Adaptations of Anomopoda Crustaceans (Cladocera) to the benthic mode of life

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ISSN 0013-8738, Entomological Review, 2006, Vol. 86, Suppl. 2, pp. S210–S225. © Pleiades Publishing, Inc., 2006.Original Russian Text © A.A. Kotov, 2006, published in Zoologicheskii Zhurnal, 2006, Vol. 85, no. 9.

INTRODUCTION

Many publications are devoted to adaptations to theplanktonic mode of life in cladocerans (Woltereck,1919; Dumont and Negrea, 2002; etc.), but planktonicforms account for less than half of all cladoceran spe-cies. Littoral cladocerans became subject to intensefunctional-morphological studies at the end of the 20thcentury (Fryer, 1968, 1974; Sergeev, 1972). However,since a series of studies by Smirnov (1969, 1971a,1971b, 1971c, 1999a, 1999b), comparative analysis ofadaptations in representatives of different families havenot received sufficient attention.

Dozens of cladoceran species are often found in asingle sample taken from the bottom of a water body incentral Russia. Yet the bottom is not a typical habitat formost of them. These species occasionally drift above orcrawl on the bottom but remain most of the time amidmacrophytes or in the littoral plankton. For instance,

Daphnia magna

Straus 1820, a most typical planktonicspecies, in cases of food shortage stirs up bottom sedi-ments and filters out food from the bottom of the water-body. Some “heavy” chydorids with thick integumentsare permanently present in the littoral plankton (Rybaket al., 1964). Many authors, including the author of thispaper, collected large numbers of

Chydorus sphaericus

(O.F. Müller 1785) from the bottom; this species iseurytopic, it commonly occurs amid macrophytes andin the littoral plankton; periodically, it enters thepelagic plankton and sometimes even dominates in it(Fryer, 1968). Therefore, the group of benthic cladocer-ans is distinguished conditionally, the more so that bio-logical features of many boreal and tropical species arepoorly known.

A special ecological group of cladocerans com-prises true benthic forms, i.e., the animals that digthemselves into the silt or live directly on the surface ofbottom sediments and can move within the silt layer.They occur among representatives of the two species-richest cladoceran orders, Ctenopoda and Anomopoda.Among ctenopods, bottom dwellers are represented byspecies of the genera

Latona, Latonopsis

, and

Sarsila-tona.

The ability of

Latona

species to dig themselvesdeep into the silt was demonstrated directly(Korovchinsky, 2004).

Anomopods comprise more than half of all cladoce-ran species (about 530 out of 600) (Korovchinsky,1996). Describing this group, we follow the modernclassification (Dumont and Silva-Briano, 2000). Fewanomopod genera and species are truly benthic; thismode of life is especially typical of some members ofthe subfamily Aloninae, family Chydoridae:

Monospi-lus

,

Leydigia, Leydigiopsis, Spinalona, Parvalona,Pseudomonospilus, Australospilus, Kozhowia, Para-kozhowia,

and some species of the large genus

Alona

Baird 1843:

A. quadrangularis

(O.F. Müller 1776),

A.affinis

Leydig 1860, and some other species (Fryer,1968; Vasil’eva and Smirnov, 1969; Smirnov, 1971b;Sars, 1993; Griggs, 2001). Among Holarctic species ofthe subfamily Chydorinae, the following forms usuallyoccur on the bottom:

Peracantha truncata

(O.F. Müller1785),

Pleuroxus uncinatus

(Baird 1850),

P. trigonellus

(O.F. Müller 1776),

Paralona pigra

(Sars 1862), and anumber of species from the genera

Disparalona

Fryer1968,

Chydorus

Leach 1816, and

Alonella

Sars 1862.However, chydorines usually crawl on the surface ofsilt and do not dig themselves into it (Fryer, 1974;Smirnov, 1975).

Adaptations of Anomopoda Crustaceans (Cladocera) to the Benthic Mode of Life

A. A. Kotov

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071 Russiae-mail: [email protected]

Received April 14, 2005

Abstract

—Crustaceans of the order Anomopoda inhabit both pelagic and littoral zones of fresh water bodies.Different adaptations to the benthic mode of life in representatives of different families and genera of this orderare described. They include incomplete molting, the presence of a mucous film on the body surface, protectionof the head from frontal damage, large lateral projections on the valves and additional sculpture on the head andvalves, well-developed lateral armature of the postabdomen, the presence of projections on the postabdomenpreanal margin, specialization of setae and spines of the second antenna, especially large exopodites on limbsIV and V, a reduced compound eye, and a large, well-developed ocellus. Similar adaptations to the benthic modeof life in the Anomopoda and Ostracoda are discussed.

DOI:

10.1134/S0013873806110157

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Among

Macrothricidae

, the ability to dig deeplyinto bottom sediments (down to 4 cm, which is six toseven times the length of an adult animal) is character-istic of

Macrothrix laticornis

Jurine 1820 (Chirkova,1984).

