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Feeding Potential in the Lecithotrophic Larvae of Adalaria Proxima and Tritonia Hombergi: An Evolutionary Perspective

Published online by Cambridge University Press:  11 May 2009

Stephen C. Kempf
Affiliation:
University of St Andrews, Department of Biology and Pre-Clinical Medicine, Gatty Marine Laboratory, St Andrews, Fife, Scotland, KY16 8LB and Department of Zoology and Wildlife Science, 101 Cary Hall, Auburn University, Auburn, AL 36849, USA
Christopher D. Todd
Affiliation:
University of St Andrews, Department of Biology and Pre-Clinical Medicine, Gatty Marine Laboratory, St Andrews, Fife, Scotland, KYI 6 8LB

Extract

Vance (1973a, b) argued that among the possible range of developmental strategies available to marine invertebrates, only the extremes of obligate planktotrophy and obligate lecithotrophy are evolutionarily stable. Vance's model, relating reproductive 'efficiency' to egg size (in terms of energetic content), predation rate, and prefeeding (lecithotrophic) vs feeding (planktotrophic) larval periods, has been a source of much discussion and debate since its inception (e.g. Underwood, 1974; Vance, 1974; Christiansen & Fenchel, 1979; Obrebski, 1979; Williams, 1980; Jablonski & Lutz, 1983; Strathmann, 1978, 1985; Todd, 1985). Subsequent publications have continued to dwell mainly on potential selective factors and the extremes of larval developmental type (i.e. obligate planktotrophy or obligate non-pelagic lecithotrophy). For the most part, these investigations have ignored questions concerning how a transition from one larval type to another would be accomplished in morphological and functional terms. Nonetheless, the consensus persists that small eggs and planktotrophy are the primitive (or ancestral) condition, and that lecithotrophy is the more advanced evolutionary derivative (see Strathmann, 1978,1985).

