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Extraordinary diversity of reef corals in the South China Sea

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Abstract

The South China Sea in the Central Indo-Pacific is a large marine region that spans an area of more than 3 million km2 bounded by the coastlines of ten Asian nation states and contains numerous small islands. Although it abuts the western border of the Coral Triangle, the designated centre of maximum marine biodiversity, the South China Sea has received much less scientific and conservation attention. In particular, a consolidated estimate of the region’s scleractinian reef coral diversity has yet to emerge. To address this issue, we assemble a comprehensive species distribution data set that comprises 16 reef areas spread across the entire South China Sea. Despite containing less than 17 % of the reef area as compared to the Coral Triangle, this region hosts 571 known species of reef corals, a richness that is comparable to the Coral Triangle’s based on a standardised nomenclatural scheme. Similarity profile analysis and non-metric multidimensional scaling demonstrate that most areas are compositionally distinct from one another and are structured according to latitude but not longitude. More broadly, this study underscores the remarkable and unexpected diversity of reef corals in the South China Sea.

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References

  • Ablan MCA, McManus JW, Chen CA, Shao KT, Bell JD, Cabanban AS, Vo ST, Arthana IW (2002) Meso-scale transboundary units for the management of coral reefs in the South China Sea area. Naga World Fish Cent Q 25:4–9

    Google Scholar 

  • Affendi YA, Rosman FR (2012) Current knowledge on scleractinian coral diversity of Peninsular Malaysia. In: Kamarruddin I, Mohamed CAR, Rozaimi MJ, Kee Alfian AA, Fitra AZ, Lee JN (eds) Malaysia’s marine biodiversity: inventory and current status. Department of Marine Park Malaysia, Putrajaya, pp 21–31

    Google Scholar 

  • Affendi YA, Tajuddin BH, Lee YL, Kee Alfian AA, Yusuf Y (2005) Scleractinian coral diversity of Kg. Tekek, Pulau Tioman Marine Park. In: Second regional symposium on environment and natural resources, Kuala Lumpur, Malaysia, 22–23 March 2005. pp 20–31

  • Affendi YA, Tajuddin BH, Yusuf Y, Kee Alfian AA, Wong NWS, Ooi JLS, Nasir MN (2007) Report on the marine biological resources survey of the proposed area for Pulau Tioman Airport, Pahang Darul Makmur. Department of Marine Park Malaysia, Kuala Lumpur

    Google Scholar 

  • Aliño PM (2001) The South China Sea - revisiting the large marine ecosystem approach. Fisheries Training Programme, United Nations University. Marine Research Institute, Reykjavík

  • Allen GR (2008) Conservation hotspots of biodiversity and endemism for Indo-Pacific coral reef fishes. Aquat Conserv: Mar Freshw Ecosyst 18:541–556. doi:10.1002/aqc.880

    Google Scholar 

  • Allen GR, Werner TB (2002) Coral reef fish assessment in the ‘coral triangle’ of southeastern Asia. Environ Biol Fish 65:209–214. doi:10.1023/A:1020093012502

  • Ang PO, McCorry D, Choi LS (2003) Establishing a reference collection and field guides for Hong Kong scleractinian coral. Final report submitted to the Marine Conservation Division, Agriculture, Fisheries and Conservation Department. Hong Kong SAR Government, Hong Kong

  • Arrigoni R, Stefani F, Pichon M, Galli P, Benzoni F (2012) Molecular phylogeny of the Robust clade (Faviidae, Mussidae, Merulinidae, and Pectiniidae): an Indian Ocean perspective. Mol Phylogenet Evol 65:183–193. doi:10.1016/j.ympev.2012.06.001

    PubMed  Google Scholar 

  • Awang D, Chan AA (2014) Reef status of Labuan Marine Park. In: Report of marine biodiversity expedition 2013. Volume 3: Federal Territory of Labuan Marine Park. Department of Marine Park Malaysia, Putrajaya, pp 27–36 (in press)

  • Bellwood DR, Hughes TP (2001) Regional-scale assembly rules and biodiversity of coral reefs. Science 292:1532–1534. doi:10.1126/science.1058635

    CAS  PubMed  Google Scholar 

  • Bellwood DR, Meyer CP (2009) Searching for heat in a marine biodiversity hotspot. J Biogeogr 36:569–576. doi:10.1111/j.1365-2699.2008.02029.x

    Google Scholar 

  • Benzoni F, Stefani F, Pichon M, Galli P (2010) The name game: morpho-molecular species boundaries in the genus Psammocora (Cnidaria, Scleractinia). Zool J Linn Soc 160:421–456. doi:10.1111/j.1096-3642.2010.00622.x

    Google Scholar 

  • Benzoni F, Arrigoni R, Stefani F, Reijnen BT, Montano S, Hoeksema BW (2012a) Phylogenetic position and taxonomy of Cycloseris explanulata and C. wellsi (Scleractinia: Fungiidae): lost mushroom corals find their way home. Contrib Zool 81:125–146

    Google Scholar 

  • Benzoni F, Arrigoni R, Stefani F, Stolarski J (2012b) Systematics of the coral genus Craterastrea (Cnidaria, Anthozoa, Scleractinia) and description of a new family through combined morphological and molecular analyses. Syst Biodivers 10:417–433. doi:10.1080/14772000.2012.744369