Macrothrix

species are numerous and have var-ious modes of life. There are probably other diggingspecies in the genus. Sars (1888) noted that the tropical

M. spinosa

King 1853 spent most of its time at the bot-tom, although did not dig in. Among other

Marcotri-cidae

, living among detritus on the bottom surface istypical of

Streblocerus serricaudatus

(Fischer 1849),

S. pygmaeus

Sars 1901,

Lathonura rectirostris

(O.F.Müller 1785), and

Grimaldina brazzai

Richard 1892.We have observed digging into the silt in

Drepanothrixdentata

(Eurén 1861) collected at the Lake GlubokoeBiological Station of the Institute of Ecology and Evo-lution, Moscow oblast; this confirms the observationsof Sars (1901) and Fryer (1974). Species of the genus

Neothrix

Gurney 1927 (Neothricidae) also spend muchof their time in bottom sediments (Fryer, 1974).

Ophry-oxus

and

Parophyoxus

(Ophryoxidae) cladocerans arelittoral dwellers occurring both in vegetation-free bot-tom areas and amid macrophytes.

The most specialized truly benthic genus of anomo-pods is

Ilyocryptus

Sars 1862, the only genus in thefamily

Ilyocryptidae.

Some species of this genus arecapable of digging as deeply as 15 cm (Chirkova,1984), which exceeds their body length by a factor ofmore than 100. Most ilyocryptids have entirely lost theability to swim and never leave the bottom. Some spe-cies of the genus are relatively mobile and retain theability to swim throughout their life span (

I. agilis

and

I. spinifer

), but even these sometimes dig into the sur-face silt layer (Chirkova, 1984; this author’s observa-tions).

The morphology of many bottom-dwelling anomo-pods, especially

Ilyocryptus

and

Leydigia

, was poorlyknown until recently. This author’s studies on thesespecies (Kotov and Dumont, 2000; Kotov, 2003; Kotovand

⁄

tifter, 2006) and some other species of alonines(Kotov, 2000; Kotov and Elías

-

Gutiérrez

, 2002

) haveshown that many morphological structures in phyloge-netically distant bottom-dwelling cladocerans are con-vergently similar. The purpose of this work is to sum-marize the data on the morphology of benthic cladocer-ans from different families and to reveal the generaltrends in evolutionary changes adaptive to the benthicmode of life. Information on animals living on the sur-face of the bottom and incapable of digging in was alsoconsidered for comparison with digging bottom-dwell-ers.

MATERIAL AND METHODS

Both information from earlier publications and newdata, the results of scanning electron microscopy, wereused in this study. Information on the localities whereeach species was collected is given in the table. Thespecimens were freeze-dried, repeatedly washed in dis-

tilled water, mounted on brass plates, coated with gold,and examined under JEOL-840A and CAMSCANscanning electron microscopes.

RESULTS

Anomopod Adaptations Relatedto the Benthic Mode of Life

Incomplete molting.

In many

Ilyocryptus

species,the old integument in molting parthenogenetic femalesis shed only from the ventral area of the head, the innersurface of the valve, the abdomen, the limbs, and thepostabdomen, whereas the head shield and the outersurface of the valves remain attached to the new integ-ument. Old head shields and valves accumulate uponone another as concentric plates (Figs. 1a–1c). Thistype of molting is termed incomplete (Chirkova, 1984;Alonso, 1996; Kotov and

⁄

tifter, 2006). When the ani-mal switches to gamogenetic development, all the oldhead shields and valves are shed during a single molt,so that gamogenetic females have one-layer integu-ment. Most

Ilyocryptus

species are characterized byincomplete molting, although some of them show ple-siomorphic complete molting (Fig. 1d). It was recentlyshown that incomplete molting developed indepen-dently in different species groups of this genus (Kotovand Dumont, 2000). In the chydorid

Monospilus

(sub-family Aloninae), old valves are also often retained dur-ing the molting, yet old head shields are shed (Figs. 1e–1f).

The preservation of old layers of the integument onnew layers is doubtlessly a way to harden the latter.Dwelling in bottom sediments implies permanent pres-sure of this viscous medium on the valves, which theanimal has to withstand. The valves and the head canalso be damaged with large mineral particles and frag-ments of organic origin.

In addition to species with obligatory incompletemolting, occasional retention of the valves of earlierinstars was observed in some other benthic alonines:

Acroperus elongatus, A. americanus, Rhynchotalonafalcata, Kozhowia kozhowi, Alona rustica, Oxyurellatenuicaudis

(Smirnov, 1971b; Frey, 1982a; Kotov,2000),

O. longicaudis

(Birge 1910) (Figs. 1g–1h, 2a,2b). At the same time, incomplete hatching was neverobserved in members of the other chydorid subfamily,Chydorinae.

