Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T10:44:25.592Z Has data issue: false hasContentIssue false

The evolution of larval morphology during the post-Paleozoic radiation of echinoids

Published online by Cambridge University Press:  08 February 2016

Gregory A. Wray*
Affiliation:
Department of Zoology, and Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington 98250

Abstract

The post-Paleozoic radiation of echinoids entailed a rapid diversification not only of adult morphology, but also of larval morphology. The timing, order, and phylogenetic distribution of evolutionary transformations in echinopluteus larvae are reconstructed here under maximum parsimony assumptions from a large neontological data base. Many echinoid larval apomorphies apparently evolved within the Paleozoic stem lineage and were subsequently retained during much of the crown-group radiation. This suite of apomorphies includes most (and perhaps all) of the skeletal elements and some features of soft anatomy such as vibratile lobes. Other features apparently arose or were modified during the post-Paleozoic radiation. These include skeletal features such as arm-rod structure and length, and soft structures such as epaulettes and skeletal muscles. Transformational hypotheses of this kind can be supported or rejected with further neontological data, and many can potentially be tested from fossil evidence. Many post-Paleozoic transformations in echinopluteus structure may be adaptive. For example, increases in arm length and flattening of arm ectoderm may increase feeding rate and efficiency, and both types of transformation have occurred several times within the crown group. Relational hypotheses of this nature can be tested through comparative functional studies in extant echinoplutei. Parallel evolutionary losses of feeding in echinoplutei are accompanied by loss or modification of characteristic structures. This suggests that developmental constraints do not fully explain the conservation of these structures in planktotrophic echinoplutei. Comparisons of larval and adult morphology over congruent time intervals demonstrate that the origin of many orders was accompanied by a suite of synapomorphies in larval morphology that was subsequently conserved. Many details of echinopluteus morphology are therefore of taxonomic significance. Intraordinal patterns of larval diversity, however, vary considerably. That larval morphology has diversified independently of adult morphology indicates that mosaic evolution has occurred within the life cycle and suggests that echinoid larvae and adults can and do respond to selection independently. Taken together, these findings underscore the complex ways in which complex life cycles can evolve.

Type
Articles
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Alberch, P. 1980. Ontogenesis and morphological diversification. American Zoologist 20:653667.CrossRefGoogle Scholar
Allmon, W. D., and Ross, R. M. 1990. Specifying causal factors in evolution: the paleontological contribution. Pp. 117in Ross, R. M. and Allmon, W. D., eds. Causes of evolution: a paleontological perspective. University of Chicago Press, Chicago.Google Scholar
Baum, D. A., and Larson, A. 1991. Adaptation reviewed: a phylogenetic methodology for studying character evolution. Systematic Zoology 40:118.CrossRefGoogle Scholar
Boidron-Metairon, I. F. 1988. Morphological plasticity in laboratory-reared echinoplutei of Dendraster excentricus (Eschscholtz) and Lytechinus pictus (Lamarck) in response to food conditions. Journal of Experimental Marine Biology and Ecology 119:3141.CrossRefGoogle Scholar
Chia, F.-S., Buckland-Nicks, J., and Young, C. M. 1984. Locomotion of marine invertebrate larvae: a review. Canadian Journal of Zoology 62:12051222.CrossRefGoogle Scholar
Coddington, J. A. 1988. Cladistic tests of adaptational hypotheses. Cladistics 4:322.CrossRefGoogle ScholarPubMed
DeBeer, G. 1958. Embryos and ancestors. Clarendon Press, Oxford.Google Scholar
Deflandre-Rigaud, M. 1946. Vestiges microscopiques des larves d'echinodermes de l'Oxfordian de Villers-sur-Mer. 222:908910.Google Scholar
