sign in sign up
<<
Home , Anomopoda, Bosmina, Bosminidae, Branchinectidae, Branchiopoda, Branchipodidae

'[fA^' Microscopic of Volume 9: Crustacea, pages 25-224 ^r © 1992 Wiley-Liss, Inc.

Chapter 3

Branchiopoda

JOEL W. MARTIN Natural History Museum of Los Angeles County, Los Angeles, California

INTRODUCTION lopodous limbs, although many of the diverse "cladocerans"—^making up half of the eight The great morphological diversity seen extant orders, accepting Fryer's (1987c) clas­ among branchiopod very nearly sification—do not conform to this descrip­ prohibits generalizations about form and tion. Although many branchiopods possess function. Branchiopods are among the most numerous body somites, others exhibit rather diverse of the classes of Crustacea, which in extreme fusion and tagmatization. Append­ turn is the most morphologically diverse (al­ ages are often flat and leaflike, sometimes though not the most speciose) taxon on earth. termed "phyllopods"; however, trunk limbs No single character or group of characters are more or less stenopodous in two predatory uniquely defines the , and for orders (Haplopoda and ). Al­ any given suite of characters there are many though as a taxonomic name meant to include exceptions. Early schemes of branchiopod all branchiopods the term Phyllopoda has classification, and many of the characters been abandoned (Fryer, 1987c), it still is oc­ upon which they were based, were reviewed casionally employed, in a very different ca­ by Fryer (1987c), who commented on the im­ pacity, to encompass various as­ pressive heterogeneity of extant branchio­ semblages (Schram, 1986) or component pods, a problem recognized by many previous groups of the Branchiopoda (Walossek, in students of the Crustacea, and discussed the press). Usually there are no on difficulties in formulating an unambiguous the "abdomen" (which is often defined as the definition that would apply to all members of postgenital somites but is a rather meaning­ the group. Perhaps as a consequence of the less term in this group), other than character­ group's morphological diversity, the mono- istic caudal rami (sometimes termed furcae phyletic status of the branchiopods is still or cercopods) on the or anal somite questioned by some worlters (e.g., see Wil­ (see Bowman, 1971; Schminke, 1976; and son, in press), although arguments for mono- Walossek, in press, for terminology) in most phyly based on larval characters (e.g., Sand­ groups. A is present in many groups, ers, 1963), sperm morphology (Wingstrand, and may be a univalve shield (notostracans 1978), and feeding apparatus (Walossek, in and the extinct Rehbachielld), or bivalved, press) seem strong. reduced, or absent (adult anostracans). Most branchiopods are small, freshwater Among the bivalved groups, where the valves with numerous, similar, phyl- actually represent a secondary shield over- MARTIN growing the initial one (Walossek, in press), and Lynch, 1987). Consequently, some bran­ it is hinged only in the Laevicaudata (and chiopod peculiarities may represent conver­ simply folded in the others); in haplopods and gent adaptations to the freshwater habitat. onychopods the carapace valves are greatly Traditional classifications divided the ap­ reduced and can no longer enclose any part of proximately 800 of living branchio- the body. A small cuticular "dorsal organ" pods (Balk, 1982) among four major group­ (= neck organ) is present in all groups at ings, usually given ordinal status: some stage of development (usually larval), (fairy and brine ), (tadpole but the homology is, in my opinion, uncertain shrimps), Conchostraca (clam shrimps), and (Martin and Laverack, in press). Most (not (water ). The Branchiopoda is onychopods or haplopods) possess a rather now recognized as consisting of eight, rather deep ventral groove, extending posteri­ than four, extant orders (Fryer, 1987c). These orly from the cephalic feeding groove and eight extant groups are the result of recogniz­ formed by an invagination of the cuticle of the ing that the "Conchostraca" consists of two thoracic stemites. Associated with this food rather different assemblages of bivalved crus­ groove are certain unique modifications of taceans, the orders Laevicaudata ( Lyn- the feeding appendages and thoracopods ceidae) and Spinicaudata (all other families (Walossek, in press). In those orders that have formerly included as conchostracans), and retained the nauplius larval stage (all groups that the "Cladocera" encompasses four mor­ except the anomopods, ctenopods, and ony­ phologically disparate taxa (the orders Ano- chopods), the nauplius is recognizable in its mopoda, , Onychopoda, and Hap- possession of the following combination of lopoda). Cladocerans encompass the widest features: (1) an unsegmented first that range of morphological and behavioral habits bears only distal setation (although segmenta­ of any branchiopod grouping, and in retro­ tion is evident in larvae of some taxa and in spect it is surprising that the group was not some extinct forms), (2) a second antenna formally reorganized into four distinct orders with an elongate protopod that is more than until recently (Fryer, 1987a,c). In general, I half the total length of the , (3) a agree with Fryer's (1987c) classification, al­ single spine on the distal article of the second though I might argue, based on naupliar char­ antennal protopod, (4) an absence of setae on acters of lynceids that were not available to the medial surface of the second antenna en- Fryer (C. Sassaman, unpublished data), that dopod, and (5) a uniramous mandible (Sand­ the Conchostraca might still be retained as a ers, 1963). Finally, all species examined pos­ valid taxon despite the many peculiarities of sess an ameboid sperm lacking on acrosome adult lynceids (Fryer, 1987c; Martin and and flagellum; this combination is unique Belk, 1988). Occasionally in this review, for among the Crustacea (Wingstrand, 1978). the sake of conserving space, I employ the Most species have adapted to life in tempo­ terms conchostracan and cladoceran when dis­ rary or permanent freshwater ponds, small cussing the above orders. The orders Anostraca streams, and occasionally lakes. Many of the and Notostraca are still believed to be valid habitats are ephemeral, i.e., they are dry dur­ monophyletic groupings. There are also several ing certain seasons, but are permanent in the taxa of ordinal or subordinal status sense that they persist from year to year. It is (Lipostraca, Kazacharthra, and possibly Reh- unclear whether multiple radiations into hachiella; see Fryer, 1987c; Miiller, 1983; freshwater occurred, as perhaps suggested by Walossek, in press; Miiller and Walossek, in the discovery of a marine anostracan-like press); these are not discussed further here but branchiopod from the Upper are of tremendous importance in phylogenetic (Walossek, in press), vs. a single invasion considerations (see Walossek, in press). Also that preceded the extensive morphological ra­ crucial for understanding branchiopod evolu­ diation (see Potts and Duming, 1980; Kerfoot tion, and for understanding much of the anat- BRANCHIOPODA 27

