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Identifying patterns and drivers of coral diversity in the Central Indo-Pacific marine biodiversity hotspot

Published online by Cambridge University Press:  18 April 2017

Morana Mihaljević
Affiliation:
School of Earth and Environmental Sciences, University of Queensland, Brisbane, Queensland 4072, Australia. E-mail: [email protected], [email protected].
Chelsea Korpanty
Affiliation:
Australian Research Council Centre of Excellence for Coral Reef Studies, School of Biological Sciences, University of Queensland, Brisbane, Queensland 4072, Australia. E-mail: [email protected], [email protected].
Willem Renema
Affiliation:
Naturalis Biodiversity Center, 2333 CR Leiden, Netherlands. E-mail: [email protected].
Kevin Welsh
Affiliation:
School of Earth and Environmental Sciences, University of Queensland, Brisbane, Queensland 4072, Australia. E-mail: [email protected], [email protected].
John M. Pandolfi
Affiliation:
Australian Research Council Centre of Excellence for Coral Reef Studies, School of Biological Sciences, University of Queensland, Brisbane, Queensland 4072, Australia. E-mail: [email protected], [email protected].

Abstract

Biodiversity hotspots are increasingly recognized as areas of high taxonomic and functional diversity. These hotspots are dynamic and shift geographically over time in response to environmental change. To identify drivers of the origin, evolution, and persistence of diversity hotspots, we investigated the diversity patterns of reef-building corals (Scleractinia) in the Central Indo-Pacific, a marine biodiversity hotspot for the last 25 Myr. We used the scleractinian fossil record (based on literature and a newly acquired fossil collection) to examine the taxonomic and functional diversity of corals from the Eocene to Pliocene. Our data identify potential drivers of coral diversity through time (and space) in the Central Indo-Pacific by constraining the timing of taxonomic turnover events and correlating them with known environmental changes. Increases in taxonomic diversity, high origination rates, and changes in abundance of functional character states indicate that the origin of the Central Indo-Pacific hotspot occurred during the Oligocene, initially through proliferation of pre-existing taxa and then by origination of new taxa. In contrast to taxonomic diversity, overall functional diversity of Central Indo-Pacific reef-building corals remained constant from the Eocene to the Pliocene. Our results identify global sea level as a main driver of diversity increase that, together with local tectonics, regulates availability of suitable habitats. Moreover, marine biodiversity hotspots develop from both the accumulation of taxa from older biodiversity hotspots and origination of new taxa. Our study demonstrates the utility of a combined literature-based and new collection approach for gaining new insights into the timing, drivers, and development of tropical biodiversity hotspots.

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Copyright © 2017 The Paleontological Society. All rights reserved 

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References

Literature Cited

Adams, C. G. 1965. The Foraminifera and stratigraphy of the Melinau Limestone, Sarawak, and its importance in Tertiary correlation. Quarterly Journal of the Geological Society 121:283338.Google Scholar
Adams, C. G., and Haak, R.. 1962. The stratigraphical succession in the Batu Gading area, Middle Baram, north Sarawak. The Geology and Mineral Resources of the Suai-Baram area, North Sarawak. Geological Survey Department (British Territories in Borneo) Memoir 13:141150.Google Scholar
Anderson, A. 1971. Ordination methods in ecology. Journal of Ecology 59:713726.Google Scholar
Aurelio, M. A., and Peña, R. E.. 2010. Geology of the Philippines. Mines and Geosciences Bureau, Manila.Google Scholar
