Abstract
Reproduction and development of two psolid sea cucumbers in waters of the San Juan Archipelago, Washington, were studied from April 1981 through August 1984. Spawning inPsolus chitonoides Clark andPsolidium bullatum Ohshima in the laboratory and in the field waters of the San Juan Archipelago, Washington, occurred from February through may, with heaviest spawning in April and May. The egg ofPsolus chitonoides was bright red in color and 627µm in diameter;Psolidium bullatum released eggs that were golden yellow in color and 330µm in diameter. Maximum measured fecundities (spawned eggs) forPsolus chitonoides andPsolidium bullatum were 34 700 and 3 074, respectively. Developmental schedules were similar in both species. Early cleavages were equal, radial, and holoblastic; slightly subequal cleavage was common inPsolus chitonoides. The gastrula elongated to form a uniformly ciliated larva and the vestibule first appeared as a ventral crescent-shaped depression, after which the larva decreased in length and formed three posterior ridges that encircled the early doliolaria. Just prior to settlement, there was loss of cilia between the three ridges and on the posterior end of the early doliolaria, leaving three ciliary rings that are characteristic of the dendrochirote doliolaria larva. Vertical swimming ensued, and five primary tentacles protruded through the vestibule, with occasional attachment to the substratum using the primary tentacles. Upon settlement, two primary podia emerged and all external ciliation was lost except among tentacular papillae and on the end of tube feet. Timing of appearance and of loss of ciliary rings suggest that the rings function in vertical swimming and substratum selection behaviors. Metamorphosis involved the following simultaneous events: (1) resorption of the preoral lobe, (2) formation of large, dorsal, calcareous ossicles, (3) flattening of the trivium, and (4) proliferation of ventral tube feet on Ambulacral Radii B and E to form the sole. Reproduction in the family Psolidae is reviewed. The large proportion of brooders in this family appears to be related to small size, the possession of protective armor and sole, and geographic distribution (mainly in Antarctica). Lecithotrophic doliolaria larvae with three ciliary rings are produced by large northern psolids.
Similar content being viewed by others
Literature cited
Agassiz, A. (1864). On the embryology of echinoderms. Mem. Am. Acad. Arts Sci. 9: 1–30
Agassiz, E. C., Agassiz, A. (1865). Seaside studies in natural history. Marine animals of Massachusetts Bay. Radiates. Ticknor & Fields, Boston, USA
Arnaud, P. M. (1974). Contribution a la bionomie marine benthique des regions antarctiques et subantarctiques. Téthys 6: 465–656
Austin, W. C. (1985). An annotated checklist of marine invertebrates in the cold temperate northeast Pacific. Vol. 1. Khoyatan Marine Laboratory, Institute of Ocean Sciences Fisheries and Oceans. Fotoprint Ltd., Victoria, B.C., Canada
Bernasconi, I. (1941). Los equinodermos de la expedición del Buque Oceanográfico “Comodoro Rivadavia” A.R.A. Physis, B. Aires 19: 37–49 + pls 1–8
Boolootian, R. A. (1966). Reproductive physiology. In: Boolootian, R. A. (ed.) Physiology of Echinodermata. Wiley-Interscience, New York, p. 561–614
Chia, F. S., Atwood, D. G., Crawford, B. (1975). Comparative morphology of echinoderm sperm and the possible phylogenetic implications. Am. Zool. 15: 533–565
Chia, F. S., Buchanan, J. B. (1969). Larval development ofCucumaria elongata. J. mar. biol. Ass. U.K. 49: 151–159
Chia, F. S., Buckland-Nicks, J., Young, C. M. (1984). Locomotion of marine invertebrate larvae: a review. Can. J. Zool. 62: 1205–1222
Chia, F. S., Spaulding, J. G. (1972). Development and juvenile growth of the sea anemone,Tealia crassicornis. Biol. Bull. mar. biol. Lab., Woods Hole 142: 206–218
Clark, H. L. (1901). The holothurians of the Pacific Coast of North America. Zool. Anz. 24: 162–171
Clark, H. L. (1902). The breeding habits of holothurians. Rep. Mich. Acad. Sci. 3: 1–28