TABLE 1. Classirication of the Extant Branchiopoda Followed in This Chapter* Anostraca Family (1, Branckinecta) Family Artemiidae (1, Anemia) Family (5 or 6) Family Streptocephalidae (1, Slreptocephalus) Family (3, . Dendrocephalus, Thamnocephalus) Family (7) Family Polyartemiidae (2, Polyartemia, Potyartemiella) Family Linderiellidac {2, Underiella and Dexleria, both monotypic) Order Notostraca Family Triopsidae (2, , ) Formerly "Conchostracans": Order Laevicaudata Family (3, . Lynceiopsis, Paraiimnetis) Order Spinicaudata Family Cyclestheriidae (1, Cyckstheria, monotypic) Family (4, Caeneslheria, Caeneslheriella, Cyzkus, Eocyzkus) Family (5) Family (6) Formerly "Cladocerans": Order Family (6) Family (2, Moinodaphnm (monotypic) and Molna) Family (2, and Bosminopsis (monotypic)) Family (16 or 17) Family (over 30) Order Ctenopoda - Family (6 or 7) Family Holopediidae (1, ) Order Onychopoda Family Polyphemidae (1, ) - Family (6 or 7) Family Cercopagidae (2, Bylhotrephes, Cercopagis) Order Haplopoda Family Leptodoridae (1, Ijeptodora, monotypic) * After Belk, 1982; Mordukhai-Boliovskoi and Rivier, 1987; Fryer, 1987c; Dodson and Ftey, 1991; and other sources. No phylogenetic relationships are implied. Numbers in parentheses are approximate number of extant genera, names of which are provided for those families with four or fewer. For reviews of various previous classification schemes and the characters on which they were based, see Fryer {1987c).

omy of adults, but given only brief mention in 1945; Tasch, 1963, 1969; Smirnov, 1971; this review, are branchiopod larval features, Briggs, 1976 [although Branchiocaris is no Unfortunately, Fryer (1987c), although longer believed to be a branchiopod]; Berg- hinting at the affinities of some taxa, pro- strom, 1979, 1980; Miiller, 1983; Fryer, posed no explicit relationships among the 1985, 1987c, 1991a,b; Walossek, in press), eight extant orders, and although Walossek which, as noted by Fryer (1987c), is longer (in press) suggests relationships among many than the time during which all radiations of of the branchiopods, he does not attempt to terrestrial vertebrates took place, it is not sur- resolve relationships among the six orders prising that extensive morphological diversi- formerly comprising the "cladocerans" or fication has occurred, and the relationships "conchostracans." For the present chapter I among the constituent groups may be ob- have simply listed the extant families under scured by homoplasies. Another problem for the orders proposed by Fryer (Table 1), which the phylogenist or comparative morphologist 1 assume will be accepted by most carcinolo- is that the branchiopods exhibit a curious gists, without giving any indication of phyio- combination of morphological plasticity and genetic relationships within the Branchiopoda evolutionary stasis. The external and cellular as a whole. morphology of some extant branchiopods can Because of the tremendous amount of time be modified by altering the conditions under that branchiopods have existed (see Linder, which they are reared. Developing daphniids 28 MARTIN (Anomopoda) will produce spines in response tions (e.g., MacRae et al., 1989; Warner to waterbome chemical cues of predators, etal., 1989; Browne etal., 1991; Belket al., with the number of spines increasing with 1991; and a series of six volumes under the predator density (e.g., see Krueger and Dod- direction of the Anemia Reference Center in son, 1981; Havel, 1986; Havel and Dodson, Ghent, Belgium [Persoone et al., 1980; Sor- 1987;Dodson, 1989; Walls and Ketola, 1989; geloos et al., 1987]) provide access to the vast Harvell, 1990). Cyclomorphosis is common Anemia literature. The attention lavished on (reviewed by Jacobs, 1961, 1987; Kerfoot, Anemia is a result of its abundance, economic 1980), and the sex ratio of developing em­ importance, ease in laboratory rearing, and bryos and the reproductive switch from pro­ importance as a model crustacean for compar­ ducing embryos vs. resting in some ative morphological studies. Similarly, "cla- branchiopods can be influenced by a variety docerans," primarily the Daphniidae (Ano­ of environmental stimuli (reviewed by Hobaek mopoda), have been the focus of numerous andLarsson, 1990). Other branchiopods have experimental studies, in part because of their been shown capable of rapid and striking value as test organisms for toxicity studies, changes in morphology caused not by exter­ ease in manipulation, and abundance (e.g., nal cues but by mutation. Bowen et al. (1966) see papers in Peters and De Bemardi, 1987). documented a single mutation in the anostra- References to morphological studies on ano- can Anemia franciscana that produces, in­ mopods can be found in the works of Fryer on stead of the normal brine with two the Daphniidae (1991a), Chydoridae (1963, widely separated eyes borne on stalks, a Cy­ 1968) and Macrothricidae (1974). clopean mutant with a single, median eye, Because the majority of previous studies complete and entirely functional, with all have centered on Anemia and some of the musculature and nerves operational. In stark daphniids, and because my own knowledge is contrast, one species of notostracan, known severely restricted to a few conchostracans, from from the (Trusheim, many of the following examples are from 1938), was considered conspecific with ex­ these taxa. But I strongly caution the reader tant by Longhurst (1955) against making any generalizations based on despite a time difference of some 200 million examples presented here. The diversity of years. If these fossils are indeed conspecific branchiopod anatomy and ultrastructure can­ with extant Triops cancriformis (which now not be deduced from a few selected illustra­ seems unlikely in light of ongoing electro- tions. For example, it would be misguided to phoretic studies [C. Sassaman, personal com­ extend an observation made on the feeding munication] that indicate divergence despite and absorption mechanisms in Artemia, so morphological similarity), then Triops can­ often depicted as a "typical" branchiopod, to criformis is the oldest continuous species of all other anostracans, some of which feed by any on earth (Fryer, 1985). rather than filtration, and meaning­ The literature on some branchiopods is less to impose such generalizations upon vast, while other groups have escaped serious other orders, such as members of the anomo- attention for many years. The Anemia, pod family Chydoridae, where there are probably the best known genus in all of the known filter feeders, scrapers, scavengers, Crustacea (rivaled only by , another and even ectoparasites on freshwater hydras branchiopod), has been the subject of over (Fryer, 1968). Several sections, such as those 4,000 primary references (Browne et al., on excretion and osmoregulation, are based 1991), and is so well known at the cellular on the brine-inhabiting Artemia, a species level that it has aided our understanding of the with diametrically opposed needs in these ar­ function of the eukaryotic cell (MacRae et al., eas compared to most other branchiopods, 1989). Several recent and extensive compila­ which inhabit fresh waters. Examples pre- BRANCHIOPODA 29 sented here must be viewed with the great typic genera), Polyartemiidae (two genera), functional and anatomical diversity of branch- Streptocephalidae (one genus, Streptoceph- iopods in mind. alus), and Thamnocephalidae (three genera). This group includes the largest branchiopods, EXTERNAL MORPHOLOGY reaching lengths of up to 100 mm in Branchi­ Anostraca necta, but most are 15-30 mm as adults (e.g., Anostracans (fairy shrimp) (Fig. lA) in­ see Linder, 1941). habit fresh or saline inland waters or (rarely) Anostracans are characterized by an elon­ marine lagoons. The habitat is most often an gate body with little regional specialization ephemeral one, although some species inhabit (tagmatization) within the three obvious permanent larger bodies of water in the Arctic tagma (head, thorax, and abdomen). There is and Antarctic; these habitats tend to have few no carapace, although it has been argued that predators. There are eight extant families: Ar- a headshield is present in early larval stages temiidae (one genus, Artemia), Branchinec- (e.g., see Schrehardt, 1986, 1987a, for fig­ tidae (one genus, ), Branchipo- ures; Walossek, in press, for discussion). didae (five or six genera), Chirocephalidae There are 19-27 postcephalic segments (seven genera), Linderiellidae (two mono- (fewer in some extinct taxa; see Fryer,