Baird, A., and Hughes, T.. 2000. Competitive dominance by tabular corals: an experimental analysis of recruitment and survival of understorey assemblages. Journal of Experimental Marine Biology and Ecology 251:117132.Google Scholar
Báldi, A. 2008. Habitat heterogeneity overrides the species–area relationship. Journal of Biogeography 35:675681.CrossRefGoogle Scholar
Barnes, E., Aurelio, M. A., Muller, C., Pubellier, M., Quebral, R. D., and Rangib, C.. 1958. Geology and coal resources of the Argao-Dalaguete region, Cebu. Philippine Bureau of Mines, Manila.Google Scholar
Bellwood, D. R., Renema, W., and Rosen, B. R.. 2012. Biodiversity hotspots, evolution and coral reef biogeography: a review. Pp. 216245 in D. J. Gower, K. G. Johnson, J. E. Richardson, B. R. Rosen, L. Rüber, and S. T. Williams, eds. Biotic evolution and environmental change in Southeast Asia. Cambridge University Press, New York.Google Scholar
Botta-Dukát, Z. 2005. Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. Journal of Vegetation Science 16:533540.CrossRefGoogle Scholar
Bray, J. R., and Curtis, J. T.. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27:325349.CrossRefGoogle Scholar
Bromfield, K. 2013. Neogene corals from the Indo-Pacific: Indonesia, Papua New Guinea, and Fiji. Bulletins of American Paleontology 387:1136.Google Scholar
Bromfield, K., and Pandolfi, J. M.. 2011. Regional patterns of evolutionary turnover in Neogene coral reefs from the central Indo-West Pacific Ocean. Evolutionary Ecology 26:375391.Google Scholar
Browne, N. K., Smithers, S. G., and Perry, C. T.. 2012. Coral reefs of the turbid inner-shelf of the Great Barrier Reef, Australia: an environmental and geomorphic perspective on their occurrence, composition and growth. Earth-Science Reviews 115:120.Google Scholar
Budd, A. F. 2000. Diversity and extinction in the Cenozoic history of Caribbean reefs. Coral Reefs 19:2535.CrossRefGoogle Scholar
Cadotte, M. W., Carscadden, K., and Mirotchnick, N.. 2011. Beyond species: functional diversity and the maintenance of ecological processes and services. Journal of Applied Ecology 48:10791087.Google Scholar
Champely, S., and Chessel, D.. 2002. Measuring biological diversity using Euclidean metrics. Environmental and Ecological Statistics 9:167177.Google Scholar
Chao, A. 1984. Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11:265270.Google Scholar
Chao, A. A. 1987. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783791.Google Scholar
Chappell, J. 1980. Coral morphology, diversity and reef growth. Nature 286:249252.Google Scholar
Cohen, K., Finney, S., Gibbard, P., and Fan, J.-X.. 2013. The ICS International Chronostratigraphic Chart. Episodes 36:199204.CrossRefGoogle Scholar
Colwell, R. K. 2013. EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User’s guide and application. http://purl.oclc.org/estimates.Google Scholar
Colwell, R. K. R., and Coddington, J. A. J.. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society B 345:101118.Google Scholar
Darling, E. S., Alvarez-Filip, L., Oliver, T. A., McClanahan, T. R., Côté, I. M., and Bellwood, D.. 2012. Evaluating life-history strategies of reef corals from species traits. Ecology Letters 15:13781386.Google Scholar
de Boer, B., van de Wal, R. S. W., Lourens, L. J., and Bintanja, R.. 2012. Transient nature of the Earth’s climate and the implications for the interpretation of benthic δ18O records. Palaeogeography, Palaeoclimatology, Palaeoecology 335–336:411.Google Scholar
Devictor, V., Mouillot, D., Meynard, C., Jiguet, F., Thuiller, W., and Mouquet, N.. 2010. Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecology Letters 13:10301040.CrossRefGoogle Scholar
Díaz, S., Purvis, A., Cornelissen, J. H., Mace, G. M., Donoghue, M. J., Ewers, R. M., Jordano, P., and Pearse, W. D.. 2013. Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecology and Evolution 3:29582975.CrossRefGoogle ScholarPubMed
Edinger, E. N. 1995. Preferential survivorship of brooding corals in a regional extinction. Paleobiology 21:200219.CrossRefGoogle Scholar