Denny, M. W. 1988. Biology and the mechanics of the wave-swept environment. Princeton University Press, Princeton, N.J.CrossRefGoogle Scholar
Durham, J. W. 1955. Classification of clypeasteroid echinoids. University of California Publications in Geological Sciences 31:73198.Google Scholar
Durham, J. W., Fell, H. B., Fischer, A. G., Kier, P. M., Melville, R. V., Pawson, D. L., and Wagner, C. D. 1966. Echinoids. Pp. U211U695in Durham, J. W. et al., eds. Treatise on invertebrate paleontology, Part U, Echinodermata 3. Geological Society of America, Boulder, Colo., and University of Kansas Press, Lawrence, Kans.Google Scholar
Emlet, R. B. 1982. Echinoderm calcite: a mechanical analysis from larval spicules. Biological Bulletin 163:264275.CrossRefGoogle Scholar
Emlet, R. B. 1988. Larval form and metamorphosis of a “primitive” sea urchin, Eucidaris thouarsi (Echinodermata: Echinoidea: Cidaroida), with implications for developmental and phylogenetic studies. Biological Bulletin 174:419.CrossRefGoogle ScholarPubMed
Emlet, R. B. 1990. World patterns of developmental mode in echinoid echinoderms. Pp. 329335in Hoshi, M. and Yamashita, O., eds. Advances in invertebrate reproduction 5. Elsevier, Amsterdam.Google Scholar
Emlet, R. B. 1991. Functional constraints on the evolution of larval forms of marine invertebrates: experimental and comparative evidence. American Zoologist 31:707725.CrossRefGoogle Scholar
Emlet, R. B., McEdward, L. R., and Strathmann, R. R. 1987. Echinoderm larval ecology viewed from the egg. Echinoderm Studies 2:55136.Google Scholar
Fell, H. B. 1946. The embryology of the viviparous ophiuroid Amphipholis squamata Delle Chiaje. Transactions of the Royal Society of New Zealand 75:419464.Google Scholar
Fell, H. B. 1948. Echinoderm embryology and the origin of chordates. Biological Reviews 23:81107.CrossRefGoogle ScholarPubMed
Fitch, W. M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology 20:406416.CrossRefGoogle Scholar
Garstang, W. 1929. The origin and evolution of larval forms. British Association for the Advancement of Science 1929:7798.Google Scholar
Gordon, I. 1929. Skeletal development in Arbacia, Echinarachnius and Leptasterias. Philosophical Transactions of the Royal Society, London B 216:289334.Google Scholar
Grave, C. 1902. Some points in the structure and development of Mellita testudinata. Johns Hopkins University Circulars 157:18.Google Scholar
Grave, C. 1903. On the occurrence among echinoderms of larvae with cilia arranged in transverse rings, with a suggestion as to their significance. Biological Bulletin 5:169186.CrossRefGoogle Scholar
Hagedoorn, A. L. 1909. On the purely motherly character of the hybrids produced from the eggs of Strongylocentrotus. Archiv für Entwickslungsmechanik der Organismen 27:120.CrossRefGoogle Scholar
Hansen, T. 1980. Influence of larval dispersal and geographic distribution on species longevity in neogastropods. Paleobiology 6:193207.CrossRefGoogle Scholar
Hart, M. 1991. Particle capture and the method of suspension feeding by echinoderm larvae. Biological Bulletin 180:1227.CrossRefGoogle ScholarPubMed
Hart, M., and Scheibling, R. E. 1988. Comparing shapes of echinoplutei using principal components analysis, with an application to larvae of Strongylocentrotus droebachiensis. Pp. 277284in Burke, R. D., Mladenov, P. V., Lambert, P., and Parsley, R. L., eds. Echinoderm biology: Proceedings of the sixth International Echinoderm Conference. Balkema, Amsterdam.Google Scholar
Harvey, P. H., and Purvis, A. 1991. Comparative methods for explaining adaptations. Nature (London) 351:619624.CrossRefGoogle ScholarPubMed
Hendler, G. 1982. An echinoderm vitellaria with a bilateral larval skeleton: evidence for the evolution of ophiuroid vitellariae from ophioplutei. Biological Bulletin 163:431437.CrossRefGoogle 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 marine benthic invertebrates: paleobiological implications. Biological Reviews 58:2189.CrossRefGoogle Scholar
Jägersten, G. 1972. Evolution of the metazoan life cycle. Academic Press, London.Google Scholar