Mucous film on the body surface.

In the few benthicanomopods (

Ophryoxus, Parophryoxus, Ilyocryptus

),the surface of the body is covered with a protectivemucous film secreted by special glands (Fryer, 1974).The film is also present on the body of the benthic cte-nopod

Latona

(Korovchinsky, 2004). The glands thatsecrete the mucous substance are poorly known, andthe same concerns the presence of the film on the bodyof anomopods: it is probably characteristic of othergenera as well.

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Species studied and localities where they were collected

Taxon Country Locality Collector Date

Ilyocryptidae

Ilyocryptus cuneatus

Russia Lake Glubokoe, Ruzskii raion,Moscow oblast

A.A. Kotov August 14, 1997

I

.

isanensis

Thailand A pond in Ban Non Muang sub-districs, Khon Kaen Province

L. Sanoamuang June 7, 1998

I

.

paranaensisinarmatus

Mexico Pulsar pond, basin of the Usuma-cinta River, Tabasco

M. Gutiérrez-Aguirre et al.

January 31, 1999

I

.

spinifer

(fig. 1) Mali Mares au bord du Niger, Bamako Th. Monod February 17, 1976

I

.

spinifer

(fig. 3) Brunei Bander smal puddle, Edinburgpalace road

H.J. Dumont October 24, 1994

I

.

uenoi

Japan A small swamp at Yoichi Town, Hokkaido Island

T. Ishida January 5, 2000

Macrothricidae

Drepanothrix dentata

Russia Lake Glubokoe, Ruzskii raion,Moscow oblast

A.A. Kotov May 20, 2004

Macrothrix laticornis

Russia Bezymyannaya River, EngelsRailway Station, Saratov oblast

A.V. Makrushin August, 1980

Lathonura rectirostris

Russia A pond near Lake Glubokoe, Ruzskii raion, Moscow oblast

A.A. Kotov June 23, 1996

Neothricidae

Neothrix armata

Australia Teddington Reserv. via St. Arnaud,Victoria

B.V. Timms December 9, 1973

Chydoridae

Chydorinae

Chydorus invaginatus

Thailand A tributary of Mekong River, Mukdahan Province

L. Sanoamuang January 31, 1998

C

.

obscurirostristasekberae

Thailand A tributary of Mekong River, Mukdahan Province

L. Sanoamuang January 31, 1998

Disparalona rostrata

Russia Bezymyannaya River, EngelsRailway Station, Saratov oblast

A.V. Makrushin August, 1980

D

.

acutirostris

Canada Pond at Bay Bulls, Avalon Penin-sula, Newfoundland

C.C. Davis July 11, 1971

Peracantha truncata

Russia Lake Glubokoe, Ruzskii raion,Moscow oblast

A.A. Kotov August 30, 1995

Pleuroxus trigonellus

Russia Lake Svyatoe, Kosino, Moscow A.A. Kotov August 23, 1998

Aloninae

Acroperus elongatus

Russia Uglich Reservoir, Yaroslavloblast

N.N. Smirnov July 23, 1962

Monosplilus dispar

Russia Lake Glubokoe, Ruzskii raion,Moscow oblast

A.A. Kotov September 26, 1999

Leydigia ciliata

Kenya Loriye fish pond, near Lake Olbo-losat

D. Veschuren August 5, 2001

L

.

propinqua

South Africa Knysna

Leydigiopsis curvirostris

Brazil Lagoa da Colher, Maranhao K. Van Damme August 17, 1996

Oxyurella longicaudis

Mexico Pond Km. 51 Villahermosa-Fron-tera, Tabasco

M. Elías-Gutiérrez January 13, 1998

Oxyurella tenuicaudis

Uzbekistan Southeast of Dzhingil’-Kuduk desert station, Kyzyl-Kum

Unknown October 4, 1962

Rhynchotalona falcata

Russia Lake Glubokoe, Ruzskii raion,Moscow oblast

A.A. Kotov September 26, 1999

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The mucous film is also present on the body surfaceof some nonbenthic cladocerans; it always plays a pro-tective role. For instance, a mucous film covers the

body of the chydorid

Anchistropus emarginatus

Sars1862, an ectoparasite of hydras (Fryer, 1968), protect-ing the cladoceran from the hydra’s nematocysts. A

a e

b f

c g

d h

Fig. 1.

Benthic anomopods: (a–c)

Ilyocryptus spinifer

with incomplete molting (lateral view, dorsal view, and head in lateral view,respectively); (d)

I. uenoi

with complete molting; (e, f)

Monospilus dispar

, lateral view and frontal view; (g, h)

Acroperus elongatus

,lateral view and posteroventral part of valve. Scale bars: (a–g) 100

µ

m; (h) 10

µ

m.

