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FAU Institutional Repository FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1989 Elsevier B.V. The final published version of this manuscript is available at http://www.sciencedirect.com/science/journal/00220981 and may be cited as: Cameron, J. L., & Fankboner, P. V. (1989). Reproductive biology of the commercial sea cucumber Parastichopus californicus (Stimpson) (Echinodermata: Holothuroidea). II. Observations on the ecology of development, recruitment and the juvenile life stage. Journal of Experimental Marine Biology and Ecology, 127(1), 43-67.doi:10.1016/0022-0981(89)90208-6 I i'V ) J. Exp. Mar. BioI. £Col., 1989, Vol. 127, pp. 43-67 43 Elsevier JEM 01229 Reproductive biology of the commercial sea cucumber Parastichopus californicus (Stimpson) (Echinodermata: Holothuroidea). II. Observations on the ecology of development, recruitment, and the juvenile life stage J. Lane Cameron and Peter V. Fankboner Department ofBiological Sciences. Simon Fraser University. Burnaby, British Columbia, Canada (Received 17 November 1987; revision received 9 January 1989; accepted 23 January 1989) Abstract: Evidence from in vitro culture of embryos and larvae of Parastichopus califomicus (Stimpson) suggests that asynchronization of development through metamorphosis and settlement results in a variable pelagic period for larvae within a particular cohort. Additionally, considerable variation in size of 0 + yr recruits observed in situ may indicate that settlement had occurred continuously for some months within the population studied. Recruitment of at least seven species of echinoderms (including P. californicus} was observed at distinct sites that were notably free of the predatory sea stars Solaster dawsoni (Verrill), S. stimpsoni (Verrill), and S. endeca (L.). The swimming response characteristic of adult P. californicus when touched by the sunflower star Pycnopodia helianthoides (Brandt) did not occur with the same regularity or intensity in juveniles. S. dawsoni preyed upon small (:S;2 yr of age) P. califomicus in aquaria; sea cucumbers > 2 yr avoided predation by swimming. Periodic collections of P. californicus recruits revealed a pattern of somatic weight loss in the fall and winter that is coincident with a similar pattern reported for the adults of this species. Visceral atrophy was observed in juvenile animals collected in the late fall. The polynoid wormArctonoepulchra (Johnson) and the endoparasitic gastropod ComenteroxenousparastichopoliTikasingh, common symbionts of adult P. californicus, were also noted on or within juvenile animals. Key words: Echinoderm; Ecology; Holothurian; Juvenile; Parastichopus califomicus INTRODUCTION The California sea cucumber Parastichopus californicus (Stimpson) is commonly found in rocky low-intertidal and subtidal areas away from strong wave action or in quiet bays and on pilings from Baja California to British Columbia (Ricketts & Calvin, 1968; Brumbaugh, 1980; Kozloff, 1983). This sea cucumber is a relatively large (60-100 em long) epibenthic detritivore, that may reach population densities as high as 0.5' m - 2, and has recently become the focus ofa limited commercial fishery within the Harbor Branch Oceanographic Institution Contribution No. 656. Correspondence address: Department of Larval Ecology, Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, Ft. Pierce, FL 34946, U.S.A. 0022-0981/89/$03.50 © 1989.Elsevier Science Publishers B.V. (Biomedical Division) 44 J.L. CAMERON AND P.V. FANKBONER inland waters of British Columbia, Canada, and Puget Sound, Washington (McDaniel, 1984; Sloan, 1985, 1986). Various aspects of the development ofP. califamicus have been examined. Mortensen (1921) reared the larvae to the early auricularia, while Courtney (1927) examined the fertility of excised gametes at various lengths of time after collection. Johnson & Johnson (1950) report on the maturity of gametes collected by dissection. M. Strathmann (1978) outlines processes for the collection and fertilization of the gametes. Smiley & Cloney (1985) discuss oogenesis and ovulation in Stichapus (= Parastichopus) califamicus (cf. Smiley, 1988). Smiley (1986) discusses metamorpho­ sis of the larvae, while Burke et al. (1986) describe the structure of the larval nervous system. Cameron & Fankboner (1984) describe tentacle structure and feeding processes in adult and juvenile animals, and describe seasonal reproductive processes (Cameron & Fankboner, 1986). Swan (1961) reports that adult P. californicus expel their visceral organs in the fall and early winter ofeach year. Fankboner & Cameron (1985), however, have shown that this process is actually visceral atrophy, not evisceration. Additionally, Margolin (1976) reports that adult P. califamicus