Kidwell, S., and Baumiller, T. 1990. Experimental disintegration of regular echinoids: roles of temperature, oxygen, and decay thresholds. Paleobiology 16:247271.CrossRefGoogle Scholar
Kier, P. M. 1965. Evolutionary trends in Paleozoic echinoids. Journal of Paleontology 39:436465.Google Scholar
Kier, P. M. 1969. Sexual dimorphism in fossil echinoids. Pp. 215222in Westerman, G.E.G., ed. Sexual dimorphism in fossil metazoa and taxonomic implications. Schweizerbartsche Verlagsbuchhandlung, Stuttgart.Google Scholar
Kier, P. M. 1974. Evolutionary trends and their functional significance in the post-Paleozoic echinoids. Paleontological Society Memoir 5 (Journal of Paleontology 48, suppl.):196.Google Scholar
Kier, P. M. 1977. Triassic echinoids. Smithsonian Contributions to Paleobiology 30:188.CrossRefGoogle Scholar
Kier, P. M. 1984. Echinoids from the Triassic (St. Cassian) of Italy, their lantern supports, and a revised phylogeny of Triassic echinoids. Smithsonian Contributions to Paleobiology 56:141.Google Scholar
Kryuchkova, G. A., and Solov'yev, A. N. 1975. The larval stages of echinoids. Paleontological Journal (Paleontologicheskii Zhurnal) 9:487493.Google Scholar
Lacalli, T. C., and Gilmour, T.H.J. 1990. Ciliary reversal and locomotory control in the pluteus larva of Lytechinus pictus. Philosophical Transactions of the Royal Society, London B 330:391396.Google Scholar
Lauder, G. V. 1981. Form and function: structural analysis in evolutionary morphology. Paleobiology 7:430442.CrossRefGoogle Scholar
Lauder, G. V. 1990. Functional morphology and systematics: studying functional patterns in an historical context. Annual Review of Ecology and Systematics 21:317340.CrossRefGoogle Scholar
Levinton, J. S. 1988. Genetics, paleontology, and macroevolution. Cambridge University Press, Cambridge.Google Scholar
Lewis, D. N., and Ensom, P. C. 1982. Archaeocidaris whatleyensis sp. nov. (Echinoidea) from the Carboniferous limestone of Somerset, and notes on echinoid phylogeny. Bulletin of the British Museum of Natural History (Geology) 36:77104.Google Scholar
Maddison, W. P., and Maddison, D. R. 1987. MacClade, version 2.01. Distributed by the authors.Google Scholar
Maddison, W. P., Donoghue, M. J., and Maddison, D. R. 1984. Outgroup analysis and parsimony. Systematic Zoology 33:83103.CrossRefGoogle Scholar
McEdward, L. R. 1984. Morphometric and metabolic analysis of the growth and form of an echinopluteus. Journal of Experimental Marine Biology and Ecology 82:259287.CrossRefGoogle Scholar
McEdward, L. R. 1985. Effects of temperature on the body form, growth, electron transport system activity, and development rate of an echinopluteus. Journal of Experimental Marine Biology and Ecology 93:169181.CrossRefGoogle Scholar
McEdward, L., and Strathmann, R. R. 1987. The body plan of the cyphonautes larva of bryozoans prevents high clearance rates: comparison with the pluteus and a growth model. Biological Bulletin 172:3045.CrossRefGoogle Scholar
Medes, G. 1917. A study of the causes and the extent of variations in the larvae of Arbacia punctulata. Journal of Morphology 30:317432.CrossRefGoogle Scholar
Mladenov, P. V. 1979. Unusual lecithotrophic development of the Caribbean brittle star Ophiothrix oerstedi. Marine Biology 55:5562.CrossRefGoogle Scholar
Mooi, R. 1989. Living and fossil genera of the Clypeasteroida (Echinoidea: Echinodermata): an illustrated key and annotated checklist. Smithsonian Contributions to Zoology 488:151.CrossRefGoogle Scholar
Mooi, R. 1990. Paedomorphosis, Aristotle's lantern, and the origin of the sand dollars (Echinodermata: Clypeasteroida). Paleobiology 16:2548.CrossRefGoogle Scholar
Mortensen, T. 1921. Studies of the development and larval forms of echinoderms. G.E.C. Gad, Copenhagen.CrossRefGoogle Scholar
Mortensen, T. 1928-1951. A monograph of the Echinoidea, vols. I to V. 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. 1937. Contributions to the study of the development and larval forms of echinoderms. III. Kongelige Danske Videnskabernes Selskab, Skrifter Naturvidenskabelig og Mathematisk Afdeling, Ser. 9, 7(1):165.Google Scholar