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thick gelatinous film covers the body of the planktonicctenopod

Holopedium.Head protection from frontal damage. Several

benthic chydorid species have a long rostrum, which is

sometimes curved backward or, more rarely, directedforward. It is especially long in the alonines Rhynchota-lona (Fig. 2b) and Leydigiopsis (Figs. 2c, 2d), whichare capable of digging into the substrate (Sars, 1901,

a e

b f

c g

d h

Fig. 2. Benthic anomopods: (a) Oxyurella longicaudis; (b) Rhynchotalona falcata; (c, d) Leydigiopsis curvirostris, lateal view andlabrum; (e, f) Disparalona rostrata, lateal view and head; (g, h) D. acutirostris, lateral view and head. Scale bars: (a–c, e, g) 100 µm;(d, f, h) 10 µm.

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1993), and in the chydorine Rhynchochydorus aus-traliensis Smirnov & Timms 1983 (Smirnov, 1999b),whose biology is poorly known. The size of the rostrumvaries considerably among the species of the genusDisparalona (Figs. 2e–2h). The rostrum obviously pro-tects the head frontally (in the case of rostrum curvedbackward, also ventrally) from contact with large parti-cles. Vitally important and tender parts of the head ven-tral surface (antennules, esthetascs on them, and theposterior surface of the labrum; see Fig. 2d) are thusprotected from damage. Members of the generaPleuroxus, Chydorus, and Pseudochydorus that do notdig into bottom sediments sometimes also have a well-developed rostrum, which is, however, smaller than inthe genera listed above. In addition to the rostrum, theanterior margins of the valves take part in protecting thehead frontally in animals with a rounded body; thevalves in some chydorines have special flanges(Smirnov, 1971c).

In the macrothricids Streblocerus, Drepanothrix,and Macrothrix laticornis, as well as in neothricids, thehead is longitudinally elongated and flattened from thesides, with a long rostrum (Figs. 3a–3f) that operates asan icebreaker, pushing aside solid particles when theanimal moves on the substrate and, possibly, within it.Streblocerus also has a longitudinal medial keel on thehead (Fryer, 1968). All the macrothricids have robustantennules, which are less prone to damage than muchsmaller antennules of chydorids.

The head of Ilyocryptus is flattened not from the sidesbut dorsoventrally. In the species with incomplete molt-ing, the head is protected dorsally with the head shieldsof earlier instars, and the margin of each head shield isadditionally thickened and chitinized (Figs. 3g–3h). Theanterior margin of the head in Ilyocryptus is similar tothe chydorid rostrum.

Additional sculpture of the head and the valves. Ingeneral, the integument of littoral anomopods is thickerand harder than that of planktonic anomopods (Dahm,1977). The sculpture of the integument also differs(Smirnov, 1971c), being sometimes even clearly differ-ent in two closely related species, such as Disparalonarostrata (Koch 1841) and D. acutirostris (Birge 1879)(Figs. 2e–2h, 4a–4d). Cellular sculpture is typical ofsome benthic anomopod species from different fami-lies. Such sculpture is especially complicated in the rel-atively numerous species of the genus Chydorus, whichhave valves with cellular or even honeycomb-likesculpture (Frey, 1982a, 1982b) (Figs. 4e–4h). The func-tion of this protruding sculpture is not fully clear. Frey(1982a) suggested that the “honeycomb cells” protectChydorus from predators, yet no attempts have beenmade to test this hypothesis. In planktonic anomopods,hard chitinized protrusions actually protect them fromthe attacks of small predators (Dumont and Negrea,2002). Daphnia lumholzi Sars 1885 is a special case,with its needle-like helmet and posterodorsal caudalspine being so hard that they protect the animal not only

from invertebrate predators, but also from juvenile fish(Swaffar and O’Brien, 1996). In Chydorus species,conversely, cellular protrusions are obviously thinnerthan the integument itself, and their protective role isapparently insignificant.

However, these structures may protect cladoceransfrom highly specialized water mites with piercing-sucking mouthparts (Monakov, 1998). The protrusionsmay prevent the mites from reaching the integument ofprey with the gnathosoma and from attaching to theintegument by suction, as, for instance, the mite Eylais(Eylaidae) does.

The chydorid Pleuroxus trigonellus has muchsmaller protrusions along the lines of reticulation on thevalves (Frey, 1982). In Lake Svyatoe (Kosino, Mos-cow), parthenogenetic females with pronounced addi-tional sculpture coexist with females that have no suchsculpture (Figs. 5a–5d). We have also observed struc-tures similar to the cellular sculpture in some macro-thricid species, such as Macrothrix spinosa and Stre-blocerus pygmaeus.

