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Extinction selectivity and ecology of Neogene Caribbean reef corals

Published online by Cambridge University Press:  08 February 2016

Kenneth G. Johnson
Affiliation:
Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom
Ann F. Budd
Affiliation:
Geology Department, The University of Iowa, Iowa City, Iowa 52242 U.S.A.
Thomas A. Stemann
Affiliation:
Geologisches Institut, Universität Bern, Baltzerstrasse 1, CH-3012 Bern, Switzerland

Abstract

We analyze a new compilation of Neogene to Recent (22-0 Ma) Caribbean coral occurrences to determine how ecological and life history traits at the population level affect long-term evolutionary patterns. The compilation consists of occurrences of 175 species and 49 genera in one continuous (> 5 m.y.) sequence and 22 scattered sites across the Caribbean region. Previous study of evolutionary rates using these data has shown that both extinction and origination were accelerated between 4 and 1 Ma, resulting in large-scale faunal turnover. Categories for three morphological and two reproductive variables (colony size, colony shape, and corallite size; and sex, and mode of embryonic development; respectively) are assigned to each species in the compilation. Comparisons of the ecological variables with evolutionary rates using randomization procedures and modified analysis of variance show that only colony size was strongly related to rates of extinction and origination during either normal background times or times of accelerated extinction. Extinction rates were lower in species with large colonies, because species with small massive colonies tend to live in small, short-lived populations with highly fluctuating recruitment rates. During turnover, extinction rates increased disproportionately in species with small colonies. Origination rates are found to be less related to ecological variables, although species with small massive colonies originated at higher rates prior to turnover.

Accelerated turnover may have therefore involved an increase in local population extinction rates that caused increased rates of both species extinction and origination across the entire fauna. Since extinction rates accelerated disproportionately with respect to colony size, the overall result was a relative increase in species with large colonies. After severe disturbance, one might expect that populations of species with large colonies and high rates of fragmentation would be more likely to escape extinction, because of larger population sizes, longer generation times, and more constant rates of population increase. The modern Caribbean reef-coral fauna is therefore structured by large, long-lived colonies that are robust to regional environmental change. Many of the very taxa that allowed reef communities to escape collapse in the past are declining today in response to anthropogenic disturbances, suggesting that Caribbean reef communities may be less resilient in the future in response to ongoing environmental perturbations.

Type
Research Article
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Allmon, W. D., Rosenberg, G., Portell, R. W., and Schindler, K. S. 1993. Diversity of Atlantic coastal plain mollusks since the Pliocene. Science 260:16261629.CrossRefGoogle ScholarPubMed
Arita, H. T., Robinson, J. G., and Redford, K. H. 1990. Rarity in neotropical forest mammals and its ecological correlates. Conservation Biology 4:181192.CrossRefGoogle Scholar
Babcock, R. C. 1984. Reproduction and distribution of two species of Goniastrea (Scleractinia) from the Great Barrier Reef province. Coral Reefs 2:187195.CrossRefGoogle Scholar
Barry, J. C., Flynn, L. J., and Pilbeam, D. R. 1990. Faunal diversity and turnover in a Miocene terrestrial sequence. Pp. 381421in Ross, R. M. and Allmon, W. D., eds. Causes of evolution. A paleontological perspective. University of Chicago Press.Google Scholar
Barton, N. H. 1989. Founder effect speciation. Pp. 229256in Otte, and Endler, 1989.Google Scholar
Bell, P. R. F., and Tomascik, T. 1993. The demise of the fringing coral reefs of Barbados and of regions in the Great Barrier Reef (GBR) lagoon—impacts of eutrophication. Pp. P1P7in Ginsburg, R. N., ed. Global aspects of coral reefs: health, hazards, and history. University of Miami Press.Google Scholar
