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FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1987 University of Washington Press. This manuscript is an author version with the final publication available and may be cited as: McEuen, F. S. (1987). Phylum Echinodermata, class Holothuroidea. In M. F. Strathmann (Ed.), Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae (pp. 574-596). Seattle, WA: University of Washington Press. ... McEuen, F. S. 1987. Pp . 574-596, in: Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast. Data and Methods f~r the Study of E~~ Embryos, and Larvae. M. Strath­ mann, ed. Univ. of Washing~n Press, Seattle. 670 pp. PHYLUM ECHINODERMATA, CLASS HOLOTHUROIDEA F. S. McEuen Chapter advisors: Richard R. Strathrnann, Scott T. Smiley. and Lane Cameron INTRODUCTION High primary production, constant tidal flushing, and habitat diversity all help to support a large number of sea cucumber species in the San Juan Archipelago. At least twelve species representing four of the six orders of holothuroids (Dendrochirotida, Aspidochirotida, Apodida, and Molpadiida) occur in relatively high densities within diving range (30 m) in this region. The majority of local sea cucumbers have separate sexes , broadcast their gametes, and produce a non-feeding, planktonic larva. Most free-spawning species reproduce from late winter to late spring and brooding species spawn in late fall and early winter. The more recent comprehensive reviews of holothuroid reproduction and development are by Hyman (1955), Inaba (1968), Boolootian (1966), and Smiley et al. (in press). Studies of larval forms and behavior of northeast Pacific holothuroids have been made by Mortensen (1921) , Johnson (1931), Johnson & Johnson (1950), Strathmann (1971), Young & Chia (1982), McEuen & Chia (1985 and in press), Cameron (1985), McEuen (1986) and Smiley (1986a,b). REPRODUCTION AND DEVELOPMENT Hermaphroditism is relatively common among small apodids but is rare in other holothuroid groups where separate sexes are the rule. Sexes can be externally distinguished in species which have (1) a thin body wall through which the color of ripe gonads shows, (2) females with incubatory behavior or brood pouches, or (3) morphological differences of the genital papilla. Sea cucumbers possess a single gonad composed of one or two tufts of long, slen­ der tubules, sometimes branched, radiating from a gonad basis. Gonadal walls have an inner epithelium of parietal and follicular epithelial cells, a central connective tissue layer and genital hemal sinus, and an outer peritoneum of epithelial cells, axons, and muscle cells (Smiley & Cloney 1985). Oocytes, surrounded by follicle cells, are connected by a follicular stalk to the inner epithelium. Full-grown oocytes in meiotic prophase I are ovulated into the gonadal lumen where they undergo germinal vesicle breakdown (GVBD) before or during spawning. The specific environmental factors entraining holothuroid gametogenic cycles still remain to be determined. Periods of no feeding and autumn or 574 4 HOWTIlUROIDEA 575 winter torpor are probably connected with gonad and oocyte nutrition and development. Kanatani (1979) summarized work on endocrine substances affecting oocyte maturation and gamete shedding. Follicle cells are stimulated by a peptide in radial nerve factor to produce a secondary factor that induces resumption of meiosis (maturation of the oocyte through GVBD) (Maruyama 1985). Hormonal substances regulating holothuroid reproductive behavior and gamete release remain unknown. To aid mixing and dispersal of gametes, sea cucumbers may lift the anterior end, wave their tentacles, sway from side to side, or forcefully expel the eggs and sperm (McEuen 1986 and in prep .). Free-spawning species have one or more gonopores on a genital papilla positioned dorsally in the tentacle crown or as far as 2-3 cm behind the tentacles on the dorsal surface. Male dendrochirotids typically possess a number of gonopores. Sperm of the primitive type are characteristic of almost all species of holothuroids (Chia et al. 1975), including local species (Everingham 1961; Brooks 1973 ; Atwood 1974a,b, 1975a,b; Chia et al. 1975; Chia & Bickell 1983; Fontaine & Lambert 1976; McEuen & Chia 1985 and in press ; McEuen 1986), with the exception of Cucumaria Iubrica and C. pseudocurata. The spermatozoon of C. Iubrica is fusiform (elongate and cylindrical) (Atwood & Chi a 1974; Atwood 1975a) and that of C. pseudocurata is tabloid in shape (elongate and dorsoventrally compressed) (Atwood 1975a,b). The acrosome of the latter is situated medially on the ventral surface. Species-specific chemoattraction of sperm to egg extracts is evident for some sea cucumbers, but is