In some cases, the formation of cellular protrusionson the valves can be explained as follows. It is typicalof many benthic cladocerans to conceal themselves onthe bottom surface with the aid of detritus particlesattached to the valves (Fryer, 1968). The detritusadheres to the mucous substance (see below); in addi-tion, various protrusions obviously facilitate its reten-tion on the valves. In particular, this concerns feather-like protrusions on the reticulation lines of Macrothrixlaticornis, which have not been described previously(Fig. 5e). All species of the genus Ilyocryptus withincomplete molting have marginal setae preserved onthe old valves; these setae also help to keep detritus par-ticles attached to the body surface (Chirkova, 1984).Such setae are also preserved on the old valves of Mono-spilus. Interestingly, the substrate and detritus particleson Ilyocryptus and Monospilus valves are inhabited bynumerous bacteria, as well as by plant and animal spe-cies constituting a specific community (Figs. 5f–5g).Diatoms are especially numerous on the valves; someof them are inhabitants of detritus, whereas others aretrue epibionts of the cladocerans, firmly attacheddirectly to the valves. At the same time, the chydoridsChydorus gibbus Sars 1891 and Oxyurella tenuicaudis(Sars 1862), which dwell near the bottom, also havedetritus attached to the valves (Frey, 1982a), although nospecial sculpture is observed on their surface (Fig. 5h).

In cladocerans of the genus Neothrix, the head andvalves are covered with numerous hairs (Figs. 6a, 6b).According to Fryer (1974), their function is exactlyopposite to the aforementioned retention of substrateparticles. These hairs are intended for minimizing con-tact of the body with detritus. This is why Neothrixspecimens in samples are always clean, almost withoutany foreign particles, in contrast to the “dirty” Macro-thrix and Ilyocryptus. Macrothrix hystrix Gurney 1927and M. pennigera Shen Chia-Jui, Sung Tahsiang et

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Chen Kou-hsiao 1961, which have similar setae on thehead and valves, are probably also bottom dwellerswith a similar system of body protection, but their bio-nomics have not yet been studied in detail.

Large lateral protrusions on the valves. A numberof species, such as Ilyocryptus cornutus Mordukhai-Boltovskoi et Chirkova 1972, I. paranaensis Paggi1989 (Ilyocryptidae), Macrothrix pennigera (Macro-

a e

b f

c g

d h

Fig. 3. Benthic anomopods: (a, b) Macrothrix laticornis, lateral view and head; (c, d) Drepanothrix dentata, ventral view and head; (e,f) Neothrix armata, lateral view and head; (g, h) Ilyocryptus spinifer, head in lateral and frontal view. Scale bars: (a, c, e, g) 100 µm;(b, d, f, h) 10 µm.

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a e

b f

c g

d h

Fig. 4. Benthic chydorines: (a, b) Disparalona rostrata, sculpture on valves and head near head pores; (c, d) D. acutirostris, sculp-ture on valves and head near head pores; (e, f) Chydorus invaginatus, lateral view and sculpture on valves; (g, h) C. obscurirostristasekberae, lateral view and sculpture on valves. Scale bars: (e, g) 100 µm; (a–d, f, h) 10 µm.

thricidae), Chydorus bicornutus Doolitle 1909, C.bicollaris Frey 1982, Pleuroxus pamirensis (Wer-estschagin 1923) (Chydoridae), Simocephalus lusati-

cus Herr 1917 (Daphniidae), have large lateral “horns”on the valves (Figs. 6c, 6d). Their function is unknown.According to Frey (1982b), they probably protect the

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ea

b

c

d

f

g

h

Fig. 5. Benthic anomopods: (a, b) Pleuroxus trigonellus, morphological type without additional sculpture; (c, d) Pleuroxus trigo-nellus, morphological type with additional sculpture; (e–g) Macrothrix laticornis, valve sculpture and detritus with a specific com-munity of organisms dwelling on the valves; (h) Oxuyrella tenuicaudis, valve. Scale bars: (a, c, f) 100 µm; (b, d, e, g, h) 10 µm.

“horned” Chydorus species from predators. Paggi(1989) hypothesized that these horns are anchoringstructures that prevent the body from moving backward

when antennae II move forward. This version appearsmore plausible. Macrothrix laticornis has small protru-sions anteriorly on the valves, which reinforce the shell

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a e

b f

c g

d h

Fig. 6. Benthic anomopods: (a, b) Neothrix armata, ventral view and setae on valves; (c, d) Ilyocryptus paranaensis inarmatus, ven-tral view and horn on valve; (e) Macrothrix laticornis, dorsal view (arrow indicates attachment site of adductor muscles); (f)Drepanothrix dentata, dorsal view; (g) Peracantha truncata, setae on ventral margin of valves; (h) Lathonura rectirostris, setae onventral margin of valves. Scale bars: (a, c, e) 100 µm; (b, d, f–h) 10 µm.

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in the areas where adductor muscles (shown with anarrow in Fig. 6e) are attached. The large horns on thevalves of the above anomopods have probably beenderived from similar protrusions. The macrothricidDrepanothrix dentata bears a peculiar medial horn dor-sally on the valves (Fig. 6f), which is reflected in itsspecies name.