respond by swimming to the touch of many predatory sea stars. Interestingly, none ofthe sea stars known to elicit swimming behavior prey regularly upon this sea cucumber (Greer, 1961; Mauzey et al., 1968; Shivji et aI., 1983). While much of the biology and ecology of aspidochirote holothurians in general (Mitsukuri, 1903; Trefz, 1958; Ricketts & Calviri, 1968; Jespersen & Lutzen, 1971; Bakus, 1973; Lawrence, 1979; Roberts, 1979; Sloan, 1979; Conand, 1981; Roberts & Bryce, 1982; and others) and P. califamicus specifically is well known, little has been reported on the ecology of development, recruitment, or the juvenile life stage from this group of sea cucumbers (Bakus, 1973; cf. Sloan, 1980; Conand, 1981, 1983). The occurrence and distribution of new recruits and juveniles, size and growth of recruits, predator-prey interactions among juveniles and co-occurring sea stars, and behavior of newly settled and juvenile animals warrants investigation. With the discovery of apparent nursery areas where recruits and juveniles of P. califamicus were regularly observed, and by rearing the larvae through settlement in vitro, we undertook a study of various aspects of the biology and ecology of development, recruitment, and the juvenile life stage of this sea cucumber. METHODS COLLECTION AND FERTILIZATION OF OOCYTES Adult individuals of P. califamicus were collected by scuba from Woodlands, Indian Arm Fjord, British Columbia, at 5-15 m depth. Portions of the excised ovaries from numerous female animals were placed into beakers containing 1200 ml of Millipore­ filtered (0.45 }lm) seawater and stirred at 60 rpm for 2 h. Ovarian fragments were JUVENILE HOLOTHURIAN ECOLOGY 45 removed by filtering the cultures through 500-pm mesh Nitex screen after which 5 ml dilute sperm solution (Strathmann, 1978) were added to each culture. After ~4 h oocytes exposed to sperm were washed and placed into fresh Millipore-filtered seawater. Prior to fertilization some cultures were treated with echinoderm, Pycnopodia helianthoides (Brandt), radial nerve factor (RNF) (Strathmann & Sato, 1969) or with 10- 3 M dithiothreitol (DTT) (Maruyama, 1980) to induce germinal vesicle breakdown. On one occasion naturally spawned oocytes were collected in situ by pipette as they exited the gonopore of a spawning female. This spawning sea cucumber was then placed, while under water, into a large plastic bag and transported to the laboratory. CULTURING TECHNIQUES Developing embryos and larvae were maintained at 10-12 °C and aerated by stirring with glass paddles attached to slow turning electric motors (60 rpm). Culture salinity was maintained at in situ levels of 27-28%0. Developing larvae were fed equal amounts, in excess, of the marine flagellates Dunaliella tertiolecta, Pavlova lutheri, and Isochrysis galbana (see Hinegardner, 1969; Strathmann, 1971). OCCURRENCE AND DISTRIBUTION OF JUVENILE ECHINODERMS 228 scuba dives were made from May 1979 through December 1984 to observe or collect P. califomicus in various locations around: San Juan Island (Cantilever Pier and Shady Cove) and Shaw Island (Pt. George), Washington; and Indian Arm Fjord (Woodlands Bay and Croker Island), Howe Sound (Kelvin Grove), and Clayoquot Sound (Ritchie Bay), British Columbia (Fig. 1). The presence or absence of juvenile echinoderms, especially P. califomicus, and potentially important predatory sea stars were qualitatively observed on each dive. SIZE AND GROWTH OF RECRUITS Traditionally, the juvenile sea cucumber that arises from the metamorphosis of a doliolaria or vitellaria larva has been termed a pentactula because it possesses five primary buccal tentacles (MacBride, 1914; Hyman, 1955). Even though this stage is morphologically similar to the adult, and generally found in the same habitat, it has been called a larva (Barnes, 1980, p. 995). For the purposes of this paper these newly settled animals are termed larvae as long as they possess no more than their five original buccal tentacles. When one additional buccal tentacle appears, we consider the animal a juvenile of the 0 + year class. Holothurians are quite plastic in their body dimensions, so single measurements of linear size, such as length, are unreliable. Additionally, because of the nature of their respiratory process (the filling and emptying of internal fluid-filled respiratory trees) repeat measurements of mass in individual adult P. califomicus can vary as much as 100g (J. L. Cameron, unpub!. data). Therefore, a bidimensional index of size was determined from the relationship of contracted length (em) times contracted width (em) 46 J.L. CAMERON AND P.V. FANKBONER A BRITISH COLUMBIA Fig. 1. (A) Primary study areas within the inland waters of mainland British Columbia (Howe
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