Dayton, P. K., Robilliard, G. S., Paine, R. T., Dayton, L. B. (1974). Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecol. Monogr. 44: 105–128
Deichmann, E. (1930). The holothurians of the western part of the Atlantic Ocean. Bull. Mus. comp. Zool. Harv. 71: 41–226 + 24 plates
Deichmann, E. (1941). The Holothuroidea collected by the Velero III during the years 1932 to 1938. Part I. Dendrochirota. Allan Hancock Pacif. Exped. 8: 61–194
Ekman, S. (1925). Holothurien. Further zool. Results Swed. Antarct. Exped. 1 (6): 1–194
Fankboner, P. V. (1978). Suspension-feeding mechanisms of the armoured sea cucumberPsolus chitonoides. J. exp. mar. Biol. Ecol. 31: 11–25
Fernald, R. L. (1959). The rearing of invertebrate embryos. In: Pratt, I., McCauley, J. E. (eds.) Marine biology (Proc. 20th A. Biol. Colloquium) Oregon State College, Corvallis, Oregon, p. 51–58
Hadfield, M. G. (1961). The morphology of a psolid holothurian. M. Sc. thesis. University of Washington, Seattle
Hendler, G. (1975). Adaptational significance of the patterns of ophiuroid development. Am Zool. 15: 691–715
Hernández, D. A. (1981). Holothuroidea de Puerto Deseado (Santa Cruz, Argentina). Revta Mus. agent. Cienc. nat. Bernardino Rivadavia Inst. nac. Invest. Cienc. nat. (Hidrobiologia) 4: 151–168
Hyman, L. H. (1955). The invertebrates. Vol. IV. Echinodermata. McGraw-Hill Book Co., Inc., New York
Johnson, L. (1931). Rearing and identification of certain holothurian larvae. M. Sc. thesis. University of Washington, Seattle
Johnson, M. W., Johnson, L. T. (1950). Early life history and larval development of some Puget Sound echinoderms. Contr. Scripps Instn Oceanogr. 439: 73–84
Jones, S. (1960). Early embryology ofPsolus chitonoides. M. Sc. thesis. University of Washington, Seattle
Lee, H. (1984). Fast swimming speeds of ciliated marine invertebrate larvae: potential importance at the time of settlement. Am. Zool. 24: p. 131A
Lee, H. (1985). Swimming of ciliated marine invertebrate larvae: relationship between speed and morphology. Am. Zool. 25: p. 129A
Ludwig, H. (1897a). Ein neuer Fall von Brutpflege bei Holothurien. Zool. Anz. 20: 217–219
Ludwig, H. (1897b). Brutpflege beiPsolus antarcticus. Zool. Anz. 20: 237–239
Ludwig, H. (1898). Holothurien der Hamburger Magalhaenische Sammelreise. Wiss. Ergebn. dt. Hamburger magalhaen. Sammelreise 3: 1–98 + 3 plates
Ludwig, H. (1904). Brutpflege bei Echinodermen. Zool. Jb. (Beih.) 7: 683–699
McEuen, F. S. (1984). Chemical and morphological defenses of holothuroid eggs, larvae and juveniles. Am. Zool. 24: p. 25A
McEuen, F. S. (1986). The reproductive biology and development of twelve species of holothuroids from the San Juan Islands, Washington. Ph. D. thesis. University of Alberta, Edmonton, Canada
McEuen, F. S. (1987). Chapter 28. Phylum Echinodermata, class Holothuroidea. In: Strathmann, M. F. (ed.) Reproduction and development of marine invertebrates of the Northern Pacific coast. Data and methods for the study of eggs, embryos, and larvae. University of Washington Press, Seattle, p. 574–596
McEuen, F. S. (1988). Spawning behaviors of northeast Pacific sea cucumbers (Holothuroidea: Echinodermata). Mar. Biol. 98: 565–585
McEuen, F. S., Chia, F. S. (1985). Larval development of a molpadiid holothuroid,Molpadia intermedia (Ludwig, 1894) (Echinodermata). Can. J. Zool. 63: 2553–2559
McKenzie, J. D. (1985). The tentacular ultrastructure of dendrochirote holothurians. A comparative SEM study. In: Keegan, B. F., O'Connor, B. D. S. (eds.) Echinodermata. A. A. Balkema, Rotterdam, p. 445–450
McKenzie, J. D. (1987). The ultrastructure of the tentacles of eleven species of dendrochirote holothurians studies with special reference to the surface coats and papillae. Cell Tissue Res. 248: 187–199
Miller, J. E. (1983). Coelomic broodcare by a psolid holothurian from Bermuda and the Caribbean. Am. Zool. 23: p. 1005
Miller, J. E. (1985). Viviparity in a psolid holothurian from the tropical western Atlantic. In: Keegan, B. F., O'Connor, B. D. S. (eds.) Echinodermata. A. A. Balkema, Rotterdam, p. 472
Miller, J. E., Pawson, D. L. (1984). Holothurians (Echinodermata: Holothuroidea). Mem. ‘Hourglass’ Cruises 7: 1–79. (Fla mar. Res. Lab., St. Petersburg)