There is some similarity between the lateral protru-sions on the valves and sharp, sometimes hooklike for-nices on the head of a number of Ceriodaphnia Dana1853 species (Jiang Xiezhi, 1977). On the whole, how-ever, medial anterior and posterior protrusions, medialkeels, and posterodorsal caudal spines are more typicalof planktonic species inhabiting the open littoral andinshore zones. The integument of the head and valves insuch species is usually thin and without protrusions(Frey, 1991).

Specialization of the marginal setae of the valves.The armature of the ventral margin of the valve, repre-sented by a small number of small uniform setae in arow along the entire margin of the valve, is a plesiomor-phic character in anomopods (Fryer, 1995). Differentspecialization of these setae was observed in anomo-pods that remain most of the time on substrates such asstems and leaves of littoral macrophytes, filamentousalgae (Fryer, 1968, 1974), or even the underside of thesurface film of water (Dumont and Negrea, 2002). Spe-cies dwelling on the surface of bottom sediments oftenhave an extremely large number of these setae (Fig. 1h),which bear long setules and form an integrated network(Fig. 6g). The setae are sometimes transformed intospecial plates, as in the macrothricid Lathonura rec-tirostris (Fig. 6h).

Long featherlike setae that protect the filtrationchamber from large particles (Fig. 7a), are typical of thediggers Parvalona, Leydigia, and Leydigiopsis. In Ily-ocryptus species, not only the ventral but also the pos-terior margin of the valve is armed with long setae,which bear strong spines (Figs. 7b, 7c). At the sametime, the setae on the valve margins of planktonic ano-mopods (Daphnia, Ceriodaphnia, Bosmina) are par-tially or completely reduced.

The lateral armature of the postabdomen. In Leydi-gia and Ilyocryptus, two digging anomopod species,the postabdomen bears strong lateral armature(Figs. 7d–7g). In both species, the postabdomen plays amajor role in locomotion within detritus or silts of dif-ferent textures (Fryer, 1968, 1974). The lateral setaeprotruding backward and to the sides considerablyenlarge the area of the surface contacting the substratein the course of pushing their body forward (which isuseful for moving inside finely dispersed silt), on theone hand, and take part in cleaning the ventral and theposterior margins of the valves, on the other hand. Itshould be noted that a number of other alonine species,close relatives (Parvalona; see Van Damme et al.,2005) or distant relatives of Leydigia (Leydigiopsis,Rhynchotalona, Spinalona, and Pseudomonospilus),

also have relatively well-developed lateral setae on thepostabdomen (Fig. 7h). At the same time, in the above-mentioned Leydigiopsis and Rhynchotalona, as well asin Alona affinis, A. quadrangularis, and some otheralonines, postanal spines of the postabdomen arestrongly developed; they help these animals move bypushing against large particles within coarse sedimentsor on their surface (Fryer, 1968). The combination ofstrong lateral setae and strong postanal spines is proba-bly evidence for adaptation to living in various sub-strates.

Spines and protrusions on the preanal margin of thepostabdomen. In several bottom-dwelling macrothricidspecies (Streblocerus, Drepanothrix, and some speciesof Macrothrix) strong spines are developed on the pre-anal margin of the postabdomen (Smirnov, 1976;Alonso, 1996), similar to those in Ilyocryptus (Fig. 8a).According to Fryer’s (1968) observations, the postab-domen of S. serricaudatus and M. laticornis plays nopart in locomotion, and its spines are used for cleaningthe setae of the posteroventral part of the valve. In Ily-ocryptus, the postabdomen is directly involved part inlocomotion, in addition to spine cleaning similar to thatof Streblocerus: its spines provide reliable contact withthe substrate. Almost no cases of special armature ofthe preanal margin have been observed in chydorids,except for Leydigia, which has preanal tubercles(Kotov, 2003; see Fig. 8b), and Chydorus pizarriAlonso 1998, which has small spines (Alonso, 1996).

Specialization of the setae and spines on antenna II.In the typically benthic forms of Ilyocryptus and Leydi-gia, thoracic legs take no part in locomotion, and themain locomotor organ is antenna II (Fryer, 1968),which bears long and strong spines (Figs. 8c, 8d) absentin planktonic forms. As specialization of antennae II inlittoral anomopods was previously discussed bySmirnov (1999), it is not considered here in detail.

Especially large exopodites of legs IV and V. Fryer(1968) noted this character in Leygidia. He related thedevelopment of powerful hind leg exopodites (Fig. 8f)to the necessity of improving ventilation of leg epi-podites (the gills) under conditions of oxygen defi-ciency: hind leg exopodites in most chydorid speciesare responsible for water flow in the filtration chamber,and oxygen deficiency is common at the bottom, espe-cially in the case of animals digging in the detritus. AllIlyocryptus species also have extremely largeexopodites of legs IV and V (Kotov and ⁄tifter, 2006;Fig. 8e). This is certainly an example of convergentevolution in phylogenetically distant lineages ratherthan a retained plesiomorphic character, because suchlarge leg epipodites are found neither in most extantanomopods from different families nor in their ances-tors (Fryer, 1995). At the same time, the hind legexopodites are small in the species living in the open lit-toral, where oxygen deficiency is rare, such as the spe-cies of the genera Monospilus and Rhynchotalona.