Edinger, E. N., and Risk, M. J.. 1994. Oligocene-Miocene extinction and geographic restriction of Caribbean corals: roles of turbidity, temperature, and nutrients. Palaios 9:576598.Google Scholar
Ellison, A. M., Farnsworth, E. J., and Merkt, R. E.. 1999. Origins of mangrove ecosystems and the mangrove biodiversity anomaly. Global Ecology and Biogeography 8:95115.Google Scholar
Faith, D. P., and Norris, R.. 1989. Correlation of environmental variables with patterns of distribution and abundance of common and rare freshwater macroinvertebrates. Biological Conservation 50:7798.Google Scholar
Foggo, A., Attrill, M. J., Frost, M. T., and Rowden, A. A.. 2003. Estimating marine species richness: an evaluation of six extrapolative techniques. Marine Ecology Progress Series 248:1526.Google Scholar
Fonseca, C. R., and Ganade, G.. 2001. Species functional redundancy, random extinctions and the stability of ecosystems. Journal of Ecology 89:118125.Google Scholar
Foote, M. 2000. Origination and extinction components of taxonomic diversity: general problems. Paleobiology 26:74102.Google Scholar
Giraudel, J., and Lek, S.. 2001. A comparison of self-organizing map algorithm and some conventional statistical methods for ecological community ordination. Ecological Modelling 146:329339.Google Scholar
Gower, J. C., and Legendre, P.. 1986. Metric and Euclidean properties of dissimilarity coefficients. Journal of Classification 3:548.Google Scholar
Guégan, J.-F., Lek, S., and Oberdorff, T.. 1998. Energy availability and habitat heterogeneity predict global riverine fish diversity. Nature 391:382384.Google Scholar
Guillemot, N., Kulbicki, M., Chabanet, P., and Vigliola, L.. 2011. Functional redundancy patterns reveal non-random assembly rules in a species-rich marine assemblage. PLoS ONE 6:e26735.CrossRefGoogle Scholar
Hall, R. 1996. Reconstructing Cenozoic SE Asia. Geological Society of London, Special Publication 106:153184.CrossRefGoogle Scholar
Hall, R. 2001. Cenozoic reconstructions of SE Asia and the SW Pacific: changing patterns of land and sea. Pp. 35–56 in Faunal and floral migrations and evolution in SE Asia— Australasia. Swets & Zeitlinger, Lisse.Google Scholar
Hall, R. 2002. Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. Journal of Asian Earth Sciences 20:353431.Google Scholar
Hall, R. 2009. Hydrocarbon basins in SE Asia: understanding why they are there. Petroleum Geoscience 15:131146.Google Scholar
Hall, R., Cottam, M. A., and Wilson, M. E.. 2011. The SE Asian gateway: history and tectonics of the Australia–Asia collision. Geological Society of London, Special Publication 355:16.Google Scholar
Hammer, Ø. 2003. Biodiversity curves for the Ordovician of Baltoscandia. Lethaia 36:305313.Google Scholar
Hammer, Ø., and Harper, D. A. T.. 2005. Paleontological data analysis. Wiley-Blackwell, Malden, Mass.Google Scholar
Huang, D., Benzoni, F., Fukami, H., Knowlton, N., Smith, N. D., and Budd, A. F.. 2014. Taxonomic classification of the reef coral families Merulinidae, Montastraeidae, and Diploastraeidae (Cnidaria: Anthozoa: Scleractinia). Zoological Journal of the Linnean Society 171:277355.Google Scholar
Hutchison, C. S. 2004. Marginal basin evolution: the southern South China Sea. Marine and Petroleum Geology 21:11291148.Google Scholar
Jackson, J. B., and Hughes, T. P.. 1985. Adaptive strategies of coral-reef invertebrates: coral-reef environments that are regularly disturbed by storms and by predation often favor the very organisms most susceptible to damage by these processes. American Scientist 73:265274.Google Scholar
Jackson, J. B., Budd, A. F., and Coates, A. G.. 1996. Evolution and environment in tropical America. University of Chicago Press, Chicago.Google Scholar
Jaramillo, C. A. 2002. Response of tropical vegetation to paleogene warming. Paleobiology 28:222243.Google Scholar
Johnson, K. G., Jackson, J. B., and Budd, A. F.. 2008. Caribbean reef development was independent of coral diversity over 28 million years. Science 319:15211523.Google Scholar
