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Apical skeletons of sea urchins (Echinodermata: Echinoidea): two methods for inferring mode of larval development

Published online by Cambridge University Press:  08 April 2016

Richard B. Emlet*
Affiliation:
Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560

Abstract

Recent data from mollusks suggest that mode of larval development may have important consequences for rates of speciation and extinction of marine organisms. The present study examines two methods that may be used to infer mode of development in the tests of fossil and Recent echinoids: genital pore size and crystallographic patterns of apical plates. Extant species with known modes of development were examined, and the following hypotheses were tested. 1) Species that produce large eggs and have nonfeeding larval development have larger genital pores than species that produce small eggs and have feeding larval development. 2) Orientations of crystallographic axes (c-axes) of genital and ocular plates differ in species with differing modes of development and can be used to infer mode of development. Genital pore size was found to be strongly dependent on body size within a species. For some taxa, pairwise interspecific comparisons of the relationships between genital pore size and body size support the hypothesis of larger genital pores for species with nonfeeding larval development. However, in multiple comparisons of linear regressions, species with nonfeeding larval development always overlapped other species with feeding larval development. An examination of the allometry of genital pore growth showed some species with nonfeeding larval development differed from those with feeding larval development; other species with differing modes of development could not be distinguished on the basis of allometric growth parameters. Orientations of c-axes of genital plates were found to be accurate indicators of mode of development, but orientations of c-axes of ocular plates were not. Among regular echinoids, 71 of 72 species supported the hypothesis that orientation of c-axes of genital plates is indicative of mode of development. Among 19 spatangoid echinoids studied, orientations of c-axes of genital plates generally allowed separation of species with differing modes of development. This method cannot be used to infer modes of development in taxa with reduced numbers of genital plates such as some spatangoids, some cassiduloids, and all clypeasteroids. Taxonomic differences in c-axis orientations require that inferences be made from comparisons between species within families.

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Articles
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Copyright © The Paleontological Society 

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References

Literature Cited

Arrau, L. 1958. Desarrollo del erizo comestible de Chile Loxechinus albus. Revista de Biologia Marina, Valparaiso 7:3962.Google Scholar
Barker, M. F. 1985. Reproduction and development in Goniocidaris umbraculum, a brooding echinoid. Pp. 207214. In Keegan, B. F., and O'Connor, B. D. S. (eds.), Proceedings of the Fifth International Echinoderm Conference, Galway. Balkema Press; Rotterdam.Google Scholar
Bay-Schmith, E. 1981. Ciclo anual de reproduction de Arbacia spatuligera (Valenciennes, 1846) en la bahia de Concepcion, Chile (Echinoidea: Arbaciidae). Boletin de la Sociedad de Biologia de Concepcion 51:4759.Google Scholar
Bernasconi, I. 1942. Primeros estados larveles de Arbacia dufresnei (Blv.). Physis (Bueno Aires) 19:305312.Google Scholar
Bernasconi, I. 1953. Monographia de los equinoideos argentinos. Anales Museo de Historia Natural de Montevideo, Serie 2A 6:158.Google Scholar