Neilsen, C. 1987. Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zoologica 68:205262.CrossRefGoogle Scholar
Okazaki, K. 1975. Normal development to metamorphosis. Pp. 177232in Czihak, G., ed. The sea urchin embryo. Springer, Berlin.CrossRefGoogle Scholar
Pennington, J. T., and Strathmann, R. R. 1990. Consequences of the calcite skeleton of planktonic echinoderm larvae for orientation, swimming, and shape. Biological Bulletin 179:121133.CrossRefGoogle ScholarPubMed
Pennington, J. T., Rumrill, S. S., and Chia, F.-S. 1986. Stage-specific predation upon embryos and larvae of the Pacific sand dollar, Dendraster excentricus, by 11 species of common zooplankton predators. Bulletin of Marine Science 39:234240.Google Scholar
Philip, G. M., and Foster, R. J. 1971. Marsupiate Tertiary echinoids from southeastern Australia and their zoogeographic significance. Paleontology 14:666695.Google Scholar
Raff, R. A. 1987. Constraint, flexibility, and phylogenetic history in the evolution of direct development in sea urchins. Developmental Biology 119:619.CrossRefGoogle ScholarPubMed
Roughgarden, J. 1989. The evolution of marine life cycles. Pp. 271300in Feldman, M. W., ed. Mathematical evolutionary theory. Princeton University Press, Princeton, N.J.Google Scholar
Rumrill, S. 1990. Natural mortality of marine invertebrate larvae. Ophelia 32:163198.CrossRefGoogle Scholar
Rumrill, S., and Chia, F.-S. 1984. Differential mortality during the embryonic and larval lives of northeast Pacific echinoids. Pp. 333338in Keegan, B. F. and O'Connor, B.D.S., eds. Echinodermata: Proceedings of the fifth International Echinoderm Conference. Balkema, Amsterdam.Google Scholar
Seilacher, A. 1979. Constructional morphology of sand dollars. Paleobiology 5:191221.CrossRefGoogle Scholar
Smith, A. B. 1984a. Classification of the Echinodermata. Paleontology 27:431459.Google Scholar
Smith, A. B. 1984b. Echinoid paleobiology. Allen & Unwin, London.Google Scholar
Smith, A. B. 1988a. Phylogenetic relationship, divergence times, and rates of molecular evolution for camarodont sea urchins. Molecular Biology and Evolution 5:345365.Google Scholar
Smith, A. B. 1988b. Fossil evidence for the relationship of extant echinoderm classes and their times of divergence. Pp. 8597in Paul, C.R.C. and Smith, A. B., eds. Echinoderm phylogeny and evolutionary biology. Clarendon, Oxford.Google Scholar
Smith, A. B. 1989. RNA sequence data in phylogenetic reconstruction: testing the limits of its resolution. Cladistics 5:321344.CrossRefGoogle ScholarPubMed
Smith, A. B., and Hollingworth, N.T.J. 1990. Tooth structure and phylogeny of the Upper Permian echinoid Miocidaris keyserlingi. Proceedings of the Yorkshire Geological Society 48:4760.CrossRefGoogle Scholar
Strathmann, R. R. 1971. The feeding behavior of planktotrophic echinoderm larvae: mechanisms, regulation, and rates of suspension feeding. Journal of Experimental Marine Biology and Ecology 6:109160.CrossRefGoogle Scholar
Strathmann, R. R. 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894906.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Strathmann, R. R. 1980. Why does a larva swim so long? Paleobiology 6:373376.CrossRefGoogle Scholar
Strathmann, R. R. 1985. Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Annual Review of Ecology and Systematics 16:339361.CrossRefGoogle Scholar
Strathmann, R. R. 1988a. Larvae, phylogeny, and von Baer's law. Pp. 5367in Paul, C.R.C. and Smith, A. B., eds. Echinoderm phylogeny and evolutionary biology. Clarendon, Oxford.Google Scholar
Strathmann, R. R. 1988b. Functional requirements and the evolution of developmental patterns. Pp. 5561in Burke, R. D., Mladenov, P. V., Lambert, P., and Parsley, R. L., eds. Echinoderm biology: proceedings of the sixth International Echinoderm Conference. Balkema, Amsterdam.Google Scholar
Strathmann, R. R. 1989. Existence and functions of a gel-filled primary body cavity in development of echinoderms and hemichordates. Biological Bulletin 176:2531.CrossRefGoogle Scholar