Johnson, K. G., Renema, W., Rosen, B. R., and Santodomingo, N.. 2015. Old data for old questions: what can the historical collections really tell us about the Neogene origins of reef-coral diversity in the Coral Triangle? Palaios 30:94108.Google Scholar
Johnson, K. G., Sánchez-Villagra, M. R., and Aguilera, O. A.. 2009. The Oligocene–Miocene transition on coral reefs in the Falcón Basin (NW Venezuela). Palaios 24:5969.Google Scholar
Jurgan, H., and Domingo, R. M. A.. 1989. Younger Tertiary limestone formations in the Visayan Basin, Philippines. In H. Porth and C. H. von Daniels, eds. On the geology and hydrocarbon prospects of the Visayan Basin, Philippines. Geologisches Jahrbuch 70:207–276. Schweizerbart, Stuttgart.Google Scholar
Kay, E. A. 1996. Origin and evolutionary radiation of the Mollusca. Pp. 211220 in J. D. Taylor, ed. Origin and evolutionary radiation of the Mollusca. Oxford University Press, New York.Google Scholar
Keith, S., Baird, A., Hughes, T., Madin, J., and Connolly, S.. 2013. Faunal breaks and species composition of Indo-Pacific corals: the role of plate tectonics, environment and habitat distribution. Proceedings of the Royal Society of London B 280:20130818.Google Scholar
King, R. S., and Richardson, C. J.. 2008. Macroinvertebrate responses to a gradient of long-term nutrient additions, altered hydroperiod, and fire. Pp. 277319 in The everglades experiments: lessons for ecosystem restoration. Springer, New York.Google Scholar
Klaus, J. S., Lutz, B. P., McNeill, D. F., Budd, A. F., Johnson, K. G., and Ishman, S. E.. 2011. Rise and fall of Pliocene free-living corals in the Caribbean. Geology 39:375378.Google Scholar
Klug, C., Kroeger, B., Kiessling, W., Mullins, G. L., Servais, T., Frýda, J., Korn, D., and Turner, S.. 2010. The Devonian nekton revolution. Lethaia 43:465477.Google Scholar
Kraft, N. J., Godoy, O., and Levine, J. M.. 2015. Plant functional traits and the multidimensional nature of species coexistence. Proceedings of the National Academy of Sciences USA 112:797–802.Google Scholar
Kusworo, A., Reich, S., Wesselingh, F. P., Santodomingo, N., Johnson, K. G., Todd, J. A., and Renema, W.. 2015. Diversity and paleoecology of Miocene coral-associated mollusks from East Kalimantan (Indonesia). Palaios 30:116127.Google Scholar
Laliberté, E., and Legendre, P.. 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299305.Google Scholar
Leigh, E. G., O’Dea, A., and Vermeij, G. J.. 2014. Historical biogeography of the Isthmus of Panama. Biological Reviews 89:148172.Google Scholar
Leloux, J., and Renema, W.. 2007. Types and originals of fossil Porifera and Cnidaria of Indonesia in Naturalis. NNM Technical Bulletin 10. http://www.repository.naturalis.nl/record/270361.Google Scholar
Lohman, D. J., de Bruyn, M., Page, T., von Rintelen, K., Hall, R., Ng, P. K. L., Shih, H.-T., Carvalho, G. R., and von Rintelen, T.. 2011. Biogeography of the Indo-Australian Archipelago. Annual Review of Ecology, Evolution, and Systematics 42:205226.Google Scholar
Luck, G. W., Harrington, R., Harrison, P. A., Kremen, C., Berry, P. M., Bugter, R., Dawson, T. P., de Bello, F., Díaz, S., Feld, C. K., Haslett, J. R., Hering, D., Kontogianni, A., Lavorel, S., Rounsevell, M., Samways, M. J., Sandin, L., Settele, J., Sykes, M. T., van den Hove, S., Vandewalle, M., and Zobel, M.. 2009. Quantifying the Contribution of organisms to the provision of ecosystem services. BioScience 59:223235.Google Scholar
Lunt, P., and Allan, T.. 2004. Larger Foraminifera in Indonesian biostratigraphy, calibrated to isotopic dating. Geological Research and Development Centre Museum, Workshop on Micropaleontology, Bandung, Indonesia.Google Scholar
Lunt, P., and Renema, W.. 2014. On the HeterosteginaTansinhokellaSpiroclypeus lineage in SE Asia. Berita Sedimentologi 30:631.Google Scholar
MacArthur, R. H., and Wilson, E. O.. 1967. The theory of island biogeography. Princeton University Press, Princeton, N.J.Google Scholar
Madin, J. S. 2005. Mechanical limitations of reef corals during hydrodynamic disturbances. Coral Reefs 24:630635.Google Scholar
Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27:209220.Google Scholar