Fig. 1. Orders Anostraca and Notostraca. A: Branchinecta conservatio (Anostraca). B: Lepidurus pack- ardi (Notostraca). al, first antenna (antennule); a2, second antenna; c, carapace; cf, caudal furca or ramus (= cercopod); ep, epipod of thoracic limb; p, external penis; s, sulcus of carapace; t, supra-anal plate of telson. 30 MARTIN 1987c). Fryer (1987c) stated that there is a "abdomen" consists of 9 segments, the first pair of dorsal sensory setae on each segment, two of which are genital and fused, and often but I have not seen these in all taxa. The head considered part of the thorax (see Benesch, is short and frontally rounded or even flat­ 1969; Walossek, in press), and the last of tened. The paired compound eyes are well which is the telson or anal somite. The post- developed and borne on movable stalks, a genital region consists of six cylindrical seg­ condition unique among branchiopods. The ments plus the telson and bears no appendages antennules of adults are simple, one-seg­ other than a pair of rather flattened caudal mented structures that are uniramous and rami (fused into paired plates extending for­ more or less tubular in design. The antennae ward along the abdomen in the genus Tham- exhibit extreme sexual dimorphism, being nocephalus) borne on the telson. Other exter­ less mobile (Fryer, 1987c) and often simple in nal features include an elongate brood pouch females (with several exceptions) but modi­ in females and an extensible penis in males, fied as highly movable claspers in males. The both of which are borne on the first post- modified male antennae may be enormous thoracic segment (= the twelfth thoracic of grasping structures, often with species-spe­ Benesch. 1969, and Walossek, in press), cific basal outgrowths and elaborate ornamen­ which typically is fused in both sexes to the tation. The labrum is large and fleshy, with following segment. functional, secretory labral glands often per­ sisting into the adult stage. The mandible is of Notostraca the grinding and rolling type, but in some taxa The Notostraca (Figs. IB, 2), commonly may be secondarily modified for biting (e.g., called tadpole shrimps, are all members of a Branchinectd). The maxillules are greatly re­ single extant family, Triopsidae, consisting of duced in extant forms, existing only as modi­ two genera, Triops and Lepidurus. There are fied gnathobases that bear a single row of approximately ten extant species (Linder, long, denticulate spines and a single stout 1952; Longhurst, 1955; Belk, 1982). Spe­ spine (Fryer, 1987c). The maxillae consist of cies inhabit inland freshwater pools, which a single lobe (the proximal endite) with two or are sometimes slightly alkaline or even brack­ three anteriorly directed setae and a variable ish. Most pools are temporary, but as with number of distal setae. Postcephalic limb- anostracans some are found in predator-poor bearing somites (which traditionally have permanent bodies of water. Notostracans are been termed the "thoracic" segments) are eas­ omnivorous, and are predominantly benthic, ily recognizable (i.e., there has been little or although they can swim well. They may attain no fusion) and may number 11, 17, or 19 lengths of 100 mm (Belk, 1982), although (excluding the two often-fused genital most often they are smaller, 30-50 mm. They somites), although as few as eight are known do not filter but rather feed on or on in one extinct species. Appendages of these other organisms, hving or dead, and will even somites are foliaceous, phyllopodous limbs pursue and catch anostracans and small that beat with a distinctive metachronal (Home, 1966; Martin, 1989a). Their various rhythm and that display considerable serial anatomical modifications reflect these basic similarity. Each limb has an exopod, endo- functional and ecological differences from pod, and a series of endites and in most spe­ anostracans and other branchiopods. cies is modified for filtering. Additionally, Notostracans superficially resemble anos­ each thoracic limb bears a "respiratory" epi- tracans that have acquired a shieldlike cara­ pod (actually osmoregulatory; see later) and pace (Fig. IB). But the resemblance goes no one or two exiles proximal to the epipod. The further. Although the body is elongate, with a more distal exopod is clearly demarcated variable number of cylindrical trunk somites from the rest of the limb. The food groove (varying even within a species or population), between the limbs is narrow and deep. The they are functionally and morphologically BRANCHIOPODA 31

