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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)...

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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C. G. Adams 1965. The Foraminifera and stratigraphy of the Melinau Limestone, Sarawak, and its importance in Tertiary correlation. Quarterly Journal of the Geological Society 121:283338.

A. Anderson 1971. Ordination methods in ecology. Journal of Ecology 59:713726.

A. Baird , and T. Hughes . 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.

A. Báldi 2008. Habitat heterogeneity overrides the species–area relationship. Journal of Biogeography 35:675681.

D. R. Bellwood , W. Renema , and B. R. Rosen . 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.

Z. Botta-Dukát 2005. Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. Journal of Vegetation Science 16:533540.

J. R. Bray , and J. T. Curtis . 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27:325349.

K. Bromfield , and J. M. Pandolfi . 2011. Regional patterns of evolutionary turnover in Neogene coral reefs from the central Indo-West Pacific Ocean. Evolutionary Ecology 26:375391.

N. K. Browne , S. G. Smithers , and C. T. Perry . 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.

A. F. Budd 2000. Diversity and extinction in the Cenozoic history of Caribbean reefs. Coral Reefs 19:2535.

M. W. Cadotte , K. Carscadden , and N. Mirotchnick . 2011. Beyond species: functional diversity and the maintenance of ecological processes and services. Journal of Applied Ecology 48:10791087.

S. Champely , and D. Chessel . 2002. Measuring biological diversity using Euclidean metrics. Environmental and Ecological Statistics 9:167177.

A. A. Chao 1987. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783791.

J. Chappell 1980. Coral morphology, diversity and reef growth. Nature 286:249252.

R. K. R. Colwell , and J. A. J. Coddington . 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society B 345:101118.

E. S. Darling , L. Alvarez-Filip , T. A. Oliver , T. R. McClanahan , I. M. Côté , and D. Bellwood . 2012. Evaluating life-history strategies of reef corals from species traits. Ecology Letters 15:13781386.

S. Díaz , A. Purvis , J. H. Cornelissen , G. M. Mace , M. J. Donoghue , R. M. Ewers , P. Jordano , and W. D. Pearse . 2013. Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecology and Evolution 3:29582975.

E. N. Edinger 1995. Preferential survivorship of brooding corals in a regional extinction. Paleobiology 21:200219.

E. N. Edinger , and M. J. Risk . 1994. Oligocene-Miocene extinction and geographic restriction of Caribbean corals: roles of turbidity, temperature, and nutrients. Palaios 9:576598.

A. M. Ellison , E. J. Farnsworth , and R. E. Merkt . 1999. Origins of mangrove ecosystems and the mangrove biodiversity anomaly. Global Ecology and Biogeography 8:95115.

D. P. Faith , and R. Norris . 1989. Correlation of environmental variables with patterns of distribution and abundance of common and rare freshwater macroinvertebrates. Biological Conservation 50:7798.

A. Foggo , M. J. Attrill , M. T. Frost , and A. A. Rowden . 2003. Estimating marine species richness: an evaluation of six extrapolative techniques. Marine Ecology Progress Series 248:1526.

C. R. Fonseca , and G. Ganade . 2001. Species functional redundancy, random extinctions and the stability of ecosystems. Journal of Ecology 89:118125.

M. Foote 2000. Origination and extinction components of taxonomic diversity: general problems. Paleobiology 26:74102.

J. Giraudel , and S. Lek . 2001. A comparison of self-organizing map algorithm and some conventional statistical methods for ecological community ordination. Ecological Modelling 146:329339.

J. C. Gower , and P. Legendre . 1986. Metric and Euclidean properties of dissimilarity coefficients. Journal of Classification 3:548.

J.-F. Guégan , S. Lek , and T. Oberdorff . 1998. Energy availability and habitat heterogeneity predict global riverine fish diversity. Nature 391:382384.

N. Guillemot , M. Kulbicki , P. Chabanet , and L. Vigliola . 2011. Functional redundancy patterns reveal non-random assembly rules in a species-rich marine assemblage. PLoS ONE 6:e26735.

R. Hall 1996. Reconstructing Cenozoic SE Asia. Geological Society of London, Special Publication 106:153184.

R. Hall 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.

R. Hall 2009. Hydrocarbon basins in SE Asia: understanding why they are there. Petroleum Geoscience 15:131146.

R. Hall , M. A. Cottam , and M. E. Wilson . 2011. The SE Asian gateway: history and tectonics of the Australia–Asia collision. Geological Society of London, Special Publication 355:16.

Ø. Hammer 2003. Biodiversity curves for the Ordovician of Baltoscandia. Lethaia 36:305313.

Ø. Hammer , and D. A. T. Harper . 2005. Paleontological data analysis. Wiley-Blackwell, Malden, Mass.