    Google Scholar 

  • Benzoni F, Arrigoni R, Waheed Z, Stefani F, Hoeksema BW (2014) Phylogenetic relationships and revision of the genus Blastomussa (Cnidaria: Anthozoa: Scleractinia) with description of a new species. Raffles Bull Zool (in press)

  • Best MB, Hoeksema BW, Moka W, Moll H, Sutarna IN (1989) Recent scleractinian coral species collected during the Snellius-II Expedition in eastern Indonesia. Neth J Sea Res 23:107–115. doi:10.1016/0077-7579(89)90005-7

    Google Scholar 

  • Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349

    Google Scholar 

  • Bridge TCL, Fabricius KE, Bongaerts P, Wallace CC, Muir PR, Done TJ, Webster JM (2012) Diversity of Scleractinia and Octocorallia in the mesophotic zone of the Great Barrier Reef, Australia. Coral Reefs 31:179–189. doi:10.1007/s00338-011-0828-1

    Google Scholar 

  • Briggs JC (1974) Marine zoogeography. McGraw-Hill, New York

    Google Scholar 

  • Budd AF, Fukami H, Smith ND, Knowlton N (2012) Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia). Zool J Linn Soc 166:465–529. doi:10.1111/j.1096-3642.2012.00855.x

    Google Scholar 

  • Burke L, Reytar K, Spalding MD, Perry A (2011) Reefs at risk revisited. World Resources Institute, Washington, DC

    Google Scholar 

  • Burke L, Reytar K, Spalding MD, Perry A (2012) Reefs at risk revisited in the Coral Triangle. World Resources Institute, Washington, DC

    Google Scholar 

  • Carpenter KE, Springer VG (2005) The center of the center of marine shore fish biodiversity: the Philippine Islands. Environ Biol Fish 72:467–480. doi:10.1007/s10641-004-3154-4

  • Chankong A (2006) Species, distribution and community structure of the scleractinian corals: genus Acropora in the Gulf of Thailand. Dissertation, Burapha University, Chonburi

  • Chen CA (1999) Analysis of scleractinian distribution in Taiwan indicating a pattern congruent with sea surface temperatures and currents: examples from Acropora and Faviidae corals. Zool Stud 38:119–129

    Google Scholar 

  • Chen J, Huang H, Huang L, Wang D (2010) Coral reefs of Sanya and their biodiversity [in Chinese]. Nanyang, Beijing

    Google Scholar 

  • Chou LM, Sudara S, Manthachitra V, Moredee R, Snidvongs A, Yeemin T (1991) Temporal variation in a coral reef community at Pattaya Bay, Gulf of Thailand. Environ Monit Assess 19:295–307. doi:10.1007/BF00401319

    CAS  PubMed  Google Scholar 

  • Chou LM, Yeemin T, bin Gor Yaman AR, Vo ST, Aliño PM, Suharsono (2009) Coral reef restoration in the South China Sea. Galaxea 11:67–74

    Google Scholar 

  • Clark A, Li C (1993) Marine mineral resources of the South China Sea. Mar Georesour Geotechnol 11:101–126. doi:10.1080/10641199309379907

    CAS  Google Scholar 

  • Clarke KR, Somerfield PJ, Gorley RN (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Biol Ecol 366:56–69. doi:10.1016/j.jembe.2008.07.009

    Google Scholar 

  • Clifton J (2009) Science, funding and participation: key issues for marine protected area networks and the Coral Triangle Initiative. Environ Conserv 36:91–96. doi:10.1017/S0376892909990075

    Google Scholar 

  • Connolly SR, Bellwood DR, Hughes TP (2003) Indo-Pacific biodiversity of coral reefs: deviations from a mid-domain model. Ecology 84:2178–2190

    Google Scholar 

  • Cornell HV, Karlson RH (2000) Coral species richness: ecological versus biogeographical influences. Coral Reefs 19:37–49

    Google Scholar 

  • Dai C-F (1991) Reef environment and coral fauna of southern Taiwan. Atoll Res Bull 354:1–24

    Google Scholar 

  • Dai C-F, Fan T-Y (1996) Coral fauna of Taiping Island (Itu Aba Island) in the Spratlys of the South China Sea. Atoll Res Bull 436:1–21

    Google Scholar 

  • Dai C-F, Horng S (2009a) Scleractinia fauna of Taiwan. I. The complex group. National Taiwan University, Taipei

    Google Scholar 

  • Dai C-F, Horng S (2009b) Scleractinia fauna of Taiwan. II. The robust group. National Taiwan University, Taipei

    Google Scholar 

  • Ditlev H (2003) New scleractinian corals (Cnidaria: Anthozoa) from Sabah, North Borneo. Description of one new genus and eight new species, with notes on their taxonomy and ecology. Zool Meded Leiden 77:193–219

    Google Scholar 

  • Djalal H (2000) South China Sea island disputes. Raffles Bull Zool Suppl 8:9–21

    Google Scholar 

  • Done TJ (1982) Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1:95–107

    Google Scholar 

  • Fang W, Fang G, Shi P, Huang Q, Xie Q (2002) Seasonal structures of upper layer circulation in the southern South China Sea from in situ observations. J Geophys Res 107:3202. doi:10.1029/2002JC001343

    Google Scholar 

  • Fenner DP (2001) Malaysian hard corals. Department of Marine Park Malaysia, Putrajaya

    Google Scholar 

  • Flower KR, Atkinson SR, Brainard R, Courtney C, Parker BA, Parks J, Pomeroy R, White A (2013) Toward ecosystem-based coastal areas and fisheries management in the Coral Triangle: integrated strategies and guidance. Coral Triangle Initiative Support Program for the U.S. Agency for International Development, Jakarta