Marko, P. B., Eytan, R. I., and Knowlton, N.. 2015. Do large molecular sequence divergences imply an early closure of the Isthmus of Panama? Proceedings of the National Academy of Sciences USA 112:E5766.Google Scholar
Marshall, C. R. 1990. Confidence intervals on stratigraphic ranges. Paleobiology 16:110.Google Scholar
Mayfield, M. M., Bonser, S. P., Morgan, J. W., Aubin, I., McNamara, S., and Vesk, P. A.. 2010. What does species richness tell us about functional trait diversity? Predictions and evidence for responses of species and functional trait diversity to land-use change. Global Ecology and Biogeography 19:423431.Google Scholar
McClanahan, T., Ateweberhan, M., Graham, N., Wilson, S., Sebastián, C. R., Guillaume, M. M., and Bruggemann, J.. 2007. Western Indian Ocean coral communities: bleaching responses and susceptibility to extinction. Marine Ecology Progress Series 337:113.Google Scholar
McMonagle, L. B. 2012. A diverse assemblage of corals from the Late Oligocene of eastern Sabah, Borneo: pre-Miocene origins of the Indo-West Pacific marine biodiversity hotspot. M.S. thesis. Durham University, Durham, U.K.Google Scholar
McMonagle, L. B., Lunt, P., Wilson, M. E., Johnson, K. G., Manning, C., and Young, J.. 2011. A re-assessment of age dating of fossiliferous limestones in eastern Sabah, Borneo: implications for understanding the origins of the Indo-Pacific marine biodiversity hotspot. Palaeogeography, Palaeoclimatology, Palaeoecology 305:2842.CrossRefGoogle Scholar
Mihaljević, M., Renema, W., Welsh, K., and Pandolfi, J. M.. 2014. Eocene-Miocene shallow-water carbonate platforms and increased habitat diversity in Sarawak, Malaysia. Palaios 29:378391.Google Scholar
Moore, J. C. 2013. Diversity, taxonomical versus functional. Pp. 206215 in S. A. Levin, ed. Encyclopedia of Biodiversity. Elsevier, Oxford.Google Scholar
Morley, R. J. 2000. Origin and evolution of tropical rain forests. Wiley, Hoboken, N.J.Google Scholar
Morley, R. J 2011. Cretaceous and Tertiary climate change and the past distribution of megathermal rainforests. Pp. 131 in R. J. Morley, ed. Tropical rainforest responses to climatic change. Springer, Berlin.Google Scholar
Morley, R. J., Morley, H. P., and Restrepo-Pace, P.. 2003. Unravelling the tectonically controlled stratigraphy of the West Natuna Basin by means of palaeo-derived mid Tertiary climate changes. Proceedings of the 29th Annual Convention of the Indonesian Petroleum Association 1:1–24.Google Scholar
Murtagh, F. 2000. Multivariate data analysis software and resources. http://www.classification-society.org/csna/mda-sw.Google Scholar
Naeem, S., and Wright, J. P. 2003. Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecology Letters 6:567579.CrossRefGoogle Scholar
Novak, V., Santodomingo, N., Rösler, A., Di Martino, E., Braga, J. C., Taylor, P. D., Johnson, K. G., and Renema, W.. 2013. Environmental reconstruction of a late Burdigalian (Miocene) patch reef in deltaic deposits (East Kalimantan, Indonesia). Palaeogeography, Palaeoclimatology, Palaeoecology 374:110122.Google Scholar
O’Dea, A., and Collins, L. S.. 2013. Environmental, ecological, and evolutionary change in seas across the Isthmus of Panama. Bulletin of Marine Science 89:769777.Google Scholar
O’Dea, A., Lessios, H. A., Coates, A. G., Eytan, R. I., Restrepo-Moreno, S. A., Cione, A. L., Collins, L. S., de Queiroz, A., Farris, D. W., and Norris, R. D. 2016. Formation of the Isthmus of Panama. Science Advances 2:e1600883.Google Scholar
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R., Simpson, G. L., Solymos, P., Stevens, M. H. H., and Wagner, H.. 2013. Package ‘vegan.’ Community ecology package. Version 2:411.Google Scholar
Pavoine, S., Vallet, J., Dufour, A.-B., Gachet, S., and Daniel, H. 2009. On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118:391402.CrossRefGoogle Scholar
Petchey, O. L., and Gaston, K. J.. 2006. Functional diversity: back to basics and looking forward. Ecology Letters 9:741758.Google Scholar