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a e

b f

c g

d h

Fig. 7. Benthic anomopods: (a–c) Leydigia propinqua, Ilyocryptus cuneatus, I. spinifer, respectively: setae on ventral margin ofvalves; (d, e) Leydigia propinqua, postabdomen; (f, g) I. isanensis and I. spinifer, respectively: postabdomen; (h) Rhynchotalonafalcata, postabdomen. Scale bars: (b, d) 100 µm; (a, c, e–h) 10 µm.

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Eye reduction and the large ocellus. This studydeals mainly with morphological adaptations of theanomopods, as most anatomic adaptations have notbeen studied sufficiently. Eye reduction, observed inseveral species, is an exception.

Vision is not the main source of information for bot-tom-dwellers. In some chydorid species, the eye is verysmall (Leydigia, Leydigiopsis) or entirely absent(Monospilus, Australospilus). At the same time, a largeocellus is typical of many benthic anomopods, such assome species of Ilyocryptus (Kotov and ⁄tifter, 2006).In some chydorids, the ocellus is several times larger indiameter than the eye, as is the case with Leydigia aus-tralis Sars 1885 and Pseudomonospilus biocellatus(Smirnov, 1971b, 1994). The ocellus is usually

extremely large in chydorids with the completelyreduced eye, such as Monospilus, Australospilus, andPseudomonospilus diporus (Smirnov et Timms 1983).This relationship between the eye and ocellus sizes isopposite to that in planktonic Daphniidae andBosminidae (Smirnov, 1971a), in which the eye is largeand functionally important, whereas the ocellus is verysmall or, in some species, even absent.

An extreme example of eye and ocellus reduction inanomopods is Spinalona, which completely lacks theeye pigment (Kotov and Elías-Gutiérrez, 2002). Theeye and the ocellus are reduced not only among bottomdwellers, but also in specialized cave-dwelling chy-dorids of the genus Alona living in entire darkness(Brancelj, 1997; Dumont and Negrea, 2002).

a b

c d

e f

Fig. 8. Benthic anomopods: (a) Ilyocryptus spinifer, preanal margin of postabdomen; (b) Leydigia ciliata, posterior margin of valve;(c) I. spinifer, antenna II; (d) L. ciliata, antenna II; (e) I. spinifer, leg exopodites; (f) L. ciliata, leg exopodites. Scale bars: (c, d, f)100 µm; (a, b, e) 10 µm.

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DISCUSSION

It should be noted that many species of the genusAlona that having none of the adaptive charactersdescribed above are, nevertheless, very successful bot-tom dwellers. Unlike digging anomopods, they occuron the bottom of water bodies with different types ofbottom sediments, expand to the macrophyte and inter-stitial zones, and even live in subterranean waters(Dumont and Negea, 2002).

Reddish coloration, resulting from high concentra-tion of hemoglobin in the hemolymph, is often typicalto bottom-dwelling anomopods. However, hemoglobinwas found both in typically littoral species (Smirnov,1971c) and in many planktonic animals inhabitingsmall water bodies, such as Moina and Daphnia(Smirnov, 1975), as well as in the hemolymph of allanomopods and of “large” branchiopods (Martin,1992). A high hemoglobin concentration in thehemolymph is typical of branchiopods living underconditions of oxygen deficiency, either in bottom sedi-ments or some other habitats.

Living upon a substrate is a phylogenetically moreancient mode of life for cladocerans than living in theplankton (Smirnov, 1975; Fryer, 1995). Yet anomopodsare much more numerous, diverse, and often morestrongly specialized for living in particular microhabi-tats than large branchiopods, the ancestors of cladocer-ans. We have revealed some common adaptations ofbenthic anomopods, especially those related to locomo-tion and foraging, that are not observed in the largebranchiopods. Therefore, the corresponding charactersare not plesiomorphic. The evolution of these structuresproceeded largely independently in different lineagesof the order Anomopoda. The greatest number of com-mon characters was observed in Leydigia and Ilyocryp-tus, the genera phylogenetically distant from eachother.