Strathmann, R. R., Fenaux, L., and Strathmann, M. F. 1992. Heterochronic developmental plasticity in larval sea urchins and its implications for evolution of non-feeding larvae. Evolution, in press.CrossRefGoogle Scholar
Swofford, D. L., and Maddison, W. P. 1987. Reconstructing ancestral states under Wagner parsimony. Mathematical Biosciences 87:199229.CrossRefGoogle Scholar
Taylor, P. D. 1988. Major radiation of cheilostome bryozoans: triggered by the evolution of a new larval type? Journal of Historical Biology 1:4564.CrossRefGoogle Scholar
Tennant, D. H. 1910. Variation in echinoid plutei. Journal of Experimental Biology 9:675.Google Scholar
Valentine, J. W., and Jablonski, D. 1983. Larval adaptations and patterns of brachiopod diversity in space and time. Evolution 37:10521061.CrossRefGoogle ScholarPubMed
Wray, G. A. 1992. Rates of evolution in developmental processes. American Zoologist 32:123134.CrossRefGoogle Scholar
Wray, G. A., and Raff, R. A. 1990. Novel origins of lineage founder cells in the direct-developing echinoid Heliocidaris erythrogramma. Developmental Biology 141:4154.CrossRefGoogle Scholar
Wray, G. A., and Raff, R. A. 1991. The evolution of developmental strategy in marine invertebrates. Trends in Ecology and Evolution 6:4550.CrossRefGoogle ScholarPubMed

Echinopluteus Anatomy Bibliography

Agassiz, A. 1864. Embryology of echinoderms. Memoirs of the American Academy of Arts and Sciences 9.CrossRefGoogle Scholar
Aiyar, R. G. 1935. Early development and metamorphosis of the tropical echinoid Salmacis bicolor, Agassiz. Proceedings of the Indian Academy of Sciences B 1:714731.CrossRefGoogle Scholar
Arrau, L. 1958. Desarrollo del erizo comestible de Chile Loxechinus albus Mol. Revista de Biologia Marina 7:3961.Google Scholar
Bernasconi, I. 1942. Primeros estados larveles de Arbacia dufresnei (Blv.). Physis (Buenos Aires) 19:305312.Google Scholar
Bisgrove, B. W., and Burke, R. D. 1987. Development of the nervous system of the pluteus larva of Strongylocentrotus droebachiensis. Cell and Tissue Research 248:335343.CrossRefGoogle Scholar
Bosch, I., Beauchamp, K., 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.CrossRefGoogle ScholarPubMed
Caldwell, J. W. 1972. Development, metamorphosis, and substrate selection of the larvae of the sand dollar Mellita quinquiesperforata (Leske, 1778). Master's thesis, University of Florida, Gainesville.Google Scholar
Cameron, R. A., and Hinegardner, R. T. 1978. Early events in sea urchin metamorphosis, description and analysis. Journal of Morphology 157:2132.CrossRefGoogle ScholarPubMed
Cram, D. L. 1971a. Life history studies on South African echinoids (Echinodermata). 1. Parechinus angulosus (Leske) (Echinidae, Parechininae). Transactions of the Royal Society of South Africa 39:321337.CrossRefGoogle Scholar
Cram, D. L. 1971b. Life history studies on South African echinoids (Echinodermata) 2. Echinolampas (Paleolampas) crassa (Bell) (Echinolampadidae). Transactions of the Royal Society of South Africa 39:339352.CrossRefGoogle Scholar
DeGreef, Y. 1983. Mise en place des structures squelettiques larvaires chez l'oursin Paracentrotus lividus (Lamarck) (Echinodermata, Echinoidea: Echinidae). Thesis, Université Libre de Bruxelles.Google Scholar
Dix, T. G. 1969. Larval life span of the echinoid Evechinus chloroticus (Val.). New Zealand Journal of Marine and Freshwater Research 3:1316.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) (Clypeasteroida: Echinoidea). Journal of Experimental Marine Biology and Ecology 95:183202.CrossRefGoogle Scholar
Emlet, R. B. 1988. Larval form and metamorphosis of a “primitive” sea urchin, Eucidaris thouarsi (Echinodermata: Echinoidea: Cidaroida), with implications for developmental and phylogenetic studies. Biological Bulletin 174:419.CrossRefGoogle ScholarPubMed
Falk-Petersen, I. 1983. Light and electron microscopical studies of the embryonic development of Strongylocentrotus pallidus (G. O. Sars). Sarsia 68:920.CrossRefGoogle Scholar
Feliciano, A. T. 1933. Studies on the early development of Arachnoides placenta. Natural and Applied Sciences Bulletin, University of the Philippines 3:405435.Google Scholar