Fig. 2. Order Notostraca, SEM of selected external features. A: Ventral view of "thoracic" limbs and cylindrical rings of anterior region of "abdomen," Triops lon_^icaudatus. Note high numbers of limbs per body somite. B: Base of single branch of caudal rami (= cercopod). (Courtesy of B. Felgenhauer.) C: Heavily spined mandible and first maxilla, Triops longicaudataus. mb, mandible; mx, first maxilla. very different from anostracans (see Fryer, sally. The compound eyes are technically ex­ 1988). The carapace is a shieldlike expansion ternal but become internalized during ontog­ of the dorsal cuticle, presumed to be of the eny; in adults the now-sessile compound eyes maxillary somite, and contains between its remain in contact with the external environ­ inner (ventral) and outer (dorsal) surfaces the ment via a small median opening (Fig. 124F, coils of the maxillary glands. It is not hinged G), seen also in some conchostracans. The or folded, but a longitudinal carina and a pos­ antennules are short and uniramous. The an­ terior carapace sulcus allow considerable tennae also are uniramous and are reduced or flexibility and mobility of the trunk. The car­ absent. The labrum is a flat, stiff plate that apace extends anteriorly to shield the head does not bear secretory glands in the adult. and posteriorly to shield the anterior half of The mandibles are enormous and well devel­ the trunk. It differs from the carapace of the oped for biting, with sharp denticles along the bivalved branchiopod orders, in which the molar region (Fig. 2C). The maxillules have carapace overgrows the head, in that, in no- two segments and are robust and heavily mus­ tostracans, the head is incorporated into the cled and sclerotized, the only maxillules in shield, with the compound eyes visible dor- the Branchiopoda capable of true biting. The MARTIN maxillae are reduced to small lobes, probably of their time at or just above the bottom and representing remnants of the former gna- feed primarily by scraping, scavenging, or thobases (Fryer, 1987c, 1988), with the open­ "grazing" on detritus (Martin et al., 1986; ing of the maxillary gland on an adjacent tu­ Martin and Belk, 1988; Martin, 1989a). bular outgrowth. The distinction between Laevicaudatans were for many years thorax and abdomen is unclear; altogether the grouped with other families of "" trunk may bear 35-72 pairs of limbs, of which (see below) in the Conchostraca. Although 24—60 occur posterior to the genital segment they resemble other conchostracans in the (segment 11) and are usually termed abdomi­ possession of a bivalved carapace, strong car­ nal. Posterior to the genital segment there apace adductor muscle, telsonal filaments (= may be up to six pairs of limbs on one cylin­ postabdominal setae), and modified male first drical somite or body ring (Fig. 2A). The thoracopods, there are many more differences "thoracic" limbs (those anterior to the genital than similarities (Linder, 1945; Fryer, 1987c; somite) are nonfiltratory and extend laterally Martin and Belk, 1988). The bivalved cara­ rather than ventrally from the axis of the pace is globose, nearly spherical, almost cir­ body. Although somewhat phyllopodous, cular in lateral view, and lacks an "umbo" or these limbs have clearer distinctions among any growth lines or other external ornamenta­ the various endites than do the anostracan tho- tion (Fig. 3C). The two valves are joined dor- racopods. In the anterior one or two postceph- sally by a true hinge in a recessed groove, alic limbs, some endites may be elongate and although the valves are not entirely separate filiform. The gnathobases of the trunk ap­ but are fused for a short distance along the pendages are thick, sclerotized, and impres­ dorsal border. The head region is enormous sively armed with a variety of spines and se­ (Fig. 3D,E), taking up nearly a third of the tae. Thoracic appendages also bear an exopod space between the valves, and articulates with and an inflated epipod. In females, the limbs the trunk, thereby becoming capable of ex­ of the genital somite are modified as oostego- tending beyond the valves, which it often pods, in which the endopod has become fused does. The eyes are sessile and "internal," in with the "apical lobe" (Fryer, 1988) to form contact with the external environment via a an -bearing pouch; the cover of this pouch median pore (Fig. 135C) (as in notostracans); is formed by the modified exopod. The food they characteristically quiver back and forth, groove between the gnathobases of the thora- much as in some anomopod cladocerans. The copods is well developed but is broad and head is produced into an elongate "rostrum" shallow. More posterior appendages are less more so than in other clam shrimps, and bears complex, becoming simple and flaplike even­ distinctive paired fields of sensilla on either tually. The long, cylindrical "abdomen" ter­ side of the midrostral carina just posterior to minates in a telson that bears a pair of long, the above-mentioned pore (Figs. 3E, 135C). thin, cylindrical, multiarticulate caudal rami The antennules are short, uniraraous, and (Fig. 2B), between which extends a platelike two-segmented, and bear sensory setae on the process in Lepidurus. expanded distal segment. The antennae are large and natatory, with the anterior flagellum Laevicaudata bearing short spines and with both rami bear­ This order contains one extant family, the ing plumose, posteriorly directed natatory se­ Lynceidae (Fig. 3C-E), with approximately tae, one per segment. The labrum is huge and 40 species (Martin and Belk, 1988) in three fleshy, and bears large internal secretory genera: Lynceus, Lynceiopsis, and Paralim- glands. The mandibles are large and heavy, of netis. Species are known from ephemeral the grinding/rolling type, but the masticatory ponds and occasionally streams on all conti­ surfaces are narrow and bear stout teeth; the nents except (Martin and Belk, proximal end of the mandibles articulates 1988). Lynceids are small to medium-sized with a cuticular ridge (the fornix) rather than (to about 8 mm) branchiopods that spend most on a protrusion of the head cuticle (as is the BRANCHIOPODA 33