D. Huang , F. Benzoni , H. Fukami , N. Knowlton , N. D. Smith , and A. F. Budd . 2014. Taxonomic classification of the reef coral families Merulinidae, Montastraeidae, and Diploastraeidae (Cnidaria: Anthozoa: Scleractinia). Zoological Journal of the Linnean Society 171:277355.

C. S. Hutchison 2004. Marginal basin evolution: the southern South China Sea. Marine and Petroleum Geology 21:11291148.

C. A. Jaramillo 2002. Response of tropical vegetation to paleogene warming. Paleobiology 28:222243.

K. G. Johnson , J. B. Jackson , and A. F. Budd . 2008. Caribbean reef development was independent of coral diversity over 28 million years. Science 319:15211523.

K. G. Johnson , W. Renema , B. R. Rosen , and N. Santodomingo . 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.

K. G. Johnson , M. R. Sánchez-Villagra , and O. A. Aguilera . 2009. The Oligocene–Miocene transition on coral reefs in the Falcón Basin (NW Venezuela). Palaios 24:5969.

R. S. King , and C. J. Richardson . 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.

J. S. Klaus , B. P. Lutz , D. F. McNeill , A. F. Budd , K. G. Johnson , and S. E. Ishman . 2011. Rise and fall of Pliocene free-living corals in the Caribbean. Geology 39:375378.

C. Klug , B. Kroeger , W. Kiessling , G. L. Mullins , T. Servais , J. Frýda , D. Korn , and S. Turner . 2010. The Devonian nekton revolution. Lethaia 43:465477.

A. Kusworo , S. Reich , F. P. Wesselingh , N. Santodomingo , K. G. Johnson , J. A. Todd , and W. Renema . 2015. Diversity and paleoecology of Miocene coral-associated mollusks from East Kalimantan (Indonesia). Palaios 30:116127.

E. Laliberté , and P. Legendre . 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299305.

E. G. Leigh , A. O’Dea , and G. J. Vermeij . 2014. Historical biogeography of the Isthmus of Panama. Biological Reviews 89:148172.

D. J. Lohman , M. de Bruyn , T. Page , K. von Rintelen , R. Hall , P. K. L. Ng , H.-T. Shih , G. R. Carvalho , and T. von Rintelen . 2011. Biogeography of the Indo-Australian Archipelago. Annual Review of Ecology, Evolution, and Systematics 42:205226.

G. W. Luck , R. Harrington , P. A. Harrison , C. Kremen , P. M. Berry , R. Bugter , T. P. Dawson , F. de Bello , S. Díaz , C. K. Feld , J. R. Haslett , D. Hering , A. Kontogianni , S. Lavorel , M. Rounsevell , M. J. Samways , L. Sandin , J. Settele , M. T. Sykes , S. van den Hove , M. Vandewalle , and M. Zobel . 2009. Quantifying the Contribution of organisms to the provision of ecosystem services. BioScience 59:223235.

J. S. Madin 2005. Mechanical limitations of reef corals during hydrodynamic disturbances. Coral Reefs 24:630635.

C. R. Marshall 1990. Confidence intervals on stratigraphic ranges. Paleobiology 16:110.

T. McClanahan , M. Ateweberhan , N. Graham , S. Wilson , C. R. Sebastián , M. M. Guillaume , and J. Bruggemann . 2007. Western Indian Ocean coral communities: bleaching responses and susceptibility to extinction. Marine Ecology Progress Series 337:113.

L. B. McMonagle , P. Lunt , M. E. Wilson , K. G. Johnson , C. Manning , and J. Young . 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.

M. Mihaljević , W. Renema , K. Welsh , and J. M. Pandolfi . 2014. Eocene-Miocene shallow-water carbonate platforms and increased habitat diversity in Sarawak, Malaysia. Palaios 29:378391.

R. J Morley 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.

S. Naeem , and J. P. Wright 2003. Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecology Letters 6:567579.

V. Novak , N. Santodomingo , A. Rösler , E. Di Martino , J. C. Braga , P. D. Taylor , K. G. Johnson , and W. Renema . 2013. Environmental reconstruction of a late Burdigalian (Miocene) patch reef in deltaic deposits (East Kalimantan, Indonesia). Palaeogeography, Palaeoclimatology, Palaeoecology 374:110122.

A. O’Dea , H. A. Lessios , A. G. Coates , R. I. Eytan , S. A. Restrepo-Moreno , A. L. Cione , L. S. Collins , A. de Queiroz , D. W. Farris , and R. D. Norris 2016. Formation of the Isthmus of Panama. Science Advances 2:e1600883.

S. Pavoine , J. Vallet , A.-B. Dufour , S. Gachet , and H. Daniel 2009. On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118:391402.

O. L. Petchey , and K. J. Gaston . 2006. Functional diversity: back to basics and looking forward. Ecology Letters 9:741758.