Porth, H., and von Daniels, C. H.. 1989. On the geology and hydrocarbon prospects of the Visayan Basin, Philippines. Geologisches Jahrbuch, Reihe B 70:1428.Google Scholar
R Development Core Team, A 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rachello-Dolmen, P., and Cleary, D.. 2007. Relating coral species traits to environmental conditions in the Jakarta Bay/Pulau Seribu reef system, Indonesia. Estuarine, Coastal and Shelf Science 73:816826.Google Scholar
Rao, C. R. 1982. Diversity and dissimilarity coefficients: a unified approach. Theoretical Population Biology 21:2443.Google Scholar
Renema, W. 2007. Fauna development of larger benthic foraminifera in the Cenozoic of Southeast Asia. Pp. 179215 in W. Renema, ed. Biogeography, time, and place: distributions, barriers, and islands. Springer, Dordrecht, Netherlands.Google Scholar
Renema, W., Bellwood, D. R., Braga, J. C., Bromfield, K., Hall, R., Johnson, K. G., Lunt, P., Meyer, C. P., McMonagle, L. B., Morley, R. J., O’Dea, A., Todd, J. A., Wesselingh, F. P., Wilson, M. E. J., and Pandolfi, J. M.. 2008. Hopping hotspots: global shifts in marine biodiversity. Science 321:654657.Google Scholar
Ricotta, C. 2005. Through the jungle of biological diversity. Acta Biotheoretica 53:2938.Google Scholar
Rosen, B., Aillud, G., Bosellini, F., Clack, N., Insalaco, E., Valldeperas, F., and Wilson, M.. 2002. Platy coral assemblages: 200 million years of functional stability in response to the limiting effects of light and turbidity. Proceedings of the Ninth International Coral Reefs Symposium, Bali 1:255–264.Google Scholar
Rosen, B. R. 1984. Reef coral biogeography and climate through the late Cainozoic: just islands in the sun or a critical pattern of islands. In P. J. Brenchley, ed. Fossils and climate. Geological Journal, Special Issue.11:201–262.Google Scholar
Rosenzweig, M. L. 1995. Species diversity in space and time. Cambridge University Press, Cambridge.Google Scholar
Russel, G. J. 1998. Turnover dynamics across ecolgical andgeological scales. Pp. 377404. in M. L. McKinney, and J. Drake, eds. Biodiversity dynamics: evolutionary turnover and volatility in higher taxa. Columbia University Press, New York.Google Scholar
Santodomingo, N., Novak, V., Petković, V., Marshall, N., Di Martino, E., Capelli, E. L. G., Roesler, A., Reich, S., Braga, J. C., Renema, W., and Johnson, K. G.. 2015a. A diverse patch reef from turbid habitats in the middle Miocene (East Kalimantan, Indonesia). Palaios 30:128149.Google Scholar
Santodomingo, N., Renema, W., and Johnson, K. G.. 2016. Understanding the murky history of the Coral Triangle: Miocene corals and reef habitats in East Kalimantan (Indonesia). Coral Reefs 35:765781.Google Scholar
Santodomingo, N., Wallace, C. C., and Johnson, K. G.. 2015b. Fossils reveal a high diversity of the staghorn coral genera Acropora and Isopora (Scleractinia: Acroporidae) in the Neogene of Indonesia. Zoological Journal of the Linnean Society 175:677763.Google Scholar
Scherer-Lorenzen, M., Schulze, E. D., Don, A., Schumacher, J., and Weller, E.. 2007. Exploring the functional significance of forest diversity: a new long-term experiment with temperate tree species (BIOTREE). Perspectives in Plant Ecology, Evolution and Systematics 9:5370.Google Scholar
Sepkoski, J. J. Jr. 1975. Stratigraphic biases in the analysis of taxonomic survivorship. Paleobiology 1:343355.Google Scholar
Smith, A. B. 2001. Large-scale heterogeneity of the fossil record: implications for Phanerozoic biodiversity studies. Philosophical Transactions of the Royal Society B 356:351367.Google Scholar
Sommer, B., Harrison, P. L., Beger, M., and Pandolfi, J. M.. 2014. Trait-mediated environmental filtering drives assembly at biogeographic transition zones. Ecology 95:10001009.Google Scholar
Soong, K. 1993. Colony size as a species character in massive reef corals. Coral Reefs 12:7783.Google Scholar
Stanley, S. M., and Hardie, L. A. 1998. Secular oscillations in the carbonate mineralogy of reef-building and sediment-producing organisms driven by tectonically forced shifts in seawater chemistry. Palaeogeography, Palaeoclimatology, Palaeoecology 144:319.Google Scholar