Fenaux, L. 1969. Les échinoplutéus de la Méditerranée. Bulletin de l'Institut Océanographique, Monaco. No. 1394.Google Scholar
Fenaux, L. 1972. Contribution à la connaissance des larves de Spatangides en Méditerranée: Echinocardium mediterraneum (Forb.) et Spatangus purpureus (O. F. M.). Bulletin du Muséum National D'Historie Naturelle 3:297304.Google Scholar
Fewkes, J. W. 1893. Preliminary observations on the development of Ophiopholis and Echinarachnius. Bulletin of the Museum of Comparative Zoology 12:105152.Google Scholar
Fukushi, T. 1959. On the cell mass observed on the left side of the pluteus of the sea urchin, Temnopleurus hardwickii. Bulletin of the Marine Biological Station of Asamushi 9:133135.Google Scholar
Fukushi, T. 1960a. The external features of development of the sea urchin, Glyptocidaris crenularis A. Agassiz. Bulletin of the Marine Biological Station of Asamushi 10:5763.Google Scholar
Fukushi, T. 1960b. The formation of the echinus rudiment and the development of the larval form in the sea urchin, Temnopleurus hardwickii. Bulletin of the Marine Biological Station of Asamushi 10:6572.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. Skeletal development in Arbacia, Echinarachnius and Leptasterias. Philosophical Transations of the Royal Society of London B 216:289334.Google Scholar
Grave, C. 1902. Some points in the structure and development of Mellita testudinata. Johns Hopkins University Circulars 157:18.Google Scholar
Hagedoorn, A. L. 1909. On the purely motherly character of the hybrids produced from the eggs of Strongylocentrotus. Archiv für Entwickslungsmechanik der Organismen 27:120.CrossRefGoogle Scholar
Harold, A. S., and Telford, M. 1990. Systematics, phylogeny and biogeography of the genus Mellita (Echinoidea: Clypeasteroida). Journal of Natural History 24:9871026.CrossRefGoogle Scholar
Harvey, E. B. 1949. The growth and metamorphosis of the Arbacia punctulata pluteus, and late development of the white halves of centrifuged eggs. Biological Bulletin 97:287299.CrossRefGoogle ScholarPubMed
Hinegardner, R. T. 1969. Growth and development of the laboratory cultured sea urchin. Biological Bulletin 137:465475.CrossRefGoogle ScholarPubMed
Hinegardner, R. T. 1975. Morphology and genetics of sea urchin development. American Zoologist 15:679689.CrossRefGoogle Scholar
Johnson, M. W. 1930. Notes on the larval development of Strongylocentrotus franciscanus. Publications of the Puget Sound Biological Station 7:401411.Google Scholar
Johnson, M. W., and Johnson, L. T. 1950. Early life history and larval development of some Puget Sound echinoderms. Contributions of the Scripps Institute of Oceanography New Series no. 439:7484.Google Scholar
Kasyanov, V. L., Kryuchkova, G. A., Kulikova, V. A., and Medvedeva, L. A. 1983. Larvae of marine bivalve molluscs and echinoderms. [In Russian.]Nauka, Moscow.Google Scholar
Kawamura, K. 1970. On the development of the planktonic larvae of Japanese sea urchins S. intermedius and S. nudus. Scientific Reports of the Hokkaido Fisheries Experimental Station 12:2532.Google Scholar
Krohn, A. 1853a. Über die Larve von Spatangus purpureus. Müller's Archiv Anatomie und Physiologie 1853:255259.Google Scholar
Krohn, A. 1853b. Über die Larve des Echinus brevispinosus. Müller's Archiv Anatomie und Physiologie 1853:361364.Google Scholar
Kryuchkova, G. A. 1976. Morphology of the larval skeleton of sea urchins from the Sea of Japan. [In Russian with English abstract.]Marine Biology (Vladivostok) 4:4554.Google Scholar
Kryuchkova, G. A. 1979. Development of the definitive skeleton of heart urchin Echinocardium cordatum. [In Russian with English abstract.]Marine Biology (Vladivostok) 6:3543.Google Scholar
Lewis, J. B. 1958. The biology of the tropical sea urchin Tripneustes esculentus Leske in Barbados, British West Indies. Canadian Journal of Zoology 36:607621.CrossRefGoogle Scholar
MacBride, E. W. 1899. The development of echinoids. Part I. The larvae of Echinus miliaris and Echinus esculentus. Quarterly Journal of Microscopical Science 42:335339.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. Part I, the external features of the development. Quarterly Journal of Microscopical Science 59:471486.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