Fig. 3. The two conchostracan orders Spinicaudata and Lae- gracilicornis corresponding approximately to region marked by vicaudata. A: ovisimilis (Spinicaudata), lateral view arrows in D. Note relatively large head size. (After Martin, with right valve removed. (After Martin, 1989b). B: Eulimnadia 1989a.) af, anterior flagellum of second antenna; am, adductor texana (Spinicaudata), enlargement of head region (approxi­ muscle of carapace (present also in A but not visible in this mately the area between arrows in A.) (After Martin, 1989a.) C: photograph); anl, first antenna; cf, caudal furca; cl, male Lynceus gracilicornis (Laevicaudata), dorsal view of carapace. clasper; ce, compound eye; do, dorsal organ; em, egg mass; ep, Note recessed hinge between valves, lacking in A, and absence epipod; f, fornix of head region; h, head region; hp, hepatopan- of growth lines. (After Martin and Belk, 1988.) D: Lateral view creas (digestive ceca); la, labrum; mb, mandible; ne, nauplius of Lynceus brachyurus with right valve removed. (After Martin eye; pf, posterior flagellum of second antenna; sf, sensory field. and Belk, 1988.) E: Enlargement of head region of Lynceus MARTIN case with spinicaudatans). The maxillules are mostly in the Cyzicidae and Limnadiidae, can reduced to a small, thin, setose lobe. The attain lengths of 18 mm (mature females), but maxillae are vestigial, with no obvious masti­ most are on the order of 8-10 mm. All inhabit catory function, and carry the duct of the ephemeral freshwater pools or prairie streams, maxillary gland. The trunk is short, consist­ and they are commonly found with other ing of only 10 segments in males and 12 in branchiopod species. Cydestheria also fre­ females, with all segments bearing append­ quents permanent bodies of water. ages. The first trunk appendage is modified in Like the lynceids, all spinicaudatans have a males as a clasper for grasping the female bivalved carapace and powerful adductor carapace during mating; however, the clasper muscle, but the nature of the valves and the components are derived from different endites external and internal morphology differ sig­ from those in the Spinicaudata. The second nificantly. The valves are joined dorsally by a male appendage is sometimes modified as simple fold; there is no true hinge. All species well {Paralimnetis, Lynceiopsis), but never have external growth lines on the carapace. as a clasper. More posterior appendages are The carapace encloses the entire body, and foliaceous, directed ventrally, and display the small and usually narrow head region marked serial similarity (e.g., Martin et al., (Fig. 3A,B) is not capable of articulating with 1986), differing mosdy in size and develop­ the trunk and extending beyond the valve ment of the various endites. The gnathobase is margins, although in large individuals of well developed, with stout spines and setae, the head may protrude slightly. The and is directed anteriorly. The food groove is compound eyes are assumed to have become broad and V-shaped. Each limb has a well- "internalized" during ontogeny at least in developed exopod, an inflated "respiratory" some families, since the same median pore as epipod (Fig. 3D), and several endites; these described above for notostracans and lae- often bear large scraping setae and perform a vicaudatans exists. These eyes are paired, but variety of functions (although not filtration). in some species, and especially in Cydesthe­ The trunk terminates in an anal somite (= tel- ria, they appear very close together and may son?) that bears telsonal filaments (postab- even be fused into one functional unit. The dominal setae) but lacks caudal rami, and is labrum is small, often tipped with setal tufts, ventrally shielded by opercular lamellae of and contains secretory glands. The antennules the penultimate trunk somite. There are no are elongate and subdivided into several spines on the dorsal surface of the trunk lobes, each of which bears sensillae, except in somites. Oviducts of females open on the 11th Cydestheria, which has a straight, tubular an- somite; those of the male open either along­ tennule with the sensory setae confined to its side the anus (claimed by Under, 1945) or at tip. The antennae are large and natatory with the base of a posterior trunk limb (Sars, plumose setae and sometimes with dorsal 1896). In females, unique lateral flaps of the spines. Although in some ways similar to lae- body wall work in conjunction with exopods vicaudatan antennae, the musculature appar­ of trunk limbs nine and ten to support the egg ently differs significantly (see Fryer, 1987c). mass. Mandibles are of the rolling/grinding type, but they lack the heavy teeth seen in notostra­ Spinicaudata cans and laevicaudatans, and they articulate with a protuberance of the head cuticle (Mar­ The Spinicaudata (Fig. 3A,B) encom­ tin, 1989a). The maxillules are reduced and passes those taxa most commonly referred to probably represent only the remaining gna­ as "clam shrimp," formerly grouped with lae- thobase, being armed with stout spines and vicaudatans in the Conchostraca. There are setae. The maxillae are reduced to small lobes four extant families: Cyclestheriidae (mono- with distal setae. The trunk, although short, is typic, Cydestheria hislopi), Limnadiidae (six comprised of 16-32 somites; and thus there genera), Leptestheriidae (five genera), and are 16-32 pairs of trunk limbs. The first and Cyzicidae (four genera). Some species. BRANCHIOPODA 35 second trunk limbs of males are modified as Anomopods are characterized by having a claspers (only the first in the Cyclestheriidae, short body exhibiting extreme fusion. The in which males are rare), which superficially carapace, which is often elaborately modified resemble those of the laevicaudatans (the or ornamented (e.g., Fig. 5D, and Frey, clasper components are derived from different 1982a,b, 1987) and may bear numerous endites; Fryer, 1987c). More posterior trunk pores, is bivalved but lacks a true hinge, and limbs are foMaceous, directed ventrally, and it does not enclose the head, which is short are composed of an exopod, endopod, and and often expanded dorsally into a protective protopod (corm) subdivided into endites. The headshield (Fig. 4C,E,G). The compound trunk limbs display serial similarity, differing eyes are fused into a single median eye (also mostly in size. Each has a "respiratory" epi- true in some spinicaudatans), which may be pod (Fig. 3A), elongate endopod, and well- variously reduced or absent, but there is no developed gnathobase, which differ slightly known connection to the external environ­ in spination from anterior to posterior limbs. ment via a median pore (although some spe­ The food groove between the gnathobases is cies have a median head pore; e.g., see Ker- broad and shallow, and usually somewhat foot et al., 1980, for Bosmina). The labrum is U-shaped. In females, trunk limbs 9-11 often short and fleshy, and bears secretory glands. bear "dorsal filaments" (actually modified Female antennules are variable, either tubular dorsal lobes of the exopods) to which the eggs and of one or two segments, or reduced to are attached. The external openings of the small vestiges, or in some cases enlarged; male and female genital ducts are at the base male antennules very often are modified as of the 11th pair of trunk limbs, and caudal clasping structures with a large grappling rami and spines (Fig. 3A) occur in all species. spine (but only slightly so in the Macrothri­ cidae and Chydoridae). The antennae are well Anomopoda developed, biramous, and natatory, with The Anomopoda (Figs. 4, 5) contains the three or four segments per ramus and often five families that are perhaps most often con­ with plumose setae on all segments, although sidered "typical" cladocerans: Daphniidae it is common to have one or more segments (six genera), Bosminidae (two genera), Chy- without setae. The mandibles are stout and of doridae (over 30 genera), Macrothricidae (ap­ the rolling/grinding type. The maxillules are proximately 16 genera), and Moinidae (two reduced and bear four or fewer spines. The genera). They are small, from less than 0.3 maxillae are reduced to small, nonsetose pro­ mm to perhaps 6 mm in adult females (all trusions, or are absent. The trunk limbs dis­ display sexual dimorphism, with smaller play none of the serial similarity seen in the males). The group includes one of the small­ more "phyllopodous" branchiopods (the est known (the chydorid Alonella above-mentioned tax a), and are fewer in nana, with an adult female maximum length number, usually numbering only five or six. of 0.26 mm; Fryer, 1968). All inhabit fresh These limbs are widely diverse in form and water, with a few exceptions in inland saline function in the various taxa. All have an epi- bodies for some bosminids and daphniids. pod, but the first trunk limbs bear unique Habits are extremely diverse, and include "ejector hooks," and they lack a true gna­ benthic, planktonic, interstitial, moist terres­ thobase basally. The trunk limbs (see Watts trial (rainforest leaf litter and mosses, e.g., and Petri, 1981) perform functions as diverse Frey, 1980), and even cave (Brancelj, 1990) as grasping, scraping, mechanically transfer­ environments. Most feed by filtration or ring food particles, and filtration, or some scraping, or by some combination of these combination of these duties, although the first modes, but others are scavengers on other and sixth (when present) are never filtratory, crustaceans {Pseudochydorus) and one genus and the limbs never beat in a metachronal (Anchistropus) is ectoparasitic on freshwater rhythm. The first is most often used in loco­ hydras (see Fryer, 1968). motion. The food groove tends to be deep and

BRANCHIOPODA 37 hs

Fig. 5. External morphology of Anomopoda, families Chy­ female of a burrowing species, Drepanothrix dentata. E: Ven­ doridae and Macrothricidae. A,B: Chydoridae. (After Fryer, tral view oi Acantholeberis curvirostris. F: A mud-frequenting 1968.) A: Ventral view of the •ycj.venger Pseudochydorus globo- burrower, llyocryptus sordidus. Not to scale, al, first antenna; sus. B: Anterior view oi Pseudochydorus globosus in "closed" a2, second antenna; c, carapace; ce, compound eye; hs, head position. C-F: Macrothricidae. (After Fryer, 1974.) C: Ante­ shield; ne, nauplius eye; pas, postabdominal setae. rior view of the primitive Acantholeberis curvirostris. D: Adult