Bosch, I., Beauchamp, K. A., Steele, M. E., and Pearse, J. S. 1987. Development, metamorphosis and seasonal abundance of embryos and larvae of the Antarctic sea urchin Sterechinus neumayeri. Biological Bulletin 173:126135.Google Scholar
Cram, D. L. 1971. Life history studies on South African echinoids 1. Parechinus angulosus (Leske) (Echinidae, Parechinidae). Transactions of the Royal Society of South Africa 39:321337.CrossRefGoogle Scholar
Dartnall, A. J. 1972. A brooding echinoid from Tasmania. Proceedings of the Linnean Society of New South Wales 97:3034.Google Scholar
Dillaman, R. M., and Hart, H. V. 1981. X-ray evaluation of a SEM technique for determining the crystallography of echinoid skeletons. Scanning Electron Microscopy 1981, 111:313320.Google Scholar
Dix, T. G. 1969. Larval life span of the echinoid Evechinus chloroticus. New Zealand Journal of Marine and Freshwater Research 3:1316.CrossRefGoogle Scholar
Emlet, R. B. 1982. Echinoderm calcite: a mechanical analysis from larval spicules. Biological Bulletin 163:264275.Google Scholar
Emlet, R. B. 1985. Crystal axes in Recent and fossil echinoids indicate trophic mode in larval development. Science 230:937940.CrossRefGoogle ScholarPubMed
Emlet, R. B. 1988a. Crystallographic axes of echinoid genital plates reflect larval form: some phylogenetic implications. Pp. 299310. In Paul, C. R. C., and Smith, A. B. (eds.), Echinoderm Phylogeny and Evolutionary Biology. Clarendon Press; Oxford.Google Scholar
Emlet, R. B. 1988b. Larval form and metamorphosis of the “primitive” echinoid Eucidaris thouarsi (Echinodermata: Echinoidea: Cidaroida): implications for developmental and phylogenetic studies. Biological Bulletin 174:419.Google Scholar
Emlet, R. B., McEdward, L. R., and Strathmann, R. R. 1987. Echinoderm larval ecology viewed from the egg. Pp. 55136. In Jangoux, M., and Lawrence, J. M. (eds.), Echinoderm Studies, Volume 2. Balkema Press; Rotterdam.Google Scholar
Emmons, R. C. 1943. The universal stage (with 5 axes of rotation). Geological Society of American Memoir 8.Google Scholar
Fell, F. J. 1976. The Cidaroida (Echinodermata: Echinoidea) of Antarctica and the Southern Oceans. Unpublished Ph.D. dissertation, University of Maine. Orono, Maine.Google Scholar
Fisher, D. C., and Cox, R. S. 1988. Application of skeletal crystallography to phylogenetic inference in fossil echinoderms. P. 797. In Burke, R. D., Mladenov, P. V., Lambert, P., and Parsley, R. L. (eds.), Echinoderm Biology, Proceedings of the Sixth International Echinoderm Conference, Victoria, August 1987. Balkema Press; Rotterdam.Google Scholar
Gage, J. D., Billet, D. S. M., Jensen, M., and Tyler, P. A. 1985. Echinoderms of the Rockall Trough and adjacent areas 2. Echinoidea and Holothurioidea. Bulletin of the British Museum of Natural History (Zoology) 48:173213.Google Scholar
Gordon, I. 1926a. The development of the calcareous test of Echinus miliaris. Philosophical Transactions of the Royal Society, London B 214:259312.Google Scholar
Gordon, I. 1926b. The development of the calcareous test of Echinocardium cordatum. Philosophical Transactions of the Royal Society, London B 215:255313.Google Scholar
Gordon, I. 1929. Skeleton development in Arbacia, Echinarachnius, and Leptasterias. Philosophical Transactions of the Royal Society, London B 217:289334.Google Scholar
Hansen, T. A. 1978. Larval dispersal and species longevity in lower Tertiary gastropods. Science 199:885887.CrossRefGoogle ScholarPubMed
Hansen, T. A. 1980. Influence of larval dispersal and geographic distribution on species longevity in neogastropods. Paleobiology 6:193207.Google Scholar
Harvey, E. B. 1956. The American Arbacia and Other Sea Urchins. Princeton University Press; Princeton, New Jersey.Google Scholar
Hesse, R., and Doflein, F. 1910-1914. Tierbau und Tierleben. Bd. I-II; Leipzig.Google Scholar
