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

  • Morana Mihaljević (a1), Chelsea Korpanty (a2), Willem Renema (a3), Kevin Welsh (a1) and John M. Pandolfi (a2)...
Abstract
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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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.
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.
Anderson A. 1971. Ordination methods in ecology. Journal of Ecology 59:713726.
Aurelio M. A., and Peña R. E.. 2010. Geology of the Philippines. Mines and Geosciences Bureau, Manila.
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.
Báldi A. 2008. Habitat heterogeneity overrides the species–area relationship. Journal of Biogeography 35:675681.
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.
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.
Botta-Dukát Z. 2005. Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. Journal of Vegetation Science 16:533540.
Bray J. R., and Curtis J. T.. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27:325349.
Bromfield K. 2013. Neogene corals from the Indo-Pacific: Indonesia, Papua New Guinea, and Fiji. Bulletins of American Paleontology 387:1136.
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.
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.
Budd A. F. 2000. Diversity and extinction in the Cenozoic history of Caribbean reefs. Coral Reefs 19:2535.
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.
Champely S., and Chessel D.. 2002. Measuring biological diversity using Euclidean metrics. Environmental and Ecological Statistics 9:167177.
Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11:265270.
Chao A. A. 1987. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783791.
Chappell J. 1980. Coral morphology, diversity and reef growth. Nature 286:249252.
Cohen K., Finney S., Gibbard P., and Fan J.-X.. 2013. The ICS International Chronostratigraphic Chart. Episodes 36:199204.
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.
Colwell R. K. R., and Coddington J. A. J.. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society B 345:101118.
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.
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.
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.
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.
Edinger E. N. 1995. Preferential survivorship of brooding corals in a regional extinction. Paleobiology 21:200219.
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.
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.
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.
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.
Fonseca C. R., and Ganade G.. 2001. Species functional redundancy, random extinctions and the stability of ecosystems. Journal of Ecology 89:118125.
Foote M. 2000. Origination and extinction components of taxonomic diversity: general problems. Paleobiology 26:74102.
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.
Gower J. C., and Legendre P.. 1986. Metric and Euclidean properties of dissimilarity coefficients. Journal of Classification 3:548.
Guégan J.-F., Lek S., and Oberdorff T.. 1998. Energy availability and habitat heterogeneity predict global riverine fish diversity. Nature 391:382384.
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.
Hall R. 1996. Reconstructing Cenozoic SE Asia. Geological Society of London, Special Publication 106:153184.
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.
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.
Hall R. 2009. Hydrocarbon basins in SE Asia: understanding why they are there. Petroleum Geoscience 15:131146.
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.
Hammer Ø. 2003. Biodiversity curves for the Ordovician of Baltoscandia. Lethaia 36:305313.
Hammer Ø., and Harper D. A. T.. 2005. Paleontological data analysis. Wiley-Blackwell, Malden, Mass.
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.
Hutchison C. S. 2004. Marginal basin evolution: the southern South China Sea. Marine and Petroleum Geology 21:11291148.
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.
Jackson J. B., Budd A. F., and Coates A. G.. 1996. Evolution and environment in tropical America. University of Chicago Press, Chicago.
Jaramillo C. A. 2002. Response of tropical vegetation to paleogene warming. Paleobiology 28:222243.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Laliberté E., and Legendre P.. 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299305.
Leigh E. G., O’Dea A., and Vermeij G. J.. 2014. Historical biogeography of the Isthmus of Panama. Biological Reviews 89:148172.
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.
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.
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.
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.
Lunt P., and Renema W.. 2014. On the HeterosteginaTansinhokellaSpiroclypeus lineage in SE Asia. Berita Sedimentologi 30:631.
MacArthur R. H., and Wilson E. O.. 1967. The theory of island biogeography. Princeton University Press, Princeton, N.J.
Madin J. S. 2005. Mechanical limitations of reef corals during hydrodynamic disturbances. Coral Reefs 24:630635.
Mantel N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27:209220.
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.
Marshall C. R. 1990. Confidence intervals on stratigraphic ranges. Paleobiology 16:110.
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.
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.
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.
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.
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.
Moore J. C. 2013. Diversity, taxonomical versus functional. Pp. 206215 in S. A. Levin, ed. Encyclopedia of Biodiversity. Elsevier, Oxford.
Morley R. J. 2000. Origin and evolution of tropical rain forests. Wiley, Hoboken, N.J.
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.
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.
Murtagh F. 2000. Multivariate data analysis software and resources. http://www.classification-society.org/csna/mda-sw.
Naeem S., and Wright J. P. 2003. Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecology Letters 6:567579.
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.
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.
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.
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.
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.
Petchey O. L., and Gaston K. J.. 2006. Functional diversity: back to basics and looking forward. Ecology Letters 9:741758.
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.
R Development Core Team, A 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
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.
Rao C. R. 1982. Diversity and dissimilarity coefficients: a unified approach. Theoretical Population Biology 21:2443.
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.
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.
Ricotta C. 2005. Through the jungle of biological diversity. Acta Biotheoretica 53:2938.
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.
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.
Rosenzweig M. L. 1995. Species diversity in space and time. Cambridge University Press, Cambridge.
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.
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.
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.
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.
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.
Sepkoski J. J. Jr. 1975. Stratigraphic biases in the analysis of taxonomic survivorship. Paleobiology 1:343355.
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.
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.
Soong K. 1993. Colony size as a species character in massive reef corals. Coral Reefs 12:7783.
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.
Stehli F. G., and Wells J. W.. 1971. Diversity and age patterns in hermatypic corals. Systematic Biology 20:115126.
Strauss D., and Sadler P. M. 1989. Classical confidence intervals and Bayesian probability estimates for ends of local taxon ranges. Mathematical Geology 21:411427.
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.
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.
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.
Umbgrove J. H. 1946. Evolution of reef corals in East Indies since Miocene time. AAPG Bulletin 30(1), 2331.
Van Valen L. M. 1984. A resetting of Phanerozoic community evolution. Nature 307:5052.
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.
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.
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.
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.
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.
Weigelt A., Schumacher J., Roscher C., and Schmid B. 2008. Does biodiversity increase spatial stability in plant community biomass? Ecology Letters 11:338347.
Wilson M. E. 2002. Cenozoic carbonates in Southeast Asia: implications for equatorial carbonate development. Sedimentary Geology 147:295428.
Wilson M. E. J. 2008. Global and regional influences on equatorial shallow-marine carbonates during the Cenozoic. Palaeogeography, Palaeoclimatology, Palaeoecology 265:262274.
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.
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.
WoRMS Editorial Board 2016. World Register of Marine Species. http://www.marinespecies.org at VLIZ. Accessed 2016-07. doi: 10.14284/170.
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.
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.
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