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1989

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References

REFERENCES

Bayne, B.L., 1983. Physiological ecology of marine molluscan larvae. In The Mollusca, vol. 3 (ed. N.H., Verdonket al.), pp. 299343. New York: Academic Press.Google Scholar
Bickell, L.R. & Chia, F.S., 1979. Organogenesis and histogenesis in the planktotrophic veliger of Doridella steinbergae (Opisthobranchia: Nudibranchia). Marine Biology, 52, 291313.CrossRefGoogle Scholar
Bickell, L.R., Chia, F.S. & Crawford, B.J., 1981. Morphogenesis of the digestive system during metamorphosis of the nudibranch Doridella steinbergae (Gastropoda): conversion from phytoplanktivore to carnivore. Marine Biology, 62, 116.CrossRefGoogle Scholar
Bickell, L.R. & Kempf, S.C., 1983. Larval and metamorphic morphogenesis in the nudibranch Melibe leonina (Mollusca: Opisthobranchia). Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 165, 119138.CrossRefGoogle Scholar
Bonar, D.B., 1978. Morphogenesis at metamorphosis in opisthobranch molluscs. In Settlement and Metamorphosis of Marine Invertebrate Larvae (ed. F-S., Chia and Rice, M.E.), pp. 177196. New York: Elsevier.Google Scholar
Bonar, D.B. & Hadfield, M.G., 1974. Metamorphosis of the marine gastropod Phestilla sibogae Bergh (Nudibranchia: Aeolidacea). I. Light and electron microscopic analysis of larval and metamorphic stages. Journal of Experimental Marine Biology and Ecology, 16, 227255.CrossRefGoogle Scholar
Bridges, C.B., 1975. Larval development of Phyllaplysia taylori Dall, with a discussion of development in the anaspidea (Opisthobranchia: Anaspidea). Ophelia, 14, 161184.CrossRefGoogle Scholar
Brody, S., 1945. Bioenergetics and Growth. New York: Reinhold.Google Scholar
Christiansen, F.B. & Fenchel, T.M., 1979. Evolution of marine invertebrate reproductive patterns. Theoretical Population Biology, 16, 267282.CrossRefGoogle Scholar
Clark, K.B. & Jensen, K.R., 1981. A comparison of egg size, capsule size, and developmental patterns in the order Ascoglossa (Sacoglossa) (Mollusca: Opisthobranchia). International Journal of Invertebrate Reproduction, 3, 5764.CrossRefGoogle Scholar
Emlet, R.B., 1986. Facultative planktotrophy in the tropical echinoid Clypeaster rosaceus (Linnaeus) and a comparison with obligate planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroidea: Echinoidea). Journal of Experimental Marine Biology and Ecology, 95, 183202.CrossRefGoogle Scholar
Eyster, L.S., 1980. Distribution and reproduction of shell-less opisthobranchs from South Carolina. Bulletin of Marine Science, 30, 580599.Google Scholar
Eyster, L.S. & Stancyk, S.E., 1981. Reproduction, growth, and trophic interactions of Doriopsilla pharpa Marcus in South Carolina. Bulletin of Marine Science, 31, 7282.Google Scholar
Folin, G. & Malmros, M., 1929. An improved form of Folin's micromethod for blood sugar determinations. Journal of Biological Chemistry, 83, 115120.CrossRefGoogle Scholar
Freeman, C.P. & West, D., 1966. Complete separation of lipid classes on a single thin-layer plate. Journal of Lipid Research, 7, 324327.CrossRefGoogle ScholarPubMed
Hadfield, M.G. & Miller, S.E., 1987. On developmental patterns of opisthobranchs. American Malacological Bulletin, 5, 197214.Google Scholar
Hadfield, M.G. & Switzer-Dunlap, M.F., 1984. Opisthobranchs. In The Mollusca, vol. 7 (ed. K.M., Wilber), pp. 209350. New York: Academic Press.Google Scholar
Harris, L.G., 1975. Studies on the life history of two coral eating nudibranchs of the genus Phestilla. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 149, 539550.CrossRefGoogle ScholarPubMed
Holland, D.L., 1978. Lipid reserves and energy metabolism in the larvae of benthic marine invertebrates. In Biochemical and Biophysical Perspectives in Marine Biology, vol. 4 (ed. D.C., Mullins and J.R., Sargent), pp. 85123. London: Academic Press.Google Scholar
Holland, D.L. & Gabbott, P.A., 1971. A micro-analytical scheme for the determination of protein, carbohydrate, lipid, and RNA levels in marine invertebrate larvae. Journal of the Marine Biological Association of the United Kingdom, 51, 659668.CrossRefGoogle Scholar
Holland, D.L. & Spencer, B.E., 1973. Biochemical changes in fed and starved oysters, Ostrea edulis L. during larval development, metamorphosis and early spat growth. Journal of the Marine Biological Association of the United Kingdom, 53, 287298.CrossRefGoogle Scholar
Holland, D.L., Tantanasiriwong, R. & Hannant, P.J., 1975. Biochemical composition and energy reserves in the larvae and adults of four British periwinkles Littorina littorea, L. littoralis, L. saxatilis, and L. neritoides. Marine Biology, 33, 235239.CrossRefGoogle Scholar
Hurst, A., 1967. The egg masses and veligers of thirty northeast Pacific opisthobranchs. Veliger, 9, 255288.Google Scholar
Jablonski, D. & Lutz, R.A., 1983. Larval ecology of marine benthic invertebrates: paleobiological implications. Biological Reviews, 58, 2189.CrossRefGoogle Scholar
Kempf, S.C., 1981. Long-lived larvae of the gastropod Aplysia juliana: do they disperse and metamorphose or just slowly fade away? Marine Ecology - Progress Series, 6, 6165.CrossRefGoogle Scholar
Kempf, S.C., 1982. Acquisition, Storage and Utilization of Nutrients by Embryos and Larvae of Marine Molluscs. PhD dissertation, University of Hawaii, Honolulu.Google Scholar
Kempf, S.C. & Hadfield, M.G., 1985. Planktotrophy by the lecithotrophic larvae of a nudibranch, Phestilla sibogae (Gastropoda). Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 169, 119130.CrossRefGoogle Scholar
Kempf, S.C. & Willows, A.O.D., 1977. Laboratory culture of the nudibranch Tritonia diomedea Bergh (Tritoniidae: Opisthobranchia) and some aspects of its behavioral development. Journal of Experimental Marine Biology and Ecology, 30, 261276.CrossRefGoogle Scholar
Lowry, O., Rosebrough, W.J., Farr, A. & Randall, R.J., 1951. Protein measurement with the Folinphenol reagent. Journal of Biological Chemistry, 193, 265275.CrossRefGoogle Scholar