Fig. 4. External morphology of the Anomopoda. A,B: Lateral Alonella exigua. G: Ventral view of Alonella exigua gliding (A) and ventral (B) views of an open water species, Daphnia over substrate. H: Lateral view of Peracantha truncata. I: galeata (Daphniidae). (After Fryer, 1991a.) C-I: Family Chy­ Oblique anterior view oi Peracantha truncata. Not to scale, al, doridae. (After Fryer, 1968.) C: Dorsal view of a gliding gas­ first antenna; a2, second antenna; ce, compound eye; hs, head tropodlike species, Graptolebris testudinaria. D: Posterior view shield; la, labrum; ne, nauplius eye; pas, postabdominal setae of Graptolebris testudinaria. E: Ventral view of Graptolebris (= telsonal filaments). testudinaria as animal glides over substrate. F: Dorsal view of 38 MARTIN narrow. There are never any postgenital lacks a functional gnathobase, whereas limbs limbs, and the telson or postabdomen termi­ one through five have a gnathobase that func­ nates in a pair of strong terminal "claws" tions in transferring food toward the mouth. (caudal rami) and bears a pair of dorsal sen­ The first trunk limb lacks the basal "ejector sory "telsonal filaments" or "postabdominal hooks" known in anomopods, and in males setae" (Figs. 4A-C,E-G, 5D~F). The telson often bears distal hooks or other modifica­ is usually bent under, so that its ventral sur­ tions for grasping. "Respiratory" epipods are face is functionally dorsal, and it may articu­ present (although not on all limbs of Holope­ late with the trunk. dium), and the limbs beat with an obvious metachronal rhythm and are never used for Ctenopoda grasping, scraping, or locomotion. The food The Ctenopoda (Fig. 6A,B) contains only groove between the limbs is deep and narrow. two families, Sididae (seven genera) and Hol- The telson, which bears caudal rami and a opediidae (one genus, Holopedium). All are pair of postabdominal setae, does not articu­ small (to about 4 mm) microphagous filter late with the trunk as in anomopods. feeders that are found mostly in open water, although they also may be benthic or associ­ Onychopoda ated with vegetation (Fryer, 1987a-c). All are Onychopods (Fig. 6C,D) are freshwater in except for , which is and marine predators variously modified for marine. grasping prey, although some may ingest par­ Ctenopods at first glance appear rather ticulate detritai matter (Fryer, i987a,b). They similar to anomopods, and indeed Fryer may reach 12 mm in length, but this measure­ (1987a~-c) discussed some deep-seated simi­ ment includes an extremely long caudal pro­ larities between the two orders. Like anomo­ cess found in some taxa (e.g., see Fig. 6C); pods, the body is short, somite boundaries are most are 2-6 mm. There are three families: obscured by fusion, and the trunk is enclosed Polyphemidae (one genus, Polyphemus), in a bivalved, hingeless carapace. But the Cercopagidae (two genera), and Podonidae head, although short and extending beyond (six or seven genera) (Mordukhai-Boltovskoi the valves of the carapace, differs from the andRivier, 1987). anomopod condition in that there is never a Onychopods have a short head and trunk, headshield (Fig. 6A,B). The compound eye is the segments of which have become obscured single and internal, with no sign of having by extensive fusion. The carapace has been become "internalized" during ontogeny. The reduced to a dorsal brood pouch (Fig. 6C,D). labrum is large and rather fleshy. The anten- The single, median eye is composed of many nules are tubular in females and are large and ommatidia, of several different structural modified for grasping in males. The antennae types in some taxa (e.g., 130 ommatidia of are biramous and natatory (secondarily four types in Polyphemus), and occupies uniramous in females of Holopedium, Fryer, nearly all of the head region, but there is no 1987a,b), with endopod and exopod each of external indication of facets. The labrum is two or three segments bearing natatory setae. large and bears secretory glands. The anten- The mandibles are of the grinding/rolling nules are uniramous and more or less tubular, type. Maxillules are small and spinose, and varying in length among taxa. The antennae the maxillae are reduced to small lobes that are biramous and natatory, with a three-seg­ may or may not bear setae. There are six pairs mented endopod and four-segmented exopod of trunk limbs, all of which are pregenital and each bearing plumose natatory setae. The display serial similarity, although the last pair mandibles are modified versions of the is always reduced and is not filtratory, which grinding/rolling type and allow biting. The the others are. Additionally, the sixth limb maxillules are reduced, and the maxillae ap- BRANCHIOPODA 39