It has been repeatedly suggested that body flattenedfrom the sides is an adaptive trait in bottom-dwellingchydorids (Fryer, 1968; Smirnov, 1971a, 1971b), butthis idea is open to criticism. A flattened body, indeed,has a smaller frontal area and, hence, experiencessmaller substrate resistance, which may be useful foranimals moving in a dense substrate. Indeed, large andmedium-sized benthic chydorids (Leydigia, Leydigiop-sis, Parvalona, Oxyurella) and macrothricids (Macro-thrix laticornis and Streblocerus serricaudatus) havethe body flattened from the sides. In some Ilyocryptusspecies, on the contrary, the body is massive; in addi-tion, two species bear strong horns on the valves (seebelow), which by no means help to reduce substrateresistance. The narrowest body is found in Ilyocryptusspecies capable of swimming at the adult stage, whichspend relatively little time in bottom sediments (Kotovand Dumont, 2000). In my opinion, they move in bot-tom sediments so slowly that the problem of substrateresistance is of no major importance to them. Thealmost spherical Monospilus also moves slowly.

A strongly flattened body is also typical of plank-tonic Daphnia species (Fryer, 1991). Although theirenvironment is less dense than detritus, daphnias movein it at a relatively high speed and, therefore, gainadvantage from minimizing frontal resistance. Themost flattened body is found in the chydorids Acrope-rus Baird 1845 and Camptocercus Baird 1845 and inthe macrothricid Bunops Birge 1893; all these dwellmostly in macrophyte beds (Fryer, 1968; Dejdar, 1927).

A strongly flattened body appears in cases wherefrontal resistance should be minimized, which alsoapplies to benthic forms. In anomopods, a more or lessspherical body is clearly apomorphic and appears inde-pendently in different lineages of the order Ano-mopoda, whereas a moderately flattened body, typicalof many benthic forms, can be regarded as plesiomor-phic. In Cladocera’s closest relatives, the orders Lae-vicaudata and, especially, Cyclesterida (formerly“Conchostraca”), the body is usually flattened from thesides. It was probably like that in the ancestors of allcladocerans.

The presence of protrusions on leg epipodites(Smirnov, 1971b, 1971c) and loops and blind divertic-ula of the gut (Smirnov, 1969) should also be consid-ered among the important features of littoral anomo-pods. However, unlike the characters described above(present in bottom-dwelling anomopods and obviouslyevolved in different anomopod lineages in parallel), thecharacters revealed by Smirnov are typical of a largespectrum of littoral crustaceans with different bionom-ics and are candidates for the role of general synapo-morphies in chydorids and some macrothricids. Thefamily Macrothricidae is probably a mixed group (Ole-sen, 1998; Dumont and Silva-Briano, 1998), and thepresence of gut loops may serve as a useful characterfor dividing the family into monophyletic taxa. At thesame time, ilyocryptids, one of the most primitive fam-ilies, have the gut without loops, like daphniids,moinids, and bosminids.

Of special interest are similarities in the structure ofinteguments between Anomopoda and Ostracoda(Bronshtein, 1947; Sex and Parthenogenesis…, 1998),common crustaceans close to Cladocera in size andevolutionary age. Different authors differently explainthe presence of sculpture on the valves of ostracods;this is natural, because the sculpture is usually multi-functional (Shornikov, 1981). Strong lateral protrusionsare often present on the valves; they are especially typ-ical of ostracod species inhabiting the surface of the siltand probably prevent the animal from sinking into it.The hypothesis of their protective function is also dis-cussed, although their protective role in ostracods andcladocerans has not yet been demonstrated conclu-sively. Triebel (1941) suggested that small spines on theostracod shell surface provide for better retention ofparticles used for concealment. Such a mechanism ofconcealment was repeatedly observed in some crabs(Birshtein and Zarenkov, 1988).

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Cyprididae ostracods, digging into the silt, haveboth well-developed sculpture on the valves and strongclawlike setae on the furca (Bronshtein, 1947). Cyprid-ids move amid silt particles by pushing the body againstthe substrate with the furca, which operates similarly tothe postabdomen of some anomopods. The clawlikesetae are similar to the lateral setae on the postabdomenof Leydigia and Ilyocryptus; they are also used forenlarging the area of the furca–substrate contact whenthe animal is moving amid silt particles.

Thus, adaptations to the benthic mode of life similarto those of Anomopoda are also observed in crusta-ceans phylogenetically distant from Cladocera.

ACKNOWLEDGMENTS

The author is grateful to N.N. Smirnov for his valu-able advice at every stage of this study; to N.M.Korovchinsky for his help in selecting relevant publica-tions; to A.Yu. Sinev for a series of helpful comments;and to K. Van Damme and H.J. Dumont (Ghent, Bel-gium), L. Sanoamuang (Khon Kaen, Thailand), S.Tanaka (Toyama, Japan), and M. Elías-Gutiérrez (Che-tumal, Mexico) for the samples of Cladocera they pro-vided. The author also thanks I.B. Mertsalov for hishelp with sample preparation and V.N. Antropov fortechnical assistance in scanning electron microscopy.

This study was supported by the Russian Founda-tion for Basic Research, project no. 03-04-48879.

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