generally lacking among the Dendrochirotida (Miller 1981, 1985). Eggs of holothuroids are probably spawned at first meiotic metaphase (Holland 1981) and are enclosed in a thick jelly coat. Fertilization is assumed to occur after GVBD and before polar body extrusion. Sperm contact with the egg jelly layer sets off an acrosome reaction, sending an acrosomal tubule through the envelope of jelly to fuse with a fertilization cone (Colwin & Col­ win 1955; Colwin & Colwin 1955, 1956; Colwin et al. 1975). Fusion of sperm and egg membranes begins the cortical reaction, and a fertilization envelope is subsequently formed. No hyaline layer is produced within the perivitelline space (Holland 1981); the low fertilization envelope is consequently difficult to see with light microscopy. Polar bodies are then extruded through the oocyte protuberance (formerly "micropyle appendage", Smiley & Cloney 1985) and may be quickly lost or may be present through the blastula stage. Unfertilized naturally spawned eggs of Psolus chitonoides can form polar bodies (McEuen unpubl.). Pelagic planktotrophic development. Relatively small (185-210 urn in diameter) eggs are broadcast during mass spawnings in late spring and early summer. A feeding larva develops in the plankton. The only local species with this type of development is Parastichopus californicus. In this type of development, spawned eggs are negatively buoyant and develop into a coeloblastula through radial, equal holoblastic cleavage. The wall of the coeloblastula at the vegetal pole thickens, then flattens into a gastral .- ... 576 F. S. McEUEN plate. Gastrulation begins by invagination of the gastral plate and subsequent­ ly produces an archenteron one-half to two-thirds the length of the embryo. Within the blastocoel, mesenchyme cells are proliferated from the tip of the archenteron. As the transparent gastrula elongates, a mid-ventral indentation appears; the archenteron bends and fuses with the indentation to form the mouth. The early auricularia is formed with the appearance of a looped band of cilia. Further growth produces arms and lobes over which the single, continu­ ous ciliary band is looped. This band of cilia is employed for feeding and locomotion (see Strathmann 1971, 1974, 1975). The width of the band varies; there are 3-7 cilia across the band, one cilium per cell. The band separates the body surface into aboral and circumoral fields. A transverse groove, along which food is conducted to the mouth, lies between the preoral and postoral transverse portions of the ciliary band. Encircling the mouth is an adoral band of cilia that is continuous with a ciliary band at the top of the esophagus. Calcareous ossicles are present in the posterolateral lobes of the auricu­ laria. The larva is transparent with occasional tinting of the ciliary band. Cells proliferate in the larval body cavity close to where the archenteron bends and form a hydroporic canal that opens on the dorsal surface as the hydropore. Other cells form a pouch, the axohydrocoel, near the base of the esophagus. Metamorphosis commences with diminution of the larval body and sim­ plification of the sinuous looping of the ciliary band. By the time a spherical body shape is assumed, the ciliary band has rearranged into five transverse rings of cilia. Further reduction in body size results in a compact barrel­ shaped doliolarfa. Five primary tentacles, containing evaginations of the hydrocoel, lengthen and push out through the oral indentation. Their protru­ sion marks the onset of the pentactula stage. The knobbed, "sticky" tips of the tentacles attach to the substratum at settlement. During or just after settle­ ment, aspidochirotid pentactulae grow a single ventroposterior podium and a covering coat of ossicles. Planktotrophic development and metamorphosis in holothuroids has been described and reviewed by Metschnikoff (1869), Selenka (1876), Semon (1888), Bury (1889, 1895), Mortensen (1921, 1937, 1938), Chia & Burke (1978), Maruyama (1980), Holland (1981), Cameron (1985), and Smiley (1986a,b). Fig. 28.1 - 28.6. Holothuroid larvae: (1) Eupentacta quinquesemita larva at 4 days (530-650 urn length j.ventral view showing even ciliation, oral indentation (0) and one podial pit (P) (the other podial pit is still positioned on the larva's right side (arrow) ; (2) Pentamera populifera doliolaria at 5.75 days (just prior to emergence of tentacles) (465-510 um length ), ventral view showing evenly ciliated preoral lobe (L); (3) Psolus chitonoides doliolaria at 6.3 days (925 x 400 urn), dorsal view (posterior end has not yet lost all the cilia); (4 ) Molpadia intermedia doliolaria at 77 hours (390 urn length).
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