Fig. 6. The orders Ctenopoda, Onychopoda, and Haplopoda. . (After Belk, 1982.) E: Sole member of A: Latonopsis serricauda (Ctenopoda), ventral view. (After the order Haplopoda, the predatory kindtii. al, first Sars, 1901.) B: Lateral view of Latonopsis serricauda. (After antenna; a2, second antenna; bp, brood pouch formed by modi­ Sars, 1901.) C: The onychopod Bythotrephes cederstroemi, a fied carapace; h, heart; pas, postabdominal setae. species with an extremely long abdomen. D: The onychopod 40 MARTIN parently have been lost. The trunk is short, pouch that appears to be situated near the pos­ and segmentation is obscured; however, all terior extremity of the thoracic region; in species have four pairs of "thoracic" (pregen- males the carapace is absent. The antennule is ital) limbs, and so at least primitively the uniramous, and is short in females but long trunk may have been composed of four (modified for grasping) in males. The antenna somites. The trunk limbs (Fig. 6C,D) are ste- is biramous, large, and natatory in both sexes. nopodous, segmented, grasping appendages Both the exopod and endopod of the antenna with exopods and small gnathobases but with­ are four-segmented, with each segment bear­ out an inflated epipod. Despite the presence ing numerous natatory (plumose) setae. The of small (but presumably functional) gna­ labmm is short and broad. The mandibles are thobases, there is no true food groove. In styliform, not grinding, and are thus unique males, the first trunk limb is sometimes mod­ among the Branchiopoda. Both maxillules ified for grasping the female, and paired ex­ and maxillae are absent. The thoracic region ternal penes are occasionally found just poste­ (the actual limits of the thorax are uncertain) rior to the base of the last trunk limb. The has undergone extensive fusion; somite bound­ form of the abdomen varies among taxa. It aries are indistinct. The six appendages of the may be short and unsegmented, or long and thorax are grasping appendages, all of which revealing some indication of former somite lack exopods and branchial epipods. Only the boundaries. The telson may terminate in "typ­ first bears a modified coxal lobe (gna- ical" cladoceran caudal rami, or the postabdo- thobase), which is rather reduced, and there is men may be produced into a long, thin caudal no food groove. The abdomen is long, slen­ process, possibly derived from a fusion of der, and cylindrical. Segmentation is more or furcal elements (e.g.. Fig. 6C). less clear; there are three rather long seg­ ments, the last of which has been termed a Haplopoda telson with caudal rami, but these do not artic­ The order Haplopoda has long been recog­ ulate with the somite as do "true" caudal rami nized as being very different from all other as seen in ctenopods, anomopods, spinicau- "cladocerans" and, even before the rearrange­ datans, etc. There are no paired telsonal fila­ ment of the Branchiopoda suggested by Fryer ments or setae. The cuticle is exceedingly thin (1987c), was treated apart from ctenopods, and transparent, and in water Leptodora is anomopods, and (less frequently) onychopods. nearly invisible to the naked eye. The order contains a single family, Leptodor- idae, with a single species, Leptodora kindtii (Fig. 6E), a nearly transparent predator on INTEGUMENT freshwater in holarctic lakes. Fe­ The branchiopod cuticle is built along the males may reach 18 mm, whereas males do same lines as for most crastaceans, i.e., it not exceed 9 mm. Leptodora is a highly spe­ consists of a thin outer epicuticle composed cialized predator, as are members of the Ony- mostly of protein, lipids, and calcium salts chopoda, and many if not all of its unusual (mostly in higher crastaceans) and an internal features can be seen as adaptations to its pred­ procuticle, usually recognized as being com­ atory life style. posed of an outer preecdysial procuticle (or The head is long, narrow, and cylindrical; exocuticle) and beneath it a postecdysial probably as a consequence the compound eye procuticle (or endocuticle) (see Stevenson, is a single, median structure that completely 1985, fig. 1). The procuticle is much thicker fills the anterior of the head and is composed than the epicuticle and is composed of layers of "about 500 specialized radially arranged of fibrous lamellae parallel to the surface; of­ ommatidia" (Fryer, 1987c), but there are no ten the two component layers of the procuticle external indications of facets. The carapace are themselves divided into sublayers. How­ has been reduced in females to a dorsal brood ever, the cuticle is typically very thin in bran- BRANCHIOPODA 41 chiopods, with no calcification of the exocuti- The epicuticle is thicker on the outer cara­ cle and with little sclerotization. Cuticle pace surface, usually about 1.6 |xm, com­ covering the thoracic epipods in Daphnia may pared to about 0.5 \x.m on the inner surface. It be only 0.2-0.5 |xm thick (Peters, 1987). In is composed of three layers (four in Triops; larval Anemia, where embryonic develop­ see Rieder, 1972b) and has a layer of material ment and proliferation of epidermal cells has loosely attached to its surface (Fig. 7B). The been the subject of several excellent papers by procuticle is not readily subdivided into an Freeman (1986, 1988, 1989), the cuticle may obvious exo- and endocuticle, possibly be­ be as thin as 0.3-1.0 jxm (Freeman, 1989), cause there is a greater similarity between pre- and the inner "procuticle" has not yet differ­ and postexuvial synthetic mechanisms than is entiated into an exo- and endocuticle. In seen in higher crustaceans such as decapods. adults the thickness of the cuticle varies ac­ The procuticle at times appears distinctly cording to functional requirements; it is of lamellate (e.g.. Fig. 7B) and at other times course extremely thin on presumed respira­ relatively homogeneous in its electron density tory structures (epipods; see below) and flex­ (Figs. 7C, 8A); Halcrow (1976) interprets this ure zones and thickest on areas that undergo variability as nothing more than an artifact of heavy use, such as the masticatory surfaces of the angle or thickness of the section. The the mandible and on male claspers. In the procuticle is traversed incompletely by thin, male anostracan "clasper" (the antenna), the rod-shaped structures (approximately 15-36 cuticle may be 7 |xm thick, whereas in the nm diameter) that appear to extend from the anostracan trunk and thoracopods it is often underlying epithelium into the procuticle only 1-1.5 \x.m (Criel, 1991a). It is possible (Fig. 7B,C). These rods are associated with that in regions where gas exchange is impor­ invaginations of the apical plasma membrane tant all layers are not present. Criel (1991a) (conical hemidesmosomes; Halcrow, 1976) points out that no endocuticle is visible in of the epidermal cells (Fig. 7B,C). Copeland's (1967, fig. 4) figure of the During the intermolt period, the epidermal (thoracopodal epipod) cuticle, and apparently cells are squamous and appear narrow in cross the epicuticle is absent in some areas of the section. Golgi bodies and mitochondria are Daphnia integument (Schultz, 1977; Schultz present, and the nucleus is disc-shaped. The and Kennedy, 1977; Stevenson, 1985). endoplasmic reticulum is loosely organized, The following account is based primarily and ribosomes "lie freely in the cytoplasmic on Halcrow's (1976) study on the integument matrix" (Halcrow, 1976: 2). Large numbers of the anomopod , which has of microtubules are present and pass ob­ a relatively simple integument. Daphnia, be­ liquely through the cytoplasm to the apical cause it is a bivalved animal, has the carapace region, where they become associated with folded back on itself in the region of the invaginations of the plasma membrane. These valves, much as in the branchiostegal region invaginations are lined by electron-dense ma­ of decapods (see also Fig. 68D for both sides terial, and each contains the base of a rod (see of the valves in a conchostracan). Thus, a above) that extends into the overlying procuti­ section through the carapace in this region cle. Below each invagination are microtu­ shows integument facing the inner (facing the bules and granular (microfibrillar) material animal) and outer (facing externally) sur­ associated with invaginations in other planes. faces, with a thin hemocoelic space sand­ In cross section, these invaginations appear to wiched between them (Fig. 7 A). The two lay­ occur in clusters. The plasma membrane of ers of cuticle are connected by "pillars" of the lateral cell border is highly convoluted, connective tissue that extend through the and septate junctions occur along the apical hemocoelic space and probably serve as sup­ regions of the lateral borders. Halcrow (1976) port (Anderson, 1933). noted similarities with the apical regions of 42 MARTIN

Mt

Mt

t\ 'V-

Fig. 7. Integument of carapace valves of Daphnia magna. C: Detail of outer integument layer. x44,500. Apm, apical (From Halcrow, 1976.) A: Inner and outer integument layers of plasma membrane; Dcv, dense core vesicles; H, hemocoel; Icf, carapace with hemocoel between, x 24,400. B: Outer integu­ intracuticular fibers; M, mitochondrion; Mt, microtubules; Pci, ment layer. Note detached outermost layer of epicuticle (arrow) procuticle of inner layer; Pco, procuticle of outer layer; Pmi, and portions of intracuticular fibers within procuticle. x25,500. invagination of apical plasma membrane. BRANCHIOPODA 43