Moore, A. R. 1959. On the embryonic development of the sea urchin Allocentrotus fragilis. Biological Bulletin 117:7583.Google Scholar
Moore, M. M. 1933. Notes on the development of the sea urchin Temnopleurus hardwickii. Scientific Reports of Tôhuku Imperial University, Biology 8:263276.Google Scholar
Mortensen, T. 1913. On the development of some British echinoderms. Journal of the Marine Biological Association of the United Kingdom 10:118.CrossRefGoogle Scholar
Mortensen, T. 1914a. Die Echinodermlarven der Deutschen Südpolar-Expedition. Deutschen Südpolar-Expedition 1901-1903. XIV:67111.Google Scholar
Mortensen, T. 1914b. On the development of some Japanese echinoderms. Annotations Zoologicae Japonensis 8.Google Scholar
Mortensen, T. 1920. Notes on the development and larval forms of some Scandinavian echinoderms. Videnskabelige Meddelelser Dansk Naturhistorisk Forening Kjobenhaven 71:133160.Google Scholar
Mortensen, T. 1921. Studies on the development and larval forms of echinoderms. G.E.C. Gad, Copenhagen.CrossRefGoogle 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. 1937. Contributions 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(2);159.Google Scholar
Müller, H. 1854. Über die Gattungen der Seeigellarven. Siebente Abhandlung über die Metamorphose der Echinodermen. Abhandlungen der Koniglicher Akademie der Wissenschaften zu Berlin 1853:153.Google Scholar
Okazaki, K. 1975. Normal development to metamorphosis. Pp. 177232in Czihak, G., ed. The sea urchin embryo. Springer, Berlin.CrossRefGoogle Scholar
Onoda, K. 1931. Notes on the development of Heliocidaris crassispina with special reference to the structure of the larval body. Memoirs of the College of Science, Kyoto Imperial University B 7:103134.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
Pennington, J. T., and Strathmann, R. R. 1990. Consequences of the calcite skeletons of planktonic echinoderm larvae for orientation, swimming, and shape. Biological Bulletin 179:121133.CrossRefGoogle ScholarPubMed
Pressoir, L. 1959. Contribution à la connaissance des échinoplutéus de Paracentrotus lividus Lmck., et Psammechinus microtuberculatus Blainv. Bulletin de l'Institut Oceanographique, Monaco. 1142.Google Scholar
Prouho, H. 1887. Recherches sur de Dorocidaris papillata et quelques autres échinides de la Méditerranée. Archives Zoologie Experimental et Génerale Ser. 2 5:213380.Google Scholar
Rees, C. B. 1953. The larvae of the Spatangidae. Journal of the Marine Biological Association of the United Kingdom 32:477490.CrossRefGoogle Scholar
Runnström, S. 1929. Eine neue Spatangidlarve von der Westküste Norwegens. Bergens Museums Årbok, Naturvidenskapelig Rekke 9:19.Google Scholar
Schroeder, T. E. 1981. Development of a “primitive” sea urchin (Eucidaris tribuloides): irregularities in the hyaline layer, micromeres, and primary mesenchyme. Biological Bulletin 161:141151.CrossRefGoogle Scholar
Shearer, C., DeMorgan, W., and Fuchs, H. M. 1914. On the experimental hybridization of echinoids. Philosophical Transactions of the Royal Society, London B 204:255362.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.CrossRefGoogle Scholar
Tennant, D. H. 1910. Variation in echinoid plutei. Journal of Experimental Zoology 9:657.CrossRefGoogle Scholar
Tennant, D. H. 1922. Studies on the hybridization of echinoids, Cidaris tribuloides. Carnegie Institute of Washington Publication 312:142.Google Scholar
Tennant, D. H. 1929. Early development and larval forms of three echinoids of the Torres Strait region. Carnegie Institute of Washington Publication 26:115128.Google Scholar
Théel, H. 1892. On the development of Echinocyamus pusillus. Nova Acta Regiae Societati Scientarum Upsaliensis, Ser III 15:157.Google Scholar
Young, C. M., Cameron, J. L., and Eckelbarger, K. J. 1989. Extended pre-feeding period in the planktotrophic larvae of the bathyal echinoid Aspidodiadema jacobyi. Journal of the Marine Biological Association, United Kingdom 69:695702.CrossRefGoogle Scholar