson, B.G.M., Ferraguti, M., 2006. Non-leech Clitellata. In: Rouse,
not provide many identification characters. Separate ele- G., Pleijel, F. (Eds.), Reproductive Biology and Phylogeny of Annel-
ments of the male ducts (funnels, vasa deferentia, atria, ida. Science Publishers, Enfield, pp. 235–392.
prostatic glands, penial apparatus) are most important for Jones, B., 1946. Impregnating polyvinyl alcohol with picric acid for the
the oligochaete taxonomy but are often hardly distinguish- simultaneous staining and permanent mounting of Acarina. Proc. R.
Entomol. Soc. London Ser. A Gen. Entomol. 21, 85–86.
able in whole mounts. Different special methods like DIC
Jördens, J., Struck, T., Purschke, G., 2004. Phylogenetic inference regarding
microscopy are helpful here, as is dissection or sectioning
Paregodrilidae and Hrabeiella periglandulata (Polychaeta, Annelida)
of the gonadal segments. based on 18 rDNA and COI sequences. J. Zool. Syst. Evol. Res. 42,
It would be reasonable to maintain in alcohol any 270–280.
unidentifiable (potentially new for the region or science), Kathman, R.D., Brinkhurst, R.O., 1998. Guide to the Freshwater Oligo-
sexually mature oligochaetes discovered in routine hydrobi- chaetes of North America. Aquatic Resources Center, Thompsons Sta-
ological surveys for further study by an expert taxonomist. tion, Tennessee.
Kent, M.L., Andrée, K.B., Bartholomew, J.L., El-Matbouli, M., Desser, Naveed, M.I., 2012. Preliminary studies on aquatic Oligochaeta in and
S.S., Devlin, R.H., Feist, S.W., Hedrick, R.P., Hoffmann, R.W., around Chennai, Tamil Nadu, India. Turkish J. Zool. 36, 25–37.
Khattra, J., Hallett, S.L., Lester, R.J.G., Longshaw, M., Palenzeula, O., Purschke, G., 2003. Is Hrabeiella periglandulata (Annelida, “Polychaeta”)
Siddall, M.E., Xiao, C.X., 2001. Recent advances in our knowledge of the sister group of Clitellata? Evidence from an ultrastructural analysis
the Myxozoa. J. Eukaryot. Microbiol. 48, 315–413. of the dorsal pharynx in H. periglandulata and Enchytraeus minutus
Marian, M.P., Chandran, S., Pandian, T.J., 1989. A rack culture system for (Annelida, Clitellata). Zoomorphology 122, 55–66.
Tubifex tubifex. Aquac. Eng. 8, 329–337. Rodriguez, P., Reynoldson, T.B., 2011. Pollution Biology of Aquatic
Martin, P., 1996. Oligochaeta and Aphanoneura in ancient lakes: a review. Oligochaetes. Springer, Dordrecht, Heidelberg, London, New York.
Hydrobiologia 334, 63–72. 263 pp.
Martin, P., 2001. On the origin of the Hirudinea and the demise of the Oli- Rousset, V., Pleijel, F., Rouse, G.W., Erséus, C., Siddall, M.E., 2007.
gochaeta. Proc. Roy. Soc. London Ser. B 268, 1089–1098. A molecular phylogeny of annelids. Cladistics 23, 41–63.
Martin, P., Aït Boughrous, A., 2012. Guide taxonomique des oligochètes aqua- Semernoy, V.P., 2004. Oligochaeta of Lake Baikal. Nauka, Novosibirsk (In
tiques du Maghreb. Belgian national focal point to the global taxonomy Russian, with English translation of descriptions of the new species).
initiative. Royal Belgian Institute of Natural Sciences, Brussels. 186 pp. 527 pp.
Martin, P., Granina, L., Martens, K., Goddeeris, B., 1998. Oxygen con- Siddall, M.E., Apakupakul, K., Burreson, E.M., Coates, K.A., Erséus, C.,
centration profiles in sediments of two ancient lakes: Lake Baikal Gelder, S.R., Källersjö, M., Trapido-Rosenthal, H., 2001. Validating
(Siberia, Russia) and Lake Malawi (East Africa). Hydrobiologia 367, Livanow: molecular data agree that leeches, branchiobdellans, and
163–174. Acanthobdella peledina form a monophyletic group of oligochaetes.
Martin, P., Martens, K., Goddeeris, B., 1999. Oligochaeta from the abyssal Mol. Phylogenet. Evol. 21, 346–351.
zone of Lake Baikal (Siberia, Russia). Hydrobiologia 406, 165–174. Struck, T.H., Paul, C., Hill, N., Hartmann, S., Hösel, C., Kube, M.,
Martin, P., Martínez-Ansemil, E., Pinder, A., Timm, T., Wetzel, M.J., 2008. Lieb, B., Meyer, A., Tiedemann, R., Purschke, G., Bleidorn, C.,
Global diversity of oligochaetous clitellates (“Oligochaeta”; Clitel- 2011. Phylogenomic analyses unravel annelid evolution. Nature
lata) in freshwater. Hydrobiologia 595, 117–127. 471, 95–98.
Martínez-Ansemil, E., Creuzé des Châtelliers, M., Martin, P., Sambugar, Struck, T.H., 2011. Direction of evolution within Annelida and the defini-
B., 2012. The Parvidrilidae – a diversified groundwater family: tion of Pleistoannelida. J. Zool. Syst. Evol. Res. 49, 340–345.
description of six new species from southern Europe, and clues for Timm, T., 1981. On the origin and evolution of aquatic Oligochaeta. Eesti
its phylogenetic position within Clitellata (Annelida). Zool. J. Linn. NSV Teaduste Akadeemia Toimetised, Bioloogia 30, 174–181.
Soc. 166, 530–558. Timm, T., 1987. Aquatic Oligochaeta of the Northwestern Part of the
Michaelsen, W., 1902. Die Oligochaeten-Fauna des Baikal-Sees. Verhand- USSR. Valgus, Tallinn (In Russian, with English Summary). 299 pp.
lungen des. Naturwiss. Vereins Hamburg 9, 43–60. Timm, T., 2012. About the scientific names of paraphyletic taxa. Turkish
Michaelsen, W., 1929. Zur Stammesgeschichte der Oligochäten. Z. für J. Zool. 36, 139–140.
Wiss. Zool. 134, 693–710. Uzunov, J., Košel, V., Sládeček, V., 1988. Indicator value of freshwater
Milbrink, G., 1978. Indicator communities of oligochaetes in Scandina- Oligochaeta. Acta Hydrochim. Hydrobiol. 16, 173–186.
vian lakes. Verhandlungen Int. Ver. für Limnol. 20, 2406–2411. Wesenberg-Lund, C., 1939. Biologie der Süswassertiere. Julius Springer,
Milbrink, G., Timm, T., 2001. Distribution and dispersal capacity of the Ponto- Wien. 817 pp.
Caspian tubificid oligochaete Potamothrix moldaviensis Vejdovský et Wiśniewski, R.J., 1978. Effect of predators on Tubificidae groupings and
Mrázek, 1903 in the Baltic Sea Region. Hydrobiologia 463, 93–102. their production in lakes. Ekol. Pol. 26, 493–512.

timm2015

Uploaded by

Document Informationclick to expand document information

Copyright:

Available Formats

timm2015

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

timm2015

Uploaded by

Copyright:

Available Formats

Chapter 21

INTRODUCTION sediments. Classifying the families into orders is difficult

The second basic type of chaetae in many aquatic Oli-

The penial chaetae (as well as unmodified ventral chaetae)

COLLECTING, CULTURING, AND

You might also like