-^y-^

Fig. 8. Integument of Daphnia magna. (From Halcrow, 1976.) A: Inner integument layer showing granules (G) in narrow exuvial space between new and old cuticle. x47,500. B: Outer integument showing inclusion (Inc). x20.000. C: Outer layer epidermal cell. Note proximity of inclusion to Golgi complexes. x35,500. Apm, apical plasma membrane; Ep, epicuticle; Go, Golgi apparatus; H, hemocoel; N, nucleus; Pen, new procuticle; Pco, procuticle of outer layer. 44 MARTIN cells in the midgut diverticulum of Daphnia For example, cuticle of the Artemia trunk re­ (Hudspeth and Revel, 1971). Golgi bodies gion (Fig. 9) is basically similar to the above pinching off dense core vesicles (each about description (Criel, 1991a). However, special­ 110 nm in diameter) are seen. These vesicles izations of the integumental epithelium exist are similar to others near the apical cell border in certain appendages and organs treated else­ and to vesicles in tissue fixed immediately where. Specialized cells of the epithelium of after ecdysis. Coated vesicles of approxi­ the thoracic epipods are described in the sec­ mately 140 nm diameter, usually seen in ani­ tion on respiration, and cells comprising the mals that are halfway through premolt (Fig. dorsal organ are described later in this sec­ 8A), are sometimes seen in just-molted ani­ tion. mals as well. The basement membrane sepa­ A study of the integument of two spinicau- rating these cells from the hemocoel is about datan conchostracans revealed a cuticle (Figs. 0.2 \im thick (Fig. 8C). 10A,B, 11 A) that in most parts of the body is During the premolt period, epithelial cells similar to that of Daphnia and Artemia are surprisingly much the same as during the (Rieder et al., 1984). However, in these taxa intermolt period. The newly forming epicuti- (Leptestheria dahalucensis and Limnadia len- cle is visible (Fig. 8A), interrupted in places ticularis) the cuticle of the carapace is not by the intercuticular fibers extending into the shed with each molt, accounting for the procuticle, and an ecdysial space filled with growth lines present on spinicaudatans (Fig. amorphous matter, suggested by Halcrow lOA). Consequently, the number of layers of (1976) to be the results of enzymatic digestion cuticle seen in a cross section of the valves of the endocuticle, is evident (Fig. 8B). How­ reveals the number of molts, and the dorsal ever, in the epithelial cells the only obvious region of the valves can become quite thick changes are in the more abundant granular with accumulated layers of unshed integu­ endoplasmic reticulum, increased cell height, ment (Figs. lOA, IIB). Rieder et al. (1984) abundance of glycogen, and presence of ir­ also described "ribs" of cuticle on several regularly shaped inclusions near Golgi bod­ parts of the spinicaudatan body, attributing ies, both seen later in the premolt period (Fig. the formation of these ribs to small exocuticu- 8A-C). Apart from the inclusions seen in pre­ lar granules that swell and eventually extrude molt cells (Fig. 8B,C), no cytoplasmic struc­ the epicuticle and outermost layers of the tures involved in cuticle synthesis were seen exocuticle. A similar thickening of the cuti­ to be restricted to any specific period during cle, including layers like those seen in spini­ the molt cycle, and fusion of the vesicles with caudatan clam shrimp, occurs in the forma­ the apical plasma membrane occurred before tion of the ephippium of anomopods (see and after premolt initiation. These changes Schultz, 1977). are of less magnitude than those seen in many Pore canals extending through the integu­ higher crustaceans, where there is a distinct ment are not seen in Daphnia (Halcrow, decline in activity and structural organization 1976) or spinicaudatans (Rieder et al., 1984) when synthesis of the new cuticle is complete. but are present, although uncommon, in Tri- This might be because the intermolt period in ops (Rieder, 1972b), which has a slightly daphniids is so short (Halcrow, 1976). Thus thicker cuticle (approximately 12 \x.m thick). the mechanism for synthesis of new cuticle is Possibly there is no need for such cytoplasmic a more continuous process. No microvilli extensions in crustaceans where the cuticle is were seen in Daphnia epithelial cells during as thin as in Daphnia (Halcrow, 1976). formation of the new epicuticle. Rieder's (1972a,b) account of the cuticle of The above synopsis can probably be ex­ the notostracan Triops dealt mostly with the tended to other parts of the body in Daphnia, layers of the cuticle itself rather than with the and possibly to other branchiopods as well. epithelial cells. In this predominantly benthic BRANCHIOPODA 45

Fig. 9. Integument of trunk region of adult Artew/a (Anostraca). EC, epidermal cell; en, endocuticle; ep, thin, three-layered epicuticle; ex, exocuticle with thin homogeneous outer layer (arrow) and broad laminated inner layer. Scale bar = 200 nm. (Courtesy of G. Criel.) order, which might be expected to require a Integumental Glands more durable and yet more flexible carapace Knowledge of integumentary glands is than in some of the mostly planktonic or fragmentary and is restricted to anostracans open-water orders, the epicuticle consists of and notostracans. In the Anostraca, Dornesco four layers, the exocuticle consists of up to and Steopoe (1958) found proximal thora- ten layers, and the endocuticle may be com­ copodal glands consisting of one large and posed of up to 80 layers (Figs. 12-14), the two small gland cells linked to the outside by most known in any branchiopod. a short duct of three to four cells; the duct All branchiopods contain in the cuti­ opens at the base of a spine on the protoendite cle. The various pathways for chitin synthesis in Branchipus and Artemia. These poorly in Artemia were reviewed by Horst (1989). known structures are treated in the section on The most likely scenario is that the chitopro- glands. Rieder (1977) described well-devel­ tein is synthesized in the rough endoplasmic oped integumental glands in notostracans that reticulum (RER), then moves to the Golgi consist of three cell types, a rather large secre­ apparatus (where Horst presumes that chitin tory cell, a collarlike intermediate cell, and synthetase is located), where it serves as a duct cells extending up through the epidermis "primer" molecule for chitin synthetase, (Fig. 15). Rieder (1977) suggested that these yielding a chitin-protein complex. The glands function in the secretion of the epicuti­ chitin-protein complex must somehow be cle, but Stevenson (1985) doubted this be­ transported to the apical membrane and ex­ cause of the inadequate number and distribu­ ported to be incorporated into the cuticle, but tion of these glands and because other studies the mechanism is unknown. (e.g., Neville, 1975) indicated epidermal se- MARTIN

Fig. 10. Integument of the spinicaudatan Leptestheria dahalacensis. (From Rieder et al., 1984.) A: Posterior end of valves showing accumulated layers of cuticle retained after ecdysis (forming "growth lines" on the carapace). x43. B: New cuticle, consisting at this stage of only the epicuticle and upper layer of the exocuticle, replacing old at edge of carapace, x 32,000. aC, old cuticle; Ep, epicuticle; En, endocuticle; Ex, exocuticle; nC, new cuticle. BRANCHIOPODA

Fig. 11. Integument of the spinicaudatan Le/jf^jf^en'fl t^o^aiflcenjw. (FromRiederet al., 1984.) A: Newly forming cuticular ribs (nR) visible under ribs (R) of older carapace. X4,800. B,C: Examples of accumulated layers of old cuticle (not shed during ecdysis). B, x 12,000; C, x 13,600. 48 MARTIN

,jD,5iJm^ ? .^

Fig. 12. Integument of Tn'op.? cancn/or/nw (Notostraca). (FromRieder, 1972b.) A: Wedge-shaped "molt­ ing suture." B: Exocuticle (Ex) and endocuticle (En), distinguished by density and contrast. C: Laminations of the exo- and endocuticle. Ep, old epicuticle; Epn, newly formed epicuticle; Eu, exuvial chamber between old and new integument layers; Ex, newly formed cuticle; S, secretory droplets; small arrow, rare archlike structure.