  • Fukami H, Chen CA, Budd AF, Collins AG, Wallace CC, Chuang Y-Y, Dai C-F, Iwao K, Sheppard CRC, Knowlton N (2008) Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria). PLoS One 3:e3222. doi:10.1371/journal.pone.0003222

    PubMed Central  PubMed  Google Scholar 

  • Gittenberger A, Reijnen BT, Hoeksema BW (2011) A molecularly based phylogeny reconstruction of mushroom corals (Scleractinia: Fungiidae) with taxonomic consequences and evolutionary implications for life history traits. Contrib Zool 80:107–132

    Google Scholar 

  • Gordon AL, Fine RA (1996) Pathways of water between the Pacific and Indian oceans in the Indonesian seas. Nature 379:146–149. doi:10.1038/379146a0

    CAS  Google Scholar 

  • Gordon AL, Susanto RD, Vranes K (2003) Cool Indonesian throughflow as a consequence of restricted surface layer flow. Nature 425:824–828. doi:10.1038/nature02038

    CAS  PubMed  Google Scholar 

  • Hanebuth T, Stattegger K, Grootes PM (2000) Rapid flooding of the Sunda Shelf: a late-glacial sea-level record. Science 288:1033–1035. doi:10.1126/science.288.5468.1033

    CAS  PubMed  Google Scholar 

  • Harborne AR, Fenner DP, Barnes A, Beger M, Harding S, Roxburgh T (2000) Status report on the coral reefs of the east coast of Peninsula Malaysia. Coral Cay Conservation Ltd, London

    Google Scholar 

  • Harding S, Comley J, Helgeveld M, Coltman N, Raines P (2003) Malaysia reefs and islands conservation project 2003. Report of the marine pilot phase. A collaborative project between the Marine Parks Section, Department of Fisheries, Government of Malaysia and Coral Cay Conservation. Coral Cay Conservation Ltd, London

    Google Scholar 

  • Hodgson G, Dixon JA (2000) El Nido revisited: ecotourism, logging and fisheries. In: Cesar HSJ (ed) Collected essays on the economics of coral reefs. CORDIO, Kalmar, pp 55–68

    Google Scholar 

  • Hoeksema BW (1989) Taxonomy, phylogeny and biogeography of mushroom corals (Scleractinia: Fungiidae). Zool Verh Leiden 254:1–295

    Google Scholar 

  • Hoeksema BW (2007) Delineation of the Indo-Malayan centre of maximum marine biodiversity: the Coral Triangle. In: Renema W (ed) Biogeography, time, and place: distributions, barriers, and islands. Springer, Dordrecht, pp 117–178. doi:10.1007/978-1-4020-6374-9_5

    Google Scholar 

  • Hoeksema BW (2009) Attached mushroom corals (Scleractinia: Fungiidae) in sediment-stressed reef conditions at Singapore, including a new species and a new record. Raffles Bull Zool Suppl 22:81–90

    Google Scholar 

  • Hoeksema BW (2012) Forever in the dark: the cave-dwelling azooxanthellate reef coral Leptoseris troglodyta sp. n. (Scleractinia, Agariciidae). ZooKeys 228:21–37. doi:10.3897/zookeys.228.3798

    PubMed  Google Scholar 

  • Hoeksema BW (2014) The “Fungia patella group” (Scleractinia, Fungiidae) revisited with a description of the mini mushroom coral Cycloseris boschmai sp. n. ZooKeys 371:57–84. doi:10.3897/zookeys.371.6677

    PubMed  Google Scholar 

  • Hoeksema BW, Koh EGL (2009) Depauperation of the mushroom coral fauna (Fungiidae) of Singapore (1860s–2006) in changing reef conditions. Raffles Bull Zool Suppl 22:91–101

    Google Scholar 

  • Hoeksema BW, Dautova TN, Savinkin OV, Vo ST, Hoang XB, Phan KH, Hoang TD (2010) The westernmost record of the coral Leptoseris kalayaanensis in the South China Sea. Zool Stud 49:325

    Google Scholar 

  • Hoeksema BW, Matthews JL, Yeemin T (2012) The 2010 coral bleaching event and its impact on the mushroom coral fauna of Koh Tao, western Gulf of Thailand. Phuket Mar Biol Cent Res Bull 71:71–81

    Google Scholar 

  • Hooper JNA, Kennedy JA, van Soest RWM (2000) Annotated checklist of sponges (Porifera) of the South China Sea region. Raffles Bull Zool Suppl 8:125–207

    Google Scholar 

  • Huang H, Lian J, Huang X, Huang L, Zou R, Wang D (2006) Coral cover as a proxy of disturbance: a case study of the biodiversity of the hermatypic corals in Yongxing Island, Xisha Islands in the South China Sea. Chin Sci Bull 51:129–135. doi:10.1007/s11434-006-9129-4

    Google Scholar 

  • Huang D, Meier R, Todd PA, Chou LM (2009a) More evidence for pervasive paraphyly in scleractinian corals: systematic study of Southeast Asian Faviidae (Cnidaria; Scleractinia) based on molecular and morphological data. Mol Phylogenet Evol 50:102–116. doi:10.1016/j.ympev.2008.10.012

    CAS  PubMed  Google Scholar 

  • Huang D, Tun KPP, Chou LM, Todd PA (2009b) An inventory of zooxanthellate scleractinian corals in Singapore, including 33 new records. Raffles Bull Zool Suppl 22:69–80