Berggren, W. A., Kent, D. V., and Van Couvering, J. A. 1985. Neogene geochronology and chronostratigraphy. Pp. 211260in Snelling, N. J., ed. The chronology of the geological record. Geological Society of London, Memoir 10.Google Scholar
Boyajian, G. E. 1991. Taxon age and selectivity of extinction. Paleobiology 17:4957.CrossRefGoogle Scholar
Boyce, M. S. 1992. Population viability analysis. Annual Review of Ecology and Systematics 23:481506.CrossRefGoogle Scholar
Budd, A. F., and Coates, A. G. 1992. Non-progressive evolution in a clade of Cretaceous Montastraea-like corals. Paleobiology 15:425446.CrossRefGoogle Scholar
Budd, A. F., Johnson, K. G., and Potts, D. C. 1994a. Recognizing morphospecies in colonial reef corals: I. Landmark-based methods. Paleobiology 20:484505.CrossRefGoogle Scholar
Budd, A. F., Stemann, T. A., and Johnson, K. G. 1994b. Stratigraphic distributions of genera and species of Neogene to Recent Caribbean reef corals. Journal of Paleontology 68:951977.CrossRefGoogle Scholar
Budd, A. F., Johnson, K. G., and Stemann, T. A.In press. Plio-Pleistocene turnover and extinctions in the Caribbean reef coral fauna. In Jackson, J. B. C., Coates, A. G., and Budd, A. F., eds. Evolution and environment in tropical America over the last ten million years. University of Chicago Press.Google Scholar
Buddemeier, R. W., and Fautin, D. G. 1993. Coral bleaching as an adaptive mechanism. Bioscience 43:320326.CrossRefGoogle Scholar
Cheetham, A. H., and Jackson, J. B. C.In press. Speciation, extinction, and the decline of erect growth in Neogene and Quaternary cheilostome Bryozoa of tropical America. In Jackson, J. B. C., Coates, A. G., and Budd, A. F., eds. Evolution and environment in tropical America over the last ten million years. University of Chicago Press.Google Scholar
Coates, A. G., Jackson, J. B. C., Collins, L. S., Cronin, T. M., Dowsett, H. J., Bybel, L. M., Jung, P., and Obando, J. A. 1992. Closure of the Isthmus of Panama: the nearshore marine record of Costa Rica and western Panama. Geological Society of America Bulletin 104:814828.2.3.CO;2>CrossRefGoogle Scholar
Cotgreave, P. 1993. The relationship between body size and population abundance in animals. Trends in Ecology and Evolution 8:244248.CrossRefGoogle ScholarPubMed
Crame, J. A. 1986. Late Pleistocene molluscan assemblages from the coral reefs of the Kenya coast. Coral Reefs 4:183196.CrossRefGoogle Scholar
D'Elia, C. F., Buddemeier, R. W., and Smith, S. V. 1991. Workshop on coral bleaching, coral reef ecosystems, and global change: report of proceedings. Maryland Sea Grant College Publication no. UM-SG-TS-91-03.Google Scholar
Diamond, J. M. 1984. ‘Normal’ extinctions of isolated populations. Pp. 191245in Nitecki, M. H., ed. Extinctions. University of Chicago Press.Google Scholar
Done, T. J. 1983. Coral zonation: its nature and significance. Pp. 107147in Barnes, D. J., ed. Perspectives on coral reefs. Australian Institute of Marine Sciences, Brian Clouston Publisher, Manuka, Australia.Google Scholar
Eldredge, N. 1992. Where the twain meet: causal intersections between the genealogical and ecological realm. Pp. 114in Eldredge, N., ed. Systematics, ecology, and the biodiversity crisis. Columbia University Press, New York.Google Scholar
Endean, R., and Cameron, A. M. 1990. Trends and new perspectives in coral-reef ecology. Pp. 469492in Dubinsky, Z., ed. Coral reefs. Elsevier, New York.Google Scholar
Endler, J. A. 1989. Conceptual and other problems in speciation. Pp. 625648in Otte, and Endler, 1989.Google Scholar
Erwin, D. H. 1989. Regional paleoecology of Permian gastropod genera, southwestern United States and the end-Permian mass extinction. Palaios 4:424438.CrossRefGoogle Scholar
Erwin, D. H. 1993. The Great Paleozoic Crisis: life and death in the Permian. Columbia University Press, New York.Google Scholar
Fahrig, L., and Merriam, G. 1994. Conservation of fragmented populations. Conservation Biology 8:5059.CrossRefGoogle Scholar
Flessa, K. W., and Thomas, R. H. 1985. Modeling the biogeographic regulation of evolutionary rates. Pp. 355376in Valentine, J., ed. Phanerozoic diversity patterns. Princeton University Press.Google Scholar
Flessa, K. W., et al. 1986. Causes and consequences of extinction: group report. Pp. 235257in Raup, D. M. and Jablonski, D., eds. Patterns and processes in the history of life. Springer-Verlag, Berlin.Google Scholar