Stehli, F. G., and Wells, J. W.. 1971. Diversity and age patterns in hermatypic corals. Systematic Biology 20:115126.Google Scholar
Strauss, D., and Sadler, P. M. 1989. Classical confidence intervals and Bayesian probability estimates for ends of local taxon ranges. Mathematical Geology 21:411427.Google Scholar
Stuart-Smith, R. D., Bates, A. E., Lefcheck, J. S., Duffy, J. E., Baker, S. C., Thomson, R. J., Stuart-Smith, J. F., Hill, N. A., Kininmonth, S. J., Airoldi, L., Becerro, M. A., Campbell, S. J., Dawson, T. P., Navarrete, S. A., Soler, G. A., Strain, E. M. A., Willis, T. J., and Edgar, G. J.. 2013. Integrating abundance and functional traits reveals new global hotspots of fish diversity. Nature 501:539542.Google Scholar
Tager, D., Webster, J. M., Potts, D. C., Renema, W., Braga, J. C., and Pandolfi, J. M.. 2010. Community dynamics of Pleistocene coral reefs during alternative climatic regimes. Ecology 91:191200.Google Scholar
Tammekänd, M., Hints, O., and Nõlvak, J.. 2010. Chitinozoan dynamics and biostratigraphy in the Väo Formation (Darriwilian) of the Uuga Cliff, Pakri Peninsula, NW Estonia. Estonian Journal of Earth Sciences 59(1), 25.Google Scholar
Umbgrove, J. H. 1946. Evolution of reef corals in East Indies since Miocene time. AAPG Bulletin 30(1), 2331.Google Scholar
Van Valen, L. M. 1984. A resetting of Phanerozoic community evolution. Nature 307:5052.CrossRefGoogle Scholar
Veron, J. E. N., and Stafford-Smith, M.. 2002. Coral ID. Australian Institute of Marine Sciences, Townsville. http://data.aims.gov.au/metadataviewer/uuid/3caf89c0-55b9-11dc-8d3c-00008a07204e.Google Scholar
Villéger, S., Miranda, J. R., Hernández, D. F., and Mouillot, D.. 2010. Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecological Applications 20:15121522.Google Scholar
Violle, C., Navas, M. L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I., and Garnier, E. 2007. Let the concept of trait be functional!. Oikos 116:882892.Google Scholar
Wallace, C. C., and Rosen, B. R.. 2006. Diverse staghorn corals (Acropora) in high-latitude Eocene assemblages: implications for the evolution of modern diversity patterns of reef corals. Proceedings of the Royal Society B 273:975–982.Google Scholar
Wannier, M. 2009. Carbonate platforms in wedge-top basins: an example from the Gunung Mulu National Park, Northern Sarawak (Malaysia). Marine and Petroleum Geology 26:177207.Google Scholar
Weigelt, A., Schumacher, J., Roscher, C., and Schmid, B. 2008. Does biodiversity increase spatial stability in plant community biomass? Ecology Letters 11:338347.Google Scholar
Wilson, M. E. 2002. Cenozoic carbonates in Southeast Asia: implications for equatorial carbonate development. Sedimentary Geology 147:295428.Google Scholar
Wilson, M. E. J. 2008. Global and regional influences on equatorial shallow-marine carbonates during the Cenozoic. Palaeogeography, Palaeoclimatology, Palaeoecology 265:262274.Google Scholar
Wilson, M. E. J. 2015. Oligo-Miocene variability in carbonate producers and platforms of the Coral Triangle biodiversity hotspot: habitat mosaics and marine biodiversity. Palaios 30:150168.Google Scholar
Wilson, M. E. J., and Rosen, B. R.. 1998. Implications of paucity of corals in the Paleogene of SE Asia: plate tectonics or centre of origin. Pp. 165195 in. Biogeography and geological evolution of SE Asia. Backhuys, Amsterdam, Netherlands.Google Scholar
WoRMS Editorial Board 2016. World Register of Marine Species. http://www.marinespecies.org at VLIZ. Accessed 2016-07. doi: 10.14284/170.Google Scholar
Wright, V. P., and Burgess, P. M.. 2005. The carbonate factory continuum, facies mosaics and microfacies: an appraisal of some of the key concepts underpinning carbonate sedimentology. Facies 51(1–4), 1723.Google Scholar
Zachos, J., Pagani, M., Sloan, L., Thomas, E., and Billups, K.. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686693.Google Scholar