Mortensen, T. (1901). Die Echinodermenlarven. Nord. Plankt. 9: 1–30
Mortensen, T. (1925). Papers from Dr. Th. Mortensen's Pacific expedition 1914–1916. 29. Parts 3–5. Vidensk. Meddr dansk naturh. Foren. 79: 261–420 + 12-13 plates
Mortensen, T. (1927). Handbook of the echinoderms of the British Isles. Oxford University Press, Edinburgh
Mortensen, T., Lieberkind, I. (1928). Echinoderma. Tierwelt N.- u. Ostsee 12: 1–127
Nordgaard, O. (1912). Faunistiske og biologiske lakttagelser ved den Biologiske Station i Bergen. K. norske Vidensk. Selsk. Skr. 1911 (6): 1–58
Pawson, D. L. (1966). Phylogeny and evolution of holothuroids. In: Moore, R. C. (ed.) Treatise on invertebrate paleontology. Part U: Echinodermata 3. Vol. 2. Geological Society of America, Inc. and University of Kansas Press, Kansas, p. 641–646
Pawson, D. L. (1967). The psolid holothurian genusLissothuria. Proc. U.S. natn. Mus. 122: 1–17
Pawson, D. L. (1969a). Holothuroidea from Chile. Report no. 46 of the Lund University Chile Expedition, 1948–1949. Sarsia 38: 121–145
Pawson, D. L. (1969b). Holothuroidea. Antarct. Map Folio Ser. (Folio Am. geogr. Soc.) 11: 36–38
Pawson, D. L. (1971a).Ekkentropelma brychia n. g., n. sp., an Antarctic psolid holothurian with a functionally lateral sole. Proc. biol. Soc. Wash. 84: 113–118
Pawson, D. L. (1971b). The western Australian psolid holothurianCeto cuvieria (Cuvier). J. Proc. R. Soc. West. Aust. 54: 33–39
Pawson, D. L. (1982). Holothuroidea. In: Parker, S. P. (ed.) Synopsis and classification of living organisms. Vol. 2. McGraw-Hill Book Co., New York, p. 813–818
Runnström, J., Runnström, S. (1919). Über die Entwicklung vonCucumaria frondosa Gunnerus undPsolus phantapus Strussenfeld. Bergens Mus. Årb. 1918–1919 (5): 1–100
Semon, R. (1888). Die Entwickelung derSynapta digitata und ihre Bedeutung für die Phylogenie der Echinodermen. Jena. Z. Naturw. 22: 175–305 + 7 plates
Smith, D. L. (1977). A guide to marine coastal plankton and marine invertebrate larvae. Kendall/Hunt Publishing Co., Dubuque, Iowa, USA
Smith, T. B. (1983). Tentacular ultrastructure and feeding behaviour ofNeopentadactyla mixta (Holothuroidea: Dendrochirota). J. mar. biol. Ass. U.K. 63: 301–311
Theel, H. (1886). Report of the Holothuroidea dredged by H.M.S. Challenger during the years 1873–1876. Rep. scient. Results Voyage HMS Challenger 14 (39): 1–290 + 2 plates
Thomson, C. W. (1878a). The voyage of the “Challenger”. The Atlantic. Vol. II. Macmillan & Co., London
Thomson, C. W. (1878b). Notice of some peculiarities in the mode of propagation of certain echinoderms of the Southern Sea. J. Linn. Soc. (Zool.) 13: 55–79
Thorson, G. (1946). Reproduction and larval development of Danish marine bottom invertebrates. Meddr Kommn Danm. Fisk.-og Havunders. (Ser. Plankton) 4: 1–523
Vaney, C. (1906). Deux nouvelles holothuries incubatrices. C. r. Ass. fr. Avanc. Sci. (Pt 2: Notes et memoires) 35: 535–538
Vaney, C. (1907). Echinodermes: Holothuries. Docums scient. Sciences nat. Expéd. antarct. fr. (1903–1905) 1: 1–30 + 2 plates (Masson et Cie, Paris)
Vaney, C. (1914). Holothuries. Docums scient. Sciences nat. II. Expéd. antarct. fr. (1908–1910) 5: 1–54 (Masson et Cie, Paris)
Vaney, C. (1925). L'incubation chez les holothuries. Trav. Stn zool. Wimereux 9: 254–274
Wootton, D. (1949). The development ofThyonepsolus nutriens. Ph. D. thesis. Stanford University, Stanford, USA
Young, C. M., Chia, F.-S. (1982). Factors controlling spatial distribution of the sea cucumberPsolus chitonoides: settling and post-settling behavior. Mar. Biol. 69: 195–205
Author information
Authors and Affiliations
Additional information
Communicated by R. S. Carney, Baton Rouge
Rights and permissions
About this article
Cite this article
McEuen, F.S., Chia, F.S. Development and metamorphosis of two psolid sea cucumbers,Psolus chitonoides andPsolidium bullatum, with a review of reproductive patterns in the family Psolidae (Holothuroidea: Echinodermata). Mar. Biol. 109, 267–279 (1991). https://doi.org/10.1007/BF01319395
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01319395