Frost, S. H. 1977. Miocene to Holocene evolution of Caribbean province reef-building corals. Proceedings of the Third International Coral Reef Symposium 2:353360.Google Scholar
Gilpin, M. E. 1987. Spatial structure and population vulnerability. Pp. 125139in Soulé, M. E., ed. Viable populations for conservation. Cambridge University Press.CrossRefGoogle Scholar
Goodman, D. 1987. The demography of chance extinction. Pp. 1134in Soulé, M. E., ed. Viable populations for conservation. Cambridge University Press, England.CrossRefGoogle Scholar
Goreau, T. F. 1959. The ecology of Jamaican coral reefs. I. Species composition and zonation. Ecology 40:6790.CrossRefGoogle Scholar
Guilderson, T. P., Fairbanks, R. G., and Rubenstone, J. L. 1994. Tropical temperature variations since 20,000 years ago: modulating interhemispheric change. Science 263:663665.CrossRefGoogle Scholar
Hanski, I. 1989. Metapopulation dynamics: does it help to have more of the same? Trends in Ecology and Evolution 4:113114.CrossRefGoogle ScholarPubMed
Hanski, I., and Gilpin, M. E. 1991. Metapopulation dynamics: brief history and conceptual domain. Pp. 316in Gilpin, M. E. and Hanski, I., eds. Metapopulation dynamics: empirical and theoretical investigations. Linnean Society of London, Academic Press, London.CrossRefGoogle Scholar
Harriott, V. J. 1992. Recruitment patterns of scleractinian corals in an isolated sub-tropical reef system. Coral Reefs 11:215219.CrossRefGoogle Scholar
Harrison, P. L., and Wallace, C. C. 1990. Reproduction, dispersal, and recruitment of scleractinian corals. Pp. 133208in Dubinsky, Z., ed. Coral reefs. Elsevier, New York.Google Scholar
Harrison, S., and Quinn, J. F. 1989. Correlated environments and the persistence of metapopulations. Oikos 56:293298.CrossRefGoogle Scholar
Highsmith, R. C. 1982. Reproduction by fragmentation in corals. Marine Ecology Progress Series 7:207226.CrossRefGoogle Scholar
Hughes, T. P. 1984. Population dynamics based on individual size rather than age: a general model with a coral reef example. American Naturalist 123:778795.CrossRefGoogle Scholar
Hughes, T. P. 1988. Long-term dynamics of coral populations: contrasting reproductive modes. Proceedings of the Sixth International Coral Reef Symposium 2:721725.Google Scholar
Hughes, T. P., and Connell, J. H. 1987. Population dynamics based on size or age? A reef-coral analysis. American Naturalist 129:818829.CrossRefGoogle Scholar
Hughes, T. P., and Jackson, J. B. C. 1985. Population dynamics and life histories of foliaceous corals. Ecological Monographs 55:141166.CrossRefGoogle Scholar
Hughes, T. P., Ayre, D., and Connell, J. H. 1992. The evolutionary ecology of corals. Trends in Ecology and Evolution 7:292295.CrossRefGoogle ScholarPubMed
Jablonski, D. 1986a. Mass and background extinctions: the alternation of macroevolutionary regimes. Science 231:129133.CrossRefGoogle ScholarPubMed
Jablonski, D. 1986b. Evolutionary consequences of mass extinctions. Pp. 313329in Raup, D. M. and Jablonski, D., eds. Patterns and processes in the history of life. Springer, Berlin.CrossRefGoogle Scholar
Jablonski, D. 1986c. Causes and consequences of mass extinctions: a comparative approach. Pp. 183229in Elliot, D. K., ed. Dynamics of extinction. Wiley, New York.Google Scholar
Jablonski, D. 1989. The biology of mass extinction: a paleontological view. Philosophical Transactions of the Royal Society of London B 325:357368.Google Scholar
Jablonski, D. 1991. Extinctions: a paleontological perspective. Science 253:754757.CrossRefGoogle ScholarPubMed
Jablonski, D., and Lutz, R. A. 1983. Larval ecology of marine benthic invertebrates: paleobiological implications. Biological Review 58:2189.CrossRefGoogle Scholar
Jackson, G. A., and Strathmann, R. R. 1981. Larval mortality from offshore mixing as a link between precompetent and competent periods of development. American Naturalist 118:1626.CrossRefGoogle Scholar
Jackson, J. B. C. 1974. Biogeographic consequences of eurytopy and stenotopy among marine bivalves and their evolutionary significance. American Naturalist 108:541560.CrossRefGoogle Scholar
Jackson, J. B. C. 1986. Modes of dispersal of clonal benthic invertebrates: consequences for species distributions and genetic structure of local populations. Bulletin of Marine Science 39:588606.Google Scholar