Hinegardner, R. T. 1969. Growth and development of the laboratory cultured sea urchin. Biological Bulletin 137:465475.Google Scholar
Holland, N. D. 1967. Gametogenesis during the annual reproductive cycle in a cidaroid sea urchin (Stylocidaris affinis). Biological Bulletin 133:578590.Google Scholar
Imschenetsky, M., Pucci, M., and Massone, R. 1980. Histone analysis during the first cell cycle of sea urchin embryos. Differentiation 17:111115.Google Scholar
Jablonski, D. 1982. Evolutionary rates and modes in late Cretaceous gastropods: role of larval ecology. Proceedings of the Third North American Paleontological Convention 1:257262.Google Scholar
Jablonski, D. 1986. Larval ecology and macroevolution in marine invertebrates. Bulletin of Marine Science 39:565587.Google Scholar
Jablonski, D., and Lutz, R. A. 1983. Larval ecology of benthic marine invertebrates: paleobiological implications. Biological Reviews, Cambridge 58:2189.Google Scholar
Johnson, M. 1930. Notes on larval development of Strongylocentrotus franciscanus. Publications of the Puget Sound Biological Station 7:401411.Google Scholar
Kier, P. M. 1968. Echinoids from the middle Eocene Lake City Formation of Georgia. Smithsonian Miscellaneous Collections 153:145.Google Scholar
Kier, P. M. 1969. Sexual dimorphism in fossil echinoids. Pp. 215222. In Westermann, G. E. G. (ed.), Sexual Dimorphism in Fossil Metazoa and Taxonomic Implications. Schweizerbart'-sche Verlagsbuchhandlung; Stuttgart.Google Scholar
Kier, P. M. 1974. Evolutionary trends and their functional significance in the post-Paleozoic echinoids. Paleontological Society Memoir 5:195.Google Scholar
Kier, P. M. 1977. The poor fossil record of the regular echinoid. Paleobiology 3:168174.Google Scholar
Koehler, R. 1912. Echinoderms (Asteries, Ophiures, et Echinides). Deuxième Expedition Antarctique Française (1908-1910) 16:1272.Google Scholar
Koehler, R. 1926. Echinodermata Echinoidea. Australasian Antarctic Expedition (1911-1914), Scientific Reports 8:1134.Google Scholar
Lawrence, J. M. 1987. A Functional Biology of Echinoderms. Johns Hopkins University Press; Baltimore, Maryland.Google Scholar
Lewis, J. B. 1958. The biology of the tropical sea urchin Tripneustes esculentus in Barbados, British West Indies. Canadian Journal of Zoology 36:607621.Google Scholar
Lonning, S., and Wennerberg, C. 1963. Biometric studies of echinoderm eggs. Sarsia 11:2527.Google Scholar
MacBride, E. W. 1903. The development of Echinus esculentus together with some points in the development of E. miliaris and E. acutus. Philosophical Transactions of the Royal Society, London B 195:285327.Google Scholar
MacBride, E. W. 1914. The development of Echinocardium cordatum Pt. 1: the external features of the development. Quarterly Journal of Microscopical Science 59:471486.Google Scholar
McEdward, L. R. 1986. Comparative morphometrics of echinoderm larvae. I. Some relationships between egg size and initial larval form in echinoids. Journal of Experimental Marine Biology and Ecology 96:251265.Google Scholar
Mazur, J. E., and Miller, J. W. 1971. A description of the complete metamorphosis of the sea urchin Lytechinus variegatus cultured in synthetic sea water. Ohio Journal of Science 71:3036.Google Scholar
Mortensen, T. 1909. Die Echinoiden der deutschen Sudpolar expedition, 1901-1903. Deutsche Sudpolar-Expedition 1901-1903, Zoologie 11:1113.Google Scholar
Mortensen, T. 1910. The Echinoidea of the Swedish South-polar expedition. Wissenschaftliche Ergebnisse der Schwedischen Sudpolar-Expedition 1901-1903. 6:1114.Google Scholar
Mortensen, T. 1913. On the development of some British echinoderms. Journal of the Marine Biological Association, United Kingdom 10:118.Google Scholar