Lucas, M.I., Walker, G., Holland, D.L. & Crisp, D.J., 1979. An energy budget for the free swimming and metamorphosing larvae of Balanus balanoides (Crustacea: Cirripedia). Marine Biology, 55, 221229.CrossRefGoogle Scholar
Marsh, J.B. & Weinstein, D.B., 1966. Simple charring method for determination of lipids. Journal of Lipid Research, 7, 574576.CrossRefGoogle ScholarPubMed
Millar, R.H. & Scott, J.M., 1967. The larva of the oyster Ostrea edulis during starvation. Journal of the Marine Biological Association of the United Kingdom, 47, 475484.CrossRefGoogle Scholar
Obrebski, S, 1979. Larval colonizing strategies in marine benthic invertebrates. Marine Ecology - Progress Series, 1, 293300.CrossRefGoogle Scholar
Perron, F.E., 1981. The partitioning of reproductive energy between ova and protective capsules in marine gastropods of the genus Conus. American Naturalist, 118, 110118.CrossRefGoogle Scholar
Provasoli, L, 1968. Media and prospects for the cultivation of marine algae. In Cultures and Collections of Algae. Proceedings of the United States - Japan Conference, Hakone, 1966 (ed. A., Watanabe and A., Hattori), pp. 6375. Hakone: Japanese Society of Plant Physiologists.Google Scholar
Rahat, M., 1976. Direct development and symbiotic chloroplasts in Elysia timida (Mollusca: Opisthobranchia). Israel Journal of Zoology, 25, 186193.Google Scholar
Richardson, K.C., Jarrett, L. & Finke, E.H., 1960. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technology, 35, 313323.CrossRefGoogle ScholarPubMed
Rivest, B.R., 1978. Development of the eolid nudibranch Cuthona nana (Alder and Hancock, 1842), and its relationship with a hydroid and hermit crab. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Mass., 154, 157175.CrossRefGoogle ScholarPubMed
Schmekel, L., 1966. Zwei neue Arten der Familie Cuthonidae aus dem Golf von Neapel: Trinchesia granosa n.sp. und Trinchesia ocellata n.sp. (Gastropoda, Opisthobranchia). Pubblicazioni della Stazione Zoologica di Napoli, 35, 1328.Google Scholar
Schonenberger, N., 1969. Beitrage zur Entwicklung und Morphologie von Trinchesia granosa Schmekel (Gastropoda, Opisthobranchia). Pubblicazioni della Stazione Zoologica di Napoli, 37, 236292.Google Scholar
Strathmann, R.R., 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evolution, 32, 894906.CrossRefGoogle ScholarPubMed
Strathmann, R.R., 1985. Feeding and non-feeding larval development and life history evolution in marine invertebrates. Annual Review of Ecology and Systematics, 16, 339361.CrossRefGoogle Scholar
Switzer-Dunlap, M.F. & Hadfield, M.G., 1977. Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda, Opisthobranchia) in laboratory culture. Journal of Experimental Marine Biology and Ecology, 29, 245261.CrossRefGoogle Scholar
Switzer-Dunlap, M.F. & Hadfield, M.G., 1981. Laboratory culture of Aplysia. In Laboratory Animal Management: Marine Invertebrates. Report of the National Research Committee on Marine Invertebrates, Institute of Laboratory Animal Resources. National Research Council, pp. 199216. Washington, DC: National Academy Press.Google Scholar
Tardy, J., 1962. Cycle biologique et métamorphose d'Eolidina alderi (Gastéropode, Nudibranche). Compte Rendu des Séances de l'Académie des Sciences, 255, 32503252.Google Scholar
Thompson, T.E., 1958. The natural history, embryology, larval biology, and post-larval development of Adalaria proxima (Alder and Hancock) (Gastropoda Opisthobranchia). Philosophical Transactions of the Royal Society (B), 242, 158.Google Scholar
Thompson, T.E., 1959. Feeding in nudibranch larvae. Journal of the Marine Biological Association of the United Kingdom, 38, 239248.CrossRefGoogle Scholar
Thompson, T.E., 1962. Studies on the ontogeny of Tritonia hombergi Cuvier (Gastropoda Opisthobranchia). Philosophical Transactions of the Royal Society (B), 245, 171218.Google Scholar
Thompson, T.E., 1966. Studies on the reproduction of Archidoris pseudoargus (Rapp) (Gastropoda Opisthobranchia). Philosophical Transactions of the Royal Society (B), 250, 343375.Google Scholar
Thompson, T.E., 1967. Direct development in a nudibranch, Cadlina laevis, with a discussion of developmental processes in Opisthobranchia. Journal of the Marine Biological Association of the United Kingdom, 47, 122.CrossRefGoogle Scholar
Todd, C.D., 1981. The ecology of nudibranch molluscs. Oceanography and Marine Biology, an Annual Review, 19, 141234.Google Scholar
Todd, C.D. 1985. Reproductive strategies of north-temperate rocky shore invertebrates. In The Ecology of Rocky Coasts (ed. P.G., Moore and R., Seed), pp. 203219. London: Hodder & Stoughton.Google Scholar
Todd, C.D., 1987. Reproductive energetics and larval strategies of nudibranch molluscs: effects of ration level during the spawning period in Onchidoris muricata (Müller) and Adalaria proxima (Alder and Hancock). American Malacological Bulletin, 5, 293301.Google Scholar
Todd, C.D., 1989. Larval strategies of nudibranch molluscs: similar means to the same end? Malacologia, in press.Google Scholar
Underwood, A.J., 1974. On models of reproductive strategy in marine benthic invertebrates. American Naturalist, 108, 874878.CrossRefGoogle Scholar
Vance, R.R., 1973a. On reproductive strategies in marine benthic invertebrates. American Naturalist, 107, 339352.CrossRefGoogle Scholar
Vance, R.R., 1973b. More on reproductive strategies in marine benthic invertebrates. American Naturalist, 107, 353361.CrossRefGoogle Scholar
Vance, R.R., 1974. Reply to Underwood. American Naturalist, 108, 879880.CrossRefGoogle Scholar
Venable, J.H. & Coggeshall, R., 1965. A simplified lead citrate stain for use in electron microscopy. Journal of Cell Biology, 25, 407408.CrossRefGoogle ScholarPubMed
Walpole, R.E., 1974. Introduction to Statistics, 2nd ed. New York: Macmillan.Google Scholar
Williams, L.G., 1980. Development and feeding of larvae of the nudibranch gastropods Hermissenda crassicornis and Aeolidia papillosa. Malacologia, 120, 99116.Google Scholar