    CAS  Google Scholar 

  • Huang H, Ma B, Lian J, Yang J, Dong Z, Fu Q, Liang W (2009c) Status and conservation strategies of the coral reef in Weizhou Island, Guangxi. Trop Geogr 29:307–312

    Google Scholar 

  • Huang D, Licuanan WY, Baird AH, Fukami H (2011a) Cleaning up the ‘Bigmessidae’: molecular phylogeny of scleractinian corals from Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae. BMC Evol Biol 11:37. doi:10.1186/1471-2148-11-37

    PubMed Central  PubMed  Google Scholar 

  • Huang H, You F, Lian J, Yang J, Li X, Dong Z, Zhang C, Yuan T (2011b) Species diversity and distribution of scleractinian coral at Xisha Islands, China. Biodivers Sci 19:710–715. doi:10.3724/SP.J.1003.2011.06132

    Google Scholar 

  • Huang H, Zhang Y, Lian J, Li X, You F, Yang J, Lei X, Zhang C (2011c) Structure and diversity of Scleractinia coral communities along the west seashore of Xuwen County. Biodivers Sci 19:505–510. doi:10.3724/SP.J.1003.2011.06055

    Google Scholar 

  • Huang H, Chen J, Sheng M, Chen Z (2012a) Preliminary report on the scientific survey of the protected coral reefs of Dongshan, Fujian [in Chinese]. South China Sea Institute of Oceanology, Guangzhou

    Google Scholar 

  • Huang H, You F, Lian J, Zhang C, Yang J, Li X, Yuan T, Dong Z (2012b) Composition and distribution of scleractinian coral in the northwest of Hainan island. Mar Sci 36:64–74

    Google Scholar 

  • Huang H, You F, Lian J, Zhang C, Yang J, Li X, Yuan T, Zhang Y, Zhou G (2012c) Status and conservation strategies of the scleractinian coral community in the Wanshan Islands at Pearl River Estuary. Mar Sci Bull 31:189–197

    Google Scholar 

  • Huang H, Zhang C, Yang J, You F, Lian J, Tan Y (2012d) Scleractinian coral community characteristics in Zhubi reef sea area of Nansha Islands. J Oceanogr Taiwan St 31:79–84

    Google Scholar 

  • Huang D, Benzoni F, Fukami H, Knowlton N, Smith ND, Budd AF (2014) Taxonomic classification of the reef coral families Merulinidae, Montastraeidae and Diploastraeidae (Cnidaria: Anthozoa: Scleractinia). Zool J Linn Soc. doi:10.1111/zoj.12140

  • Hughes TP, Bellwood DR, Connolly SR (2002) Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecol Lett 5:775–784. doi:10.1046/j.1461-0248.2002.00383.x

    Google Scholar 

  • Hughes TP, Connolly SR, Keith SA (2013) Geographic ranges of reef corals (Cnidaria: Anthozoa: Scleractinia) in the Indo-Pacific. Ecology 94:1659. doi:10.1890/13-0361.1

    Google Scholar 

  • Humphries UW, Webb DJ (2008) On the Indonesian throughflow in the OCCAM 1/4 degree ocean model. Ocean Sci 4:183–198

    Google Scholar 

  • Jiravat V (1985) Taxonomic study of stony corals collected from the Gulf of Thailand. Dissertation, Chulalongkorn University, Bangkok

  • Jokiel PL, Martinelli FJ (1992) The vortex model of coral reef biogeography. J Biogeogr 19:449–458. doi:10.2307/2845572

  • Jones DS, Hewitt MA, Sampey A (2000) A checklist of the Cirripedia of the South China Sea. Raffles Bull Zool Suppl 8:233–307

    Google Scholar 

  • Kahng SE, Maragos JE (2006) The deepest, zooxanthellate scleractinian corals in the world? Coral Reefs 25:254. doi:10.1007/s00338-006-0098-5

  • Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275. doi:10.1007/s00338-010-0593-6

    Google Scholar 

  • Karlson RH, Cornell HV (1998) Scale-dependent variation in local vs. regional effects on coral species richness. Ecol Monogr 68:259–274

    Google Scholar 

  • Keshavmurthy S, Yang S-Y, Alamaru A, Chuang Y-Y, Pichon M, Obura DO, Fontana S, De Palmas S, Stefani F, Benzoni F, MacDonald A, Noreen AME, Chen C, Wallace CC, Moothein Pillay R, Denis V, Affendi YA, Reimer JD, Mezaki T, Sheppard CRC, Loya Y, Abelson A, Mohammed MA, Baker AC, Mostafavi PG, Suharsono BA, Chen CA (2013) DNA barcoding reveals the coral ‘laboratory-rat’, Stylophora pistillata encompasses multiple identities. Sci Rep 3:1520. doi:10.1038/srep01520

    PubMed Central  PubMed  Google Scholar 

  • Kimura T, Dai C-F, Park H-S, Huang H, Ang PO (2008) Status of coral reefs in East and North Asia (China, Hong Kong, Taiwan, South Korea and Japan). In: Wilkinson C (ed) Status of the coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, pp 145–158

    Google Scholar 

  • Komai T (2000) A check list of Thalassinidea and Anomura (Crustacea: Decapoda) from the South China Sea. Raffles Bull Zool Suppl 8:343–376