P. Rachello-Dolmen , and D. Cleary . 2007. Relating coral species traits to environmental conditions in the Jakarta Bay/Pulau Seribu reef system, Indonesia. Estuarine, Coastal and Shelf Science 73:816826.

C. R. Rao 1982. Diversity and dissimilarity coefficients: a unified approach. Theoretical Population Biology 21:2443.

W. Renema , D. R. Bellwood , J. C. Braga , K. Bromfield , R. Hall , K. G. Johnson , P. Lunt , C. P. Meyer , L. B. McMonagle , R. J. Morley , A. O’Dea , J. A. Todd , F. P. Wesselingh , M. E. J. Wilson , and J. M. Pandolfi . 2008. Hopping hotspots: global shifts in marine biodiversity. Science 321:654657.

C. Ricotta 2005. Through the jungle of biological diversity. Acta Biotheoretica 53:2938.

M. L. Rosenzweig 1995. Species diversity in space and time. Cambridge University Press, Cambridge.

N. Santodomingo , V. Novak , V. Petković , N. Marshall , E. Di Martino , E. L. G. Capelli , A. Roesler , S. Reich , J. C. Braga , W. Renema , and K. G. Johnson . 2015a. A diverse patch reef from turbid habitats in the middle Miocene (East Kalimantan, Indonesia). Palaios 30:128149.

N. Santodomingo , W. Renema , and K. G. Johnson . 2016. Understanding the murky history of the Coral Triangle: Miocene corals and reef habitats in East Kalimantan (Indonesia). Coral Reefs 35:765781.

N. Santodomingo , C. C. Wallace , and K. G. Johnson . 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.

M. Scherer-Lorenzen , E. D. Schulze , A. Don , J. Schumacher , and E. Weller . 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.

J. J. Sepkoski Jr. 1975. Stratigraphic biases in the analysis of taxonomic survivorship. Paleobiology 1:343355.

A. B. Smith 2001. Large-scale heterogeneity of the fossil record: implications for Phanerozoic biodiversity studies. Philosophical Transactions of the Royal Society B 356:351367.

B. Sommer , P. L. Harrison , M. Beger , and J. M. Pandolfi . 2014. Trait-mediated environmental filtering drives assembly at biogeographic transition zones. Ecology 95:10001009.

K. Soong 1993. Colony size as a species character in massive reef corals. Coral Reefs 12:7783.

S. M. Stanley , and L. A. Hardie 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.

D. Strauss , and P. M. Sadler 1989. Classical confidence intervals and Bayesian probability estimates for ends of local taxon ranges. Mathematical Geology 21:411427.

R. D. Stuart-Smith , A. E. Bates , J. S. Lefcheck , J. E. Duffy , S. C. Baker , R. J. Thomson , J. F. Stuart-Smith , N. A. Hill , S. J. Kininmonth , L. Airoldi , M. A. Becerro , S. J. Campbell , T. P. Dawson , S. A. Navarrete , G. A. Soler , E. M. A. Strain , T. J. Willis , and G. J. Edgar . 2013. Integrating abundance and functional traits reveals new global hotspots of fish diversity. Nature 501:539542.

D. Tager , J. M. Webster , D. C. Potts , W. Renema , J. C. Braga , and J. M. Pandolfi . 2010. Community dynamics of Pleistocene coral reefs during alternative climatic regimes. Ecology 91:191200.

M. Tammekänd , O. Hints , and J. Nõlvak . 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.

L. M. Van Valen 1984. A resetting of Phanerozoic community evolution. Nature 307:5052.

S. Villéger , J. R. Miranda , D. F. Hernández , and D. Mouillot . 2010. Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecological Applications 20:15121522.

C. Violle , M. L. Navas , D. Vile , E. Kazakou , C. Fortunel , I. Hummel , and E. Garnier 2007. Let the concept of trait be functional!. Oikos 116:882892.

M. Wannier 2009. Carbonate platforms in wedge-top basins: an example from the Gunung Mulu National Park, Northern Sarawak (Malaysia). Marine and Petroleum Geology 26:177207.

A. Weigelt , J. Schumacher , C. Roscher , and B. Schmid 2008. Does biodiversity increase spatial stability in plant community biomass? Ecology Letters 11:338347.

M. E. Wilson 2002. Cenozoic carbonates in Southeast Asia: implications for equatorial carbonate development. Sedimentary Geology 147:295428.

M. E. J. Wilson 2008. Global and regional influences on equatorial shallow-marine carbonates during the Cenozoic. Palaeogeography, Palaeoclimatology, Palaeoecology 265:262274.

M. E. J Wilson . 2015. Oligo-Miocene variability in carbonate producers and platforms of the Coral Triangle biodiversity hotspot: habitat mosaics and marine biodiversity. Palaios 30:150168.

V. P. Wright , and P. M. Burgess . 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.

J. Zachos , M. Pagani , L. Sloan , E. Thomas , and K. Billups . 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686693.

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