Jackson, J. B. C., Jung, P., Coates, A. G., and Collins, L. S. 1993. Diversity and extinction of tropical American mollusks and emergence of the isthmus of Panama. Science 260:16241626.CrossRefGoogle ScholarPubMed
Johnson, K. G. 1992a. Population dynamics of a free-living coral: recruitment, growth, and survivorship of Manicina areolata (Linnaeus) on the Caribbean coast of Panama. Journal Experimental Marine Biology and Ecology 164:171191.CrossRefGoogle Scholar
Johnson, K. G. 1992b. Synchronous planulation of Manicina areolata (Scleractinia) with lunar periodicity. Marine Ecology Progress Series 87:265273.CrossRefGoogle Scholar
Jokiel, P. L. 1984. Long distance dispersal of reef corals by rafting. Coral Reefs 3:113116.CrossRefGoogle Scholar
Jokiel, P. L. 1990. Transport of reef corals into the Great Barrier Reef. Nature (London) 347:665667.CrossRefGoogle Scholar
Karr, J. R. 1982. Population variability and extinction in the avifauna of a tropical land bridge island. Ecology 63:19751978.CrossRefGoogle Scholar
Knowlton, N. 1993. Sibling species in the sea. Annual Review of Ecology and Systematics 24:189216.CrossRefGoogle Scholar
Knowlton, N., and Jackson, J. B. C. 1993. Inbreeding and outbreeding in marine invertebrates. Pp. 200249in Thornhill, N. W., ed. The natural history of inbreeding and outbreeding. University of Chicago Press.Google Scholar
Knowlton, N., and Jackson, J. B. C. 1994. New taxonomy and niche partitioning on coral reefs: jack of all trades or master of some? Trends in Ecology and Evolution 9:79.CrossRefGoogle ScholarPubMed
Knowlton, N., Lang, J. C., and Keller, B. D. 1990. A case study of natural population collapse: post-hurricane predation on Jamaican staghorn corals. Smithsonian Contributions to Marine Science 31:125.Google Scholar
Knowlton, N., Weil, E., Weigt, L. A., and Guzman, H. M. 1992. Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255:330333.CrossRefGoogle ScholarPubMed
Lacy, R. C. 1992. The effects of inbreeding on isolated populations: are minimum viable population sizes predictable? Pp. 277296in Fiedler, P. L. and Jain, S. K., eds. Conservation biology. Chapman and Hall, London.CrossRefGoogle Scholar
Lande, R. 1988. Genetics and demography in biological conservation. Science 241:14551460.CrossRefGoogle ScholarPubMed
Lawton, J. H. 1990. Species richness and population dynamics of animal assemblages. Patterns in body size: abundance space. Philosophical Transactions of the Royal Society of London B 330:283291.Google Scholar
Leigh, E. G. 1981. The average lifetime of a population in a varying environment. Journal of Theoretical Biology 90:213239.CrossRefGoogle Scholar
Levinton, J. S. 1988. Genetics, paleontology, and macroevolution. Cambridge University Press.Google Scholar
Liddell, W. D., and Ohlhorst, S. L. 1988. Comparison of western Atlantic coral reef communities. Proceedings of the Sixth International Coral Reef Symposium (Townsville, Australia) 3:281286.Google Scholar
Manly, B. F. J. 1991. Randomization and Monte Carlo methods in biology. Chapman and Hall, London.CrossRefGoogle Scholar
Mayr, E. 1982. Processes of speciation in animals. Pp. 119in Barigozzi, C., ed. Mechanisms of speciation. A. R. Liss, New York.Google Scholar
McKinney, M. L., and Allmon, W. D.In press. Metapopulations and disturbance: from patch dynamics to biodiversity dynamics. In Erwin, D. and Anstey, R., eds. New approaches to speciation in the fossil record. Columbia University Press, New York.Google Scholar
Nee, S., Harvey, P. H., and Cotgreave, P. 1992. Population persistence and the natural relationships between body size and abundance. Pp. 124136in Sandlund, O. T., Hindar, K., and Brown, A. H. D., eds. Conservation of biodiversity for sustainable development. Scandinavian University Press, Oslo.Google Scholar
Neigel, J. E., and Avise, J. C. 1983. Clonal diversity and population structure in a reef-building coral, Acropora cervicornis: self-recognition analysis and demographic interpretation. Evolution 37:437453.Google Scholar
Otte, D., and Endler, J. A., eds. 1989. Speciation and its consequences. Sinauer, Sunderland, Mass.Google Scholar
Patton, J. L., and Smith, M. F. 1989. Population structure and the genetic and morphologic divergence among pocket gopher species (Genus Thomomys). Pp. 284304in Otte, and Endler, 1989.Google Scholar
