Ings for Leptestheria Dahalacensis. Even More Curious Is the Fact That
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BRANCHIOPODA 151 Fig. 93. Peripheral cytoplasm of nurse cell of vitellogenic oocyte in Leptestheria dahalacensis (Spinicau- data). (From Zeni and Zaffagnini, 1989.) Scale bar — 0.5 \i.m. BM, basal membrane of follicle; FC, follicle cell; G|, immature protein yolk globule; IG, intracistemal granules. ings for Leptestheria dahalacensis. Even in the Laevicaudata, where attempts to locate more curious is the fact that, according to the female genital opening have failed (Mar these same authors, the egg envelope is cre tin et al., 1986), and is reminiscent of the role ated by exocytosis of the egg itself, rather of the notostracan female 11th trunk limb. than by secretions of oviducal cells (Notos- Oogenesis in the major cladoceran orders traca) or shell glands (Anostraca), and this is was reviewed by Rossi (1980) and Zaffagnini the only egg membrane present throughout (1987, for Daphnia). It is a complex process, development. If so, then these two genera complicated further by the fact that there are differ even from other spinicaudatans (see cytological differences between comparable Belk, 1987; Zeni and Zaffagnini, 1989). Fi organs, depending upon whether reproduc nally, the eggs are coated with mucus pro tion is parthenogenetic or amphigonic (sex duced by ovarian mucous glands (also ual), and space does not allow a detailed re unique) and then pass into the dilated epipod view here. Resulting eggs may be of two (Figs. 94B, 95) of several posterior thoracic different types, also depending on mode of appendages, from which they are later dis reproduction, with thicker shelled "resting" charged through a distal medial slit on the eggs produced by ephippial females as a result epipod, to adhere via their mucus coating to of sexual reproduction (Zaffagnini, 1987). the mother's body wall (Tommasini and The germarium is at the anterior end of the Scanabissi Sabelli, 1989; Scanabissi Sabelli ovary in the Sididae (Ctenopoda), but at the and Tommasini, 1990a). This use of selected posterior end in the Anomopoda, Ony- thoracic epipods to store and transfer eggs to chopoda, and Haplopoda. Ovaries and brood the lateral external body wall may also occur chamber are confined to the thorax, except for 152 MARTIN B ^" loop Fig. 94. Oviduct and egg formation in Leptestheria dahalacensis (Spinicaudata). (From Tommasini and Scanabissi Sabelli, 1989.) A: Semithin section of oviducal sac showing eggs (E), egg envelopes (arrows), and mucus (m). B: Longitudinal section showing eggs as they enter base of thoracic limb epipods (ep). E, egg; mt, midgut; O, ovary. Leptodora, where they are abdominal. Oo all cladoceran orders possess yolk in the genesis proceeds in "waves" (Rossi, 1980), oocytes, the nature of the yolk differs in allowing simultaneous development of eggs Leptodora, further supporting the separation at several different stages, but direction of the of haplopods from other cladocerans. wave (i.e., longitudinal or lateral) differs be tween anomopods (in which oogenetic waves Resting Eggs arise laterally) and all other taxa (Rossi, Many branchiopods produce some form of 1980). Rossi (1980) also noted that, although resting eggs (or cysts), although the method BRANCHIOPODA 153 Fig. 95. Use of thoracic limb epipods for egg storage/transfer left by egg and residual mucus (m). C: Recently laid eggs in Leptestheria dahalacensis (A-D) and eggs of Eoleptestheria adhering to epipods (ep) via mucus (m).D: Egg mass on lateral ticinensis (E-G) (Spinicaudata). (From Tommasini and Scan- surface of female's trunk. E: Egg with mucous layer (m) torn. abissi Sabelli, 1989.) A: Epipods (ep) during laying of eggs. F: Mucous layer (m) and vitelline envelope (ve) surrounding Note enlargement (arrow) where egg is issuing from epipod. B: egg (E). G: Detail of F showing vitelline envelope (ve) and Opening on interior distal surface of epipod showing opening mucous layer (m). of formation of these eggs varies among taxa (Bishop, 1968; Belk, 1970). Resting eggs of (see above). Although often assumed to play a Artemia do not engage in detectable metabo role in enabling the embryo to withstand des lism and contain less than 1 % water by weight iccation, the thick external shell (Figs. 96-98) (Kasturi et al., 1990). Notostracan resting plays a more important role in protection eggs can survive temperatures up to within against physical damage and sunlight 1°C of boiling, and in some populations of 154 MARTIN Fig. 96. Trilaminate structure of the egg in No tostraca and Spinicaudata. A: Diagram of Triops cancriformis egg membranes, showing newly formed unstratified eggshell (a), formation of the inner layer (b), and construction of the final egg shell (c). (After Tommasini et al., 1989.) B: Trans verse section through two eggs of Triops granarius, showing cryptobiotic embryo (ec) and alveolar na ture of tertiary envelope (ca). (From Thiery, 1985.) Scale bar = 100 \ym. C: Section through dehy drated egg of Eulimnadia antlei (Spinicaudata). (After Belk, 1987.) Black