    Google Scholar 

  • Kongjandtre N, Ridgway T, Ward S, Hoegh-Guldberg O (2010) Broadcast spawning patterns of Favia species on the inshore reefs of Thailand. Coral Reefs 29:227–234. doi:10.1007/s00338-009-0551-3

    Google Scholar 

  • Kongjandtre N, Ridgway T, Cook LG, Huelsken T, Budd AF, Hoegh-Guldberg O (2012) Taxonomy and species boundaries in the coral genus Favia Milne Edwards and Haime, 1857 (Cnidaria: Scleractinia) from Thailand revealed by morphological and genetic data. Coral Reefs 31:581–601. doi:10.1007/s00338-011-0869-5

    Google Scholar 

  • Kruskal JB (1964a) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27. doi:10.1007/BF02289565

    Google Scholar 

  • Kruskal JB (1964b) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115–129. doi:10.1007/BF02289694

    Google Scholar 

  • Lambert JH (1772) Anmerkungen und Zusätze zur Entwerfung der Land- und Himmelscharten. Herausgegeben von A. Wangerin (1894). Wilhelm Engelmann, Leipzig

  • Lane DJW, Marsh LM, Van den Spiegel D, Rowe FWE (2000) Echinoderm fauna of the South China Sea: an inventory and analysis of distribution patterns. Raffles Bull Zool Suppl 8:459–493

    Google Scholar 

  • Latypov YY (1986) Coral communities of the Namsu Islands (Gulf of Siam, South China Sea). Mar Ecol-Prog Ser 29:261–270

    Google Scholar 

  • Latypov YY (2006) Scleractinian corals of Vietnam. A. V. Zhirmunsky Institute of Marine Biology, Vladivostok

    Google Scholar 

  • Latypov YY (2011) Scleractinian corals and reefs of Vietnam as a part of the Pacific reef ecosystem. Open J Mar Sci 1:50–68. doi:10.4236/ojms.2011.12006

    Google Scholar 

  • Latypov YY (2012) Encrusting protected reef Hon Nai in Cam Ranh Bay in the South China Sea. Nat Sci 4:14–21. doi:10.4236/ns.2012.41003

    Google Scholar 

  • Latypov YY (2013) Favia camranensis sp. n. (Scleractinia: Faviidae), a new coral species from southern Vietnam. Russ J Mar Biol 39:223–224. doi:10.1134/S1063074013030085

    Google Scholar 

  • Li J-J, Lee T-F, Tew KS, Fang L-S (2000) Changes in the coral community at Dong-Sha Atoll, South China Sea from 1975 to 1998. Acta Zool Taiwan 11:1–15

    Google Scholar 

  • Licuanan WY (2009) Guide to the common corals of the Bolinao-Anda reef complex, northwestern Philippines. U.P. Marine Science Institute, Diliman

    Google Scholar 

  • Licuanan WY, Aliño PM (2009) Leptoseris kalayaanensis (Scleractinia: Agariciidae), a new coral species from the Philippines. Raffles Bull Zool 57:1–4

    Google Scholar 

  • Lin M-F, Luzon KS, Licuanan WY, Ablan-Lagman MC, Chen CA (2011) Seventy-four universal primers for characterizing the complete mitochondrial genomes of scleractinian corals (Cnidaria; Anthozoa). Zool Stud 50:513–524

    CAS  Google Scholar 

  • Lin M-F, Kitahara MV, Tachikawa H, Fukami H, Miller DJ, Chen CA (2012a) Novel organization of the mitochondrial genome in the deep-sea coral, Madrepora oculata (Hexacorallia, Scleractinia, Oculinidae) and its taxonomic implications. Mol Phylogenet Evol 65:323–328. doi:10.1016/j.ympev.2012.06.011

    PubMed  Google Scholar 

  • Lin M-F, Kitahara MV, Tachikawa H, Keshavmurthy S, Chen CA (2012b) A new shallow-water species, Polycyathus chaishanensis sp. nov. (Scleractinia: Caryophylliidae), from Chaishan, Kaohsiung, Taiwan. Zool Stud 51:213–221

    Google Scholar 

  • Lowry JK (2000) Taxonomic status of amphipod crustaceans in the South China Sea with a checklist of known species. Raffles Bull Zool Suppl 8:309–342

    Google Scholar 

  • Luck DG, Forsman ZH, Toonen RJ, Leicht SJ, Kahng SE (2013) Polyphyly and hidden species among Hawai’i’s dominant mesophotic coral genera, Leptoseris and Pavona (Scleractinia: Agariciidae). PeerJ 1:e132. doi:10.7717/peerj.132

    PubMed Central  PubMed  Google Scholar 

  • Lukas R, Yamagata T, McCreary JP (1996) Pacific low-latitude western boundary currents and the Indonesian throughflow. J Geophys Res 101:12209–12216. doi:10.1029/96JC01204

    Google Scholar 

  • McManus JW (1985) Marine speciation, tectonics and sea-level changes in Southeast Asia. Proc 5th Int Coral Reef Symp 4:133–138

    Google Scholar 

  • McManus JW (1994) The Spratly Islands: a marine park? Ambio 23:181–186

    Google Scholar 

  • McManus JW (1997) Tropical marine fisheries and the future of coral reefs: a brief review with emphasis on Southeast Asia. Coral Reefs 16:S121–S127. doi:10.1007/s003380050248

    Google Scholar 

  • McManus JW, Meñez LAB (1997) The proposed international Spratly Island marine park: ecological considerations. Proc 8th Int Coral Reef Symp 2:1943–1948