Paulay, G. 1989. Effects of glacio-eustatic sea level fluctuations on insular coral faunas. American Zoologist 29:90A.Google Scholar
Paulay, G. 1990. Effects of late Cenozoic sea-level fluctuations on the bivalve faunas of tropical oceanic islands. Paleobiology 16:415434.CrossRefGoogle Scholar
Pimm, S. L. 1991. The balance of nature? University of Chicago Press.Google Scholar
Pimm, S. L., Jones, H. L., and Diamond, J. 1988. On the risk of extinction. American Naturalist 132:757785.CrossRefGoogle Scholar
Porter, J. W. 1976. Autotrophy, heterotrophy, and resource partitioning in Caribbean reef-building corals. American Naturalist 110:731742.CrossRefGoogle Scholar
Potts, D. C. 1984. Generation times and the Quaternary evolution of reef-building corals. Paleobiology 10:4858.CrossRefGoogle Scholar
Potts, D. C., Done, T. J., Isdale, P. J., and Fisk, D. A. 1985. Dominance of a coral community by the genus Porites (Scleractinia). Marine Ecology Progress Series 23:7984.CrossRefGoogle Scholar
Raup, D. M. 1991. A kill curve for Phanerozoic marine species. Paleobiology 17:3748.CrossRefGoogle ScholarPubMed
Richmond, R. A. 1989. Competency and dispersal potential of planula larvae of a spawning versus a brooding coral. Proceedings of the Sixth International Coral Reef Symposium 2:827831.Google Scholar
Richmond, R. A., and Hunter, C. L. 1990. Reproduction and recruitment of corals: comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Marine Ecology Progress Series 60:185203.CrossRefGoogle Scholar
Rosen, B. R., and Turnsek, D. 1989. Extinction patterns and biogeography of scleractinian corals across the Cretaceous/Tertiary. Memoirs of the Association of Australasian Palaeontologists 8:355370.Google Scholar
Saunders, J. B., Jung, P., and Biju-Duval, B. 1986. Neogene paleontology in the northern Dominican Republic. 1. Field surveys, lithology, environment, and age. Bulletins of American Paleontology 89:179.Google Scholar
Schaffer, M. L. 1987. Minimum viable populations: coping with uncertainty. Pp. 6986in Soulé, M. E., ed. Viable populations for conservation. Cambridge University Press.CrossRefGoogle Scholar
Sheehan, P. M. 1985. Reefs are not so different—they follow the evolutionary pattern of level-bottom communities. Geology 13:4649.2.0.CO;2>CrossRefGoogle Scholar
Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236:787792.CrossRefGoogle ScholarPubMed
Stanley, S. M. 1984a. Temperature and biotic crises in the marine realm. Geology 12:205208.2.0.CO;2>CrossRefGoogle Scholar
Stanley, S. M. 1984b. Marine mass extinctions: a dominant role for temperature. Pp. 69117in Nitecki, M. H., ed. Extinctions. University of Chicago Press.Google Scholar
Stanley, S. M. 1986. Population size, extinction, and speciation: the fission effect of Neogene Bivalvia. Paleobiology 12:89110.CrossRefGoogle Scholar
Stanley, S. M. 1990. The general correlation between rate of speciation and rate of extinction: fortuitous causal linkages. Pp. 103127in Ross, R. M. and Allmon, W. D., eds. Causes of evolution: a paleontological perspective. University of Chicago Press.Google Scholar
Stoddart, J. A. 1983. Asexual production of planulae in the coral Pocillopora damicornis. Marine Biology 76:279284.CrossRefGoogle Scholar
Stoddart, J. A. 1984. Genetical structure within populations of the coral Pocillopora damicornis. Marine Biology 81:1930.CrossRefGoogle Scholar
Szmant, A. M. 1986. Reproductive ecology of Caribbean reef corals. Coral Reefs 5:4354.CrossRefGoogle Scholar
Szmant, A. M. 1991. Sexual reproduction by the Caribbean reef coral Montastrea annularis and M. cavernosa. Marine Ecology Progress Series 74:1325.CrossRefGoogle Scholar
Szmant-Froelich, A. M. 1985. The effect of colony size on the reproductive ability of the Caribbean coral Montastrea annularis (Ellis and Solander). Proceedings of the Fifth International Coral Reef Symposium 4:295300.Google Scholar
Taylor, J. D. 1978. Faunal response to the instability of reef habitats: Pleistocene molluscan assemblages of Aldabra atoll. Palaeontology 21:130.Google Scholar
Wells, J. W., and Lang, J. C. 1973. Systematic list of Jamaican shallow-water Scleractinia. Bulletin of Marine Science 23:5558.Google Scholar
Williams, E. H., and Bunkley-Williams, L. 1990. The world-wide coral reef bleaching cycle and related sources of coral mortality. Atoll Research Bulletin 335:171.CrossRefGoogle Scholar