embryonic mass (EM) approximately 0.1 mm across at greatest width. EC], embryonic cuticle 1; TE, tertiary envelope. Triops (Notostraca) and Streptocephalus leptestheriid conchostracans (see above and (Anostraca) high temperatures are required to also Belk, 1987). interrupt diapause (Carlisle, 1968). In many The dormant resting egg usually consists of taxa (e.g., Notostraca, Laevicaudata, and a thick, external, outer shell, termed a tertiary most Spinicaudata), production of resting envelope, and one or two inner chitin-con- eggs is the only mode of reproduction, taining embryonic cuticles formed by ecdysis whereas in others (e.g., Haplopoda, many of the growing embryo after the tertiary enve Anomopoda, Cyclestheria among the spini- lope has formed (Mawson and Yonge, 1938; caudatans, etc.) resting eggs are but one op Weisz, 1947; Under, 1960; Morris and Af- tion. The final (tertiary) eggshell is produced zelius, 1967; Anderson et al., 1970; Garreau by distinct shell glands in anostracans, by de Loubresse, 1974; Gilchrist, 1978; Belk, cells of the follicular duct in notostracans and 1987, for Anostraca; Thiery, 1985; Tommas at least some limnadiid spinicaudatans, and ini et al., 1989, for Notostraca; Zaffagnini by exocytosis of the oocyte itself in some and Minelli, 1970; Belk, 1987, for Spinicau- BRANCHIOPODA 155 i 10 /ur Fig. 97. Details of the dehydrated cyst of Streptocephalus window section of c.l. AL, a.l., alveolar layer; As, covering of dichotomus (Anostraca). (From De Walsche et al., 1991.) A: alveolar layer; CL, c.l., cortical layer; e L- , embryonic cuticle; Cross section through entire cyst. B,C: Details of cyst outer EMBC, emb.c, embryonic cells; icm, internal cuticular mem wall. Numbered arrows designate: 1, upturned section of inter brane; p.m., peripheral membrane; s.m., spongy mass at foot of nal layer (i.l.); 2, "curtains" of cortical layer (c.l.); 3, thin AL. window-like sections of c.l.; 4, externally visible "spokes" of data). The tertiary envelope is composed of (Fig. 96C), the first one (ECl) inelastic and three layers, termed simply inner, outer, and the second (EC2) elastic with outpocketings alveolar (e.g., Tommasini et al., 1989, for over the developing antennae (termed the "cu Notostraca; Fig. 96A), and these layers are ticular membrane" and "hatching membrane" formed around the notostracan oocyte by red in notostracans by Tommasini et al., 1989). dish fluid secreted by the follicular tubule Formation of the two cuticles, which are cells (Trentini and Sabelli Scanabissi, 1982). fused in the caudal region of the developing Belk (1987) demonstrated that in the Spini- embryo in Artemia (but not in spinicauda- caudata and in some (but not all) anostracans tans), is separated by a period of embryonic there are two embryonic cuticles produced growth (Belk, 1987). The two embryonic cu- 156 MARTIN Fig. 98. Layers of the eggshell in Triops cancriformis (Noto- cuticle. I: Embryonated egg showing alveolar and inner layers straca). (From Tommasini et al., 1989.) A: Single-layered egg and hatching membrane. J: Final form of the egg and its layers shell. B: Formation of the inner layer. C,D: Eggshell surface after hatching of larva, al, alveolar layer; ec, embryonic cuticle; showing craters. E: Cross section showing increased thickness hm, hatching membrane; il, inner layer; ol, outer layer; white after formation of alveolar layer. F: Pores in final stage of arrow in H, alveolar pore; white arrow in I, embryonic cuticle. eggshell. G,H: Cross sections of the three layers and embryonic tides differ slightly structurally and chemi space within the tertiary envelope in the Spi- cally (Garreau de Loubresse, 1974). When nicaudata (Bishop, 1968; Belk, 1987), Notos- the resting egg is dry, the embryo itself is a traca (Thiery, 1985), and Artemia (Belk, cuplike mass occupying less than half of the 1987) (Figs. 96B,C, 97A). Hatching involves BRANCHIOPODA 157 shedding of the tertiary envelope, rupture of of the carapace, and the number of eggs has EC 1, and finally rupture of the elastic EC2 to stabilized at one (advanced chydorids) or two release the nauplius (Belk, 1987; Tommasini (daphniids) per ephippium (Fryer, 1972, etal., 1989). 1987c; Fryer and Frey, 1981). The ephippium Resting eggs so produced may be of many is often modified, with additional structural different shapes (Fig. 99), and are often used components such as a strengthened dorsal in taxonomic distinctions. In the Notostraca ridge or other ornamentation, and in some (e.g., Gilchrist, 1978; Alonso and Alcaraz, macrothricid species bears long fdaments, ac 1984; Thiery, 1985; Tommasini et al., 1989) tually remnants of the original carapace bor and Laevicaudata (Martin and Beik, 1989), der, that now aid in entangling the ephippium resting eggs are rather unremarkable, being among vegetation (Fig. lOOC) (Fryer, 1972; spherical and with little external ornamenta Fryer and Frey, 1981). Ephippia are secreted tion (Figs. 98J, 99E). In the Anostraca, there while the amphigonic (resting) eggs are grow is a seemingly endless variety of resting egg ing in the ovary (Zaffagnini, 1987).