    Google Scholar 

  • McManus JW, Shao K-T, Lin S-Y (2010) Toward establishing a Spratly Islands international Marine Peace Park: ecological importance and supportive collaborative activities with an emphasis on the role of Taiwan. Ocean Dev Int Law 41:270–280. doi:10.1080/00908320.2010.499303

    Google Scholar 

  • Minchin PR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69:89–107. doi:10.1007/BF00038690

    Google Scholar 

  • Moosa MK (2000) Marine biodiversity of the South China Sea: a checklist of stomatopod Crustacea. Raffles Bull Zool Suppl 8:405–457

    Google Scholar 

  • Morton B, Blackmore G (2001) South China Sea. Mar Poll Bull 42:1236–1263

    CAS  Google Scholar 

  • Napitupulu L, Cruz-Trinidad A, Titaningtyas (2012) The worth of coastal ecosystems in the Coral Triangle. Proc 12th Int Coral Reef Symp 22D:3

  • Ng PKL, Tan KS (2000) The state of marine biodiversity in the South China Sea. Raffles Bull Zool Suppl 8:3–7

    Google Scholar 

  • Nguyen HY, Dang NT (2008) Biological resources and ecosystems in Spratly Archipelago [in Vietnamese]. Publishing House of Natural Science and Technology, Hanoi

    Google Scholar 

  • Norman MD, Lu CC (2000) Preliminary checklist of the cephalopods of the South China Sea. Raffles Bull Zool Suppl 8:539–567

    Google Scholar 

  • Nyanti L, Johnston NA (1992) The coral reefs of the Tunku Abdul Rahman Park, Sabah. Sabah Soc J 9:323–348

    Google Scholar 

  • Obura DO (2012) Evolutionary mechanisms and diversity in a western Indian Ocean center of diversity. Proc 12th Int Coral Reef Symp 3A:2

  • Obura DO (2012b) The diversity and biogeography of Western Indian Ocean reef-building corals. PLoS One 7:e45013. doi:10.1371/journal.pone.0045013

    CAS  PubMed Central  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R package version 2.0-8

  • Pandolfi JM (1992) Successive isolation rather than evolutionary centres for the origination of Indo-Pacific reef corals. J Biogeogr 19:593–609. doi:10.2307/2845703

    Google Scholar 

  • Paxton H, Chou LM (2000) Polychaetous annelids from the South China Sea. Raffles Bull Zool Suppl 8:209–232

    Google Scholar 

  • Pernetta JC (2009) Terminal report of the UNEP/GEF Project: reversing environmental degradation trends in the South China Sea and Gulf of Thailand. UNEP/GEF, Bangkok

    Google Scholar 

  • Phan KH (2012) Hard coral in the waters bordering Phu Qui Island, Binh Thuan Province [in Vietnamese]. International conference on Bien Dong, Nha Trang, Vietnam, 13 September 2012

  • Phan KH, Vo ST (2010) Coral communities in the coastal waters of Phu Yen Province [in Vietnamese]. Coll Mar Res Works 17:155–166

    Google Scholar 

  • Pichon M (2007) Scleractinia of New Caledonia: check list of reef dwelling species. In: Payri C, de Forges BR (eds) Compendium of marine species of New Caledonia, 2nd edn. Institut de Recherche pour le Développement, Nouméa, pp 149–157

    Google Scholar 

  • Pichon M, Benzoni F (2007) Taxonomic re-appraisal of zooxanthellate scleractinian corals in the Maldive Archipelago. Zootaxa 1441:21–33

    Google Scholar 

  • Pichon M, Chuang Y-Y, Chen CA (2012) Pseudosiderastrea formosa sp. nov. (Cnidaria: Anthozoa: Scleractinia) a new coral species endemic to Taiwan. Zool Stud 51:93–98

    Google Scholar 

  • Pitcher TJ, Watson R, Haggan N, Guénette S, Kennish R, Sumaila UR, Cook D, Wilson K, Leung A (2000) Marine reserves and the restoration of fisheries and marine ecosystems in the South China Sea. Bull Mar Sci 66:543–566

    Google Scholar 

  • Potts DC (1983) Evolutionary disequilibrium among Indo-Pacific corals. Bull Mar Sci 33:619–632

    Google Scholar 

  • Putchim L, Chavanich S, Viyakarn V (2002) Species diversity of mushroom corals (family Fungiidae) in the inner Gulf of Thailand. Nat Hist J Chulalongkorn Univ 2:47–49

    Google Scholar 

  • Qu T (2000) Upper-layer circulation in the South China Sea. J Phys Oceanogr 30:1450–1460. doi:10.1175/1520-0485(2000)030<1450:ULCITS>2.0.CO;2

    Google Scholar 

  • Qu T, Du Y, Meyers G, Ishida A, Wang D (2005) Connecting the tropical Pacific with Indian Ocean through South China Sea. Geophys Res Lett 32, L24609. doi:10.1029/2005GL024698

    Google Scholar 

  • Rahayu DL (2000) Hermit crabs from the South China Sea (Crustacea: Decapoda: Anomura: Diogenidae, Paguridae, Parapaguridae). Raffles Bull Zool Suppl 8:377–404

    Google Scholar 

  • Randall JE, Lim KKP (2000) A checklist of the fishes of the South China Sea. Raffles Bull Zool Suppl 8:569–667

    Google Scholar 

  • Renema W, Bellwood DR, Braga JC, Bromfield K, Hall R, Johnson KG, Lunt P, Meyer CP, McMonagle LB, Morley RJ, O’Dea A, Todd JA, Wesselingh FP, Wilson MEJ, Pandolfi JM (2008) Hopping hotspots: global shifts in marine biodiversity. Science 321:654–657. doi:10.1126/science.1155674

  • Rosen BR (1984) Reef coral biogeography and climate through the late Cainozoic: just islands in the sun or a critical pattern of islands? In: Brenchley P (ed) Fossils and climate. Wiley, Chichester, pp 201–262

    Google Scholar 

  • Rosen BR (1988) Progress, problems and patterns in the biogeography of reef corals and other tropical marine organisms. Helgol Mar Res 42:269–301

    Google Scholar 

  • Sachidhanandam U, Willan RC, Chou LM (2000) Checklist of the nudibranchs (Opisthobranchia: Nudibranchia) of the South China Sea. Raffles Bull Zool Suppl 8:513–537

    Google Scholar 

  • Saenghaisuk C, Yeemin T (2009) A study on determination of rare coral species at Koh Kood, Gulf of Thailand. In: Proceedings of the 35th congress on science and technology of Thailand. pp 1–5

  • Sakai K, Yeemin T, Snidvongs A, Yamazato K, Nishihira M (1986) Distribution and community structure of hermatypic corals in the Sichang Islands, inner part of the Gulf of Thailand. Galaxea 5:27–74

    Google Scholar 

  • Sanciangco JC, Carpenter KE, Etnoyer PJ, Moretzsohn F (2013) Habitat availability and heterogeneity and the Indo-Pacific warm pool as predictors of marine species richness in the tropical Indo-Pacific. PLoS One 8:e56245. doi:10.1371/journal.pone.0056245

    CAS  PubMed Central  PubMed  Google Scholar 

  • Santini F, Winterbottom R (2002) Historical biogeography of Indo-western Pacific coral reef biota: is the Indonesian region a centre of origin? J Biogeogr 29:189–205

    Google Scholar 

  • Scheer G, Pillai CSG (1974) Report on the Scleractinia from the Nicobar Islands. Zoologica 42:1–198

    Google Scholar 

  • Scheltema RS (1986) Long-distance dispersal by planktonic larvae of shoal-water benthic invertebrates among central Pacific islands. Bull Mar Sci 39:241–256

    Google Scholar 

  • Scheltema RS (1988) Initial evidence for the transport of teleplanic larvae of benthic invertebrates across the east Pacific barrier. Biol Bull 174:145–152

    Google Scholar 

  • Scheltema RS, Williams IP (1983) Long-distance dispersal of planktonic larvae and the biogeography and evolution of some Polynesian and western Pacific mollusks. Bull Mar Sci 33:545–565

    Google Scholar 

  • Shen JW, Yang HQ, Wang Y, Fu FX, Zhao N (2013) Coral community dynamics and shallow-water carbonate deposition of the reef-flat around Yongxing Island, the Xisha Islands. Sci China Earth Sci 56:1471–1486. doi:10.1007/s11430-013-4677-3

    CAS  Google Scholar 

  • Sheppard CRC (1987) Coral species of the Indian Ocean and adjacent seas: a synonymized compilation and some regional distributional patterns. Atoll Res Bull 307:1–32

    Google Scholar 

  • Siddall M, Rohling EJ, Almogi-Labin A, Hemleben C, Meischner D, Schmelzer I, Smeed DA (2003) Sea-level fluctuations during the last glacial cycle. Nature 423:853–858. doi:10.1038/nature01690

    CAS  PubMed  Google Scholar 

  • Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. University of California Press, Berkeley

    Google Scholar 

  • Spalding MD, Fox HE, Allen GR, Davidson N, Ferdana ZA, Finlayson M, Halpern BS, Jorge MA, Lombana AL, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583. doi:10.1641/B570707

    Google Scholar 

  • Srithunya S, Muchacheep S, Srirattanachai S, Harden V (1981) Pattern of distribution and correlated parameters of corals in coral reefs at Koa Larn, Chonburi, Thailand (a preliminary report). Proc 4th Int Coral Reef Symp 2:309–313

    Google Scholar 

  • Stefani F, Benzoni F, Yang SY, Pichon M, Galli P, Chen CA (2011) Comparison of morphological and genetic analyses reveals cryptic divergence and morphological plasticity in Stylophora (Cnidaria, Scleractinia). Coral Reefs 30:1033–1049. doi:10.1007/s00338-011-0797-4

    Google Scholar 

  • Talaue-McManus L (2000) Transboundary diagnostic analysis for the South China Sea. UNEP, Bangkok

    Google Scholar 

  • Tan KS (2000) Species checklist of Muricidae (Mollusca: Gastropoda) in the South China Sea. Raffles Bull Zool Suppl 8:495–512

    Google Scholar 

  • Taylor B, Hayes DE (1983) Origin and history of the South China Sea basin. In: Hayes DE (ed) The tectonic and geologic evolution of Southeast Asian seas and islands: part 2. American Geophysical Union, Washington, DC, pp 23–56

    Google Scholar 

  • Tun KPP, Chou LM, Yeemin T, Affendi YA, Ho N, Sour K, Nguyen VL, Nanola CL Jr, Lane DJW, Tuti Y (2008) Status of coral reefs in Southeast Asia. In: Wilkinson C (ed) Status of the coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, pp 131–144

    Google Scholar 

  • Turak E, DeVantier LM (2010) Marine tourism, coral biodiversity and conservation priorities in El Nido, Palawan. El Nido Foundation, El Nido

    Google Scholar 

  • Turak E, DeVantier LM (2011) Field guide to reef-building corals of Brunei Darussalam. Fisheries Department, Ministry of Industry and Primary Resources, Bandar Seri Begawan

    Google Scholar 

  • Umbgrove JHF (1947) Coral reefs of the East Indies. Geol Soc Am Bull 58:729–778. doi:10.1130/0016-7606(1947)58[729:CROTEI]2.0.CO;2

    Google Scholar 

  • UNEP (2004) Coral reefs in the South China Sea. UNEP/GEF/SCS, Bangkok

    Google Scholar 

  • Veron JEN (1995) Corals in space and time. UNSW Press, Sydney

    Google Scholar 

  • Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville

    Google Scholar 

  • Veron JEN (2002) New species described in ‘Corals of the world’. Australian Institute of Marine Science, Townsville

    Google Scholar 

  • Veron JEN, Hodgson G (1989) Annotated checklist of the hermatypic corals of the Philippines. Pac Sci 43:234–287

    Google Scholar 

  • Veron JEN, Pichon M (1976) Scleractinia of eastern Australia. Part I. Families Thamnasteriidae, Astrocoeniidae, Pocilloporidae. AIMS Monogr Ser 1:1–86

    Google Scholar 

  • Veron JEN, Pichon M (1980) Scleractinia of eastern Australia. Part III. Families Agariciidae, Siderastreidae, Fungiidae, Oculinidae, Merulinidae, Mussidae, Pectiniidae, Caryophylliidae, Dendrophylliidae. AIMS Monogr Ser 4:1–459

    Google Scholar 

  • Veron JEN, Pichon M (1982) Scleractinia of eastern Australia. Part IV. Family Poritidae. AIMS Monogr Ser 5:1–159

    Google Scholar 

  • Veron JEN, Wallace CC (1984) Scleractinia of eastern Australia. Part V. Family Acroporidae. AIMS Monogr Ser 6:1–485

    Google Scholar 

  • Veron JEN, Pichon M, Wijsman-Best M (1977) Scleractinia of eastern Australia. Part II. Families Faviidae, Trachyphylliidae. AIMS Monogr Ser 3:1–233

    Google Scholar 

  • Veron JEN, DeVantier LM, Turak E, Green AL, Kininmonth S, Stafford-Smith MG, Peterson N (2009) Delineating the Coral Triangle. Galaxea 11:91–100. doi:10.3755/galaxea.11.91

    Google Scholar 

  • Veron JEN, DeVantier LM, Turak E, Green AL, Kininmonth S, Stafford-Smith MG, Peterson N (2011) The Coral Triangle. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 47–55

    Google Scholar 

  • Vo ST (1998) Hermatypic Scleractinia of South Vietnam. In: Third international conference on the marine biology of the South China Sea, Hong Kong, 28 October – 1 November 1996. pp 11–20

  • Vo ST, Hodgson G (1997) Coral reefs of Vietnam: recruitment limitation and physical forcing. Proc 8th Int Coral Reef Symp 1:477–482

    Google Scholar 

  • Vo ST, Nguyen HY (2010) Hermatypic corals in the waters bordering Con Co Island (Quang Tri Province) [in Vietnamese]. Coll Mar Res Works 17:147–154

    Google Scholar 

  • Vo ST, Phan KH (1997) Species composition of Scleractinia from the coastal waters of South Vietnam [in Vietnamese]. Coll Mar Res Works 7:194–204

    Google Scholar 

  • Vo ST, DeVantier LM, Nguyen VL, Hua TT, Nguyen XH, Phan KH (2004) Coral reefs of Hon Mun marine protected area, Nha Trang Bay, Vietnam: 2002. Species composition, community structure, status and management recommendations. In: Proceedings of the scientific conference ‘Bien Dong – 2002’. Agricultural Publishing House, pp 649–690

  • Vo ST, Pernetta JC, Paterson CJ (2013) Status and trends in coastal habitats of the South China Sea. Ocean Coast Manag 85:153–163. doi:10.1016/j.ocecoaman.2013.02.018

    Google Scholar 

  • Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167

    Google Scholar 

  • Wafar M, Venkataraman K, Ingole B, Khan SA, LokaBharathi P (2011) State of knowledge of coastal and marine biodiversity of Indian Ocean countries. PLoS One 6:e14613. doi:10.1371/journal.pone.0014613

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waheed Z, Hoeksema BW (2013) A tale of two winds: species richness patterns of reef corals around the Semporna peninsula, Malaysia. Mar Biodivers 43:37–51. doi:10.1007/s12526-012-0130-7

    Google Scholar 

  • Waheed Z, Hoeksema BW (2014) Diversity patterns of scleractinian corals at Kota Kinabalu, Malaysia, in relation to exposure and depth. Raffles Bull Zool 62:66–82

  • Waheed Z, Rahman RA, Ariff AJ (2012) The status of hard coral diversity in Sabah. In: Kamarruddin I, Mohamed CAR, Rozaimi MJ, Kee Alfian AA, Fitra AZ, Lee JN (eds) Malaysia’s marine biodiversity: inventory and current status. Department of Marine Park Malaysia, Putrajaya, pp 1–19

    Google Scholar 

  • Wallace CC (1999) Staghorn corals