Mortensen, T. 1920. Notes on the development and larval forms of some Scandinavian echinoderms. Videnskabelige Meddelelser Danske Naturhistorisk Forening 71:133160.Google Scholar
Mortensen, T. 1921. Studies on the Development and Larval Forms of Echinoderms. G. E. C. Gad; Copenhagen.Google Scholar
Mortensen, T. 1927. On the postlarval development of some cidaroids. Kongelige Danske Videnskabernes Selskab, Skrifter Naturvidenskabelig og Mathematisk Afdeling, Series 8, 11:368387.Google Scholar
Mortensen, T. 1928. A Monograph of the Echinoidea I. Cidaroidea. C. A. Reitzel; Copenhagen.Google Scholar
Mortensen, T. 1931. Contributions to the study of the development and larval forms of echinoderms I-II. Kongelige Danske Videnskabernes Selskab, Skrifter Naturvidenskabelig og Mathematisk Afdeling, Series 9, 4(1):139.Google Scholar
Mortensen, T. 1936. Echinoidea and Ophiuroidea. Discovery Reports, Cambridge 12:199348.Google Scholar
Mortensen, T. 1937. Contibutions to the study of the development and larval forms of echinoderms III. Kongelige Danske Videnskabernes Selskab, Skrifter Naturvidenskabelig og Mathematisk Afdeling, Series 9, 7(1):165.Google Scholar
Mortensen, T. 1938. Contributions to the study of the development and larval forms of echinoderms IV. Kongelige Danske Videnskabernes Selskab, Skrifter Naturvidenskabelig og Mathematisk Afdeling, Series 9, 7(3):159.Google Scholar
Mortensen, T. 1940. A Monograph of the Echinoidea III (1) Aulodonta. C. A. Reitzel; Copenhagen.Google Scholar
Mortensen, T. 1943. A Monograph of the Echinoidea III (2) Camarodonta I. C. A. Reitzel; Copenhagen.Google Scholar
Mortensen, T. 1951. A Monograph of the Echinoidea V (2) Spatangoida II. C. A. Reitzel; Copenhagen.Google Scholar
Muller, A. H. 1970. Uber den sexualdimorphismus regularer Echinoidea (Echinodermata) der Oberkreide. Deutsche Akademie der Wissenschaften zu Berlin, Monatsberichte 12:923935.Google Scholar
Nye, O. B. Jr., Dean, D. A., and Hinds, R. W. 1972. Improved thin section techniques for fossil and recent organisms. Journal of Paleontology 46:271275.Google Scholar
Okazaki, K., and Inoue, S. 1976. Crystal property of the larval sea urchin spicule. Development, Growth, and Differentiation 18:413434.CrossRefGoogle ScholarPubMed
Okazaki, K., Dillaman, R. M., and Wilbur, K. M. 1981. Crystalline axes of the spine and test of the sea urchin Strongylocentrotus purpuratus: determination by crystal etching and decoration. Biological Bulletin 161:402415.Google Scholar
Olson, R. R., Cameron, J. L., and Young, C. M. 1988. Larval development of the pencil urchin Phyllacanthus imperialis: a lecithotrophic echinopluteus. P. 807. In Burke, R. D., Mladenov, P. V., Lambert, P., and Parsley, R. L. (eds.), Echinoderm Biology, Proceedings of the Sixth International Echinoderm Conference, Victoria, August 1987. Balkema Press; Rotterdam.Google Scholar
Onoda, K. 1936. Notes on the development of some Japanese echinoids with special reference to the structure of the larval body. Japanese Journal of Zoology 6:637654.Google Scholar
Onoda, K. 1938. Notes on the development of some Japanese echinoids with special reference to the structure of the larval body. Report II. Japanese Journal of Zoology 8:113.Google Scholar
Parks, A. L., Parr, B. A., Chin, J.-E., Leaf, D. S., and Raff, R. A. 1988. Molecular analysis of heterochronic changes in the evolution of direct developing sea urchins. Journal of Evolutionary Biology 1:2744.Google Scholar
Perron, F. E., and Kohn, A. J. 1986. Larval dispersal and geographic distribution in coral reef gastropods of the genus Conus. Proceedings of the Fifth International Coral Reef Symposium 4:95100.Google Scholar
Raff, R. A. 1987. Constraint, flexibility, and phylogenetic history in the evolution of direct development in sea urchins. Developmental Biology 119:619.Google Scholar
Ralston, M. 1985. PAR, derivative-free nonlinear regression. Pp. 305313. In Dixon, W. J. (chief ed.), BMDP Statistical Software Manual. University of California Press; Berkeley.Google Scholar
Raup, D. M. 1962. The phylogeny of calcite crystallography in echinoids. Journal of Paleontology 36:793810.Google Scholar
Raup, D. M. 1965. Crystal orientations in the echinoid apical system. Journal of Paleontology 39:934951.Google Scholar
Raup, D. M. 1966a. The endoskeleton. Pp. 379395. In Boolootian, R. A. (ed.), Physiology of Echinodermata. Interscience Publishers; New York.Google Scholar
Raup, D. M. 1966b. Crystallographic data for echinoid coronal plates. Journal of Paleontology 40:555568.Google Scholar
Scheltema, R. S. 1977. Dispersal of marine invertebrate organisms: paleobiogeographic and biostratigraphic implications. Pp. 73108. In Kauffman, E. G., and Hazel, J. E. (eds.), Concepts and Methods of Biostratigraphy. Hutchinson and Ross, Incorporated; Stroudsburg, Pennsylvania.Google Scholar
Scheltema, R. S. 1978. On the relationship between dispersal of pelagic veliger larvae and the evolution of marine prosobranch gastropods. Pp. 303321. In Battaglia, B., and Beard-more, J. A. (eds.), Marine Organisms. Plenum Press; New York.Google Scholar
Scheltema, R. S., and Williams, I. P. 1983. Long distance dispersal of planktonic larvae and the biogeography and evolution of some Polynesian and Western Pacific mollusks. Bulletin of Marine Science 33:545565.Google Scholar
Shearer, C., de Morgan, W., and Fuchs, H. M. 1913. On the experimental hybridization of echinoids. Philosophical Transactions of the Royal Society, London 204:255362.Google Scholar
Shuto, T. 1974. Larval ecology of prosobranch gastropods and its bearing on biogeography and paleontology. Lethaia 7:239256.Google Scholar
Smith, A. B. 1984. Echinoid Palaeobiology. George Allen and Unwin; London.Google Scholar
Sokal, R. R., and Rohlf, F. J. 1981. Biometry. Second Edition. W. H. Freeman and Company; New York.Google Scholar
Strathmann, R. R. 1979. Echinoid larvae from the northeast Pacific (with a key and comment on an unusual type of planktotrophic development). Canadian Journal of Zoology 57:610616.Google Scholar
Stephens, R. E. 1972. Studies on the development of the sea urchin Strongylocentrotus droebachiensis. I. Ecology and normal development. Biological Bulletin 142:132144.Google Scholar
Tennent, D. H. 1914. The early influence of the spermatozoan upon the characters of echinoid larvae. Carnegie Institute of Washington Publication 182:129138.Google Scholar
Tennent, D. H. 1929. Early development land larval forms of three echinoids of the Torres Strait region. Papers of the Tortugas Laboratory 26:115128.Google Scholar
Tyler, P. A., and Gage, J. D. 1984a. The reproductive biology of echinothurid and cidarid sea urchins from the deep sea (Rockall Trough, N.E. Atlantic Ocean). Marine Biology 80:6374.Google Scholar
Tyler, P. A., and Gage, J. D. 1984b. Seasonal reproduction of Echinus affinis in the Rockall Trough, northeast Atlantic Ocean. Deep Sea Research 31:387402.Google Scholar
Ubisch, L. von. 1913. Die Entwicklung von Strongylocentrotus lividus. (Echinus microtuberculatus, Arbacia pustulosa). Zeitschrift fur Wissenschaftliche Zoologie 106:409448.Google Scholar
Williams, D. H. C., and Anderson, D. T. 1975. The reproductive system, embryonic development, larval development, and metamorphosis of the sea urchin Heliocidaris erythrogramma (Val.) (Echinoidea, Echinometridae). Australian Journal of Zoology 23:371403.Google Scholar
Young, C. M., and Cameron, J. L. 1988. Larval forms and developmental rates of some bathyal echinoderms. P. 818. In Burke, R. D., Mladenov, P. V., Lambert, P., and Parsley, R. L. (eds.), Echinoderm Biology, Proceedings of the Sixth International Echinoderm Conference, Victoria, August 1987. Balkema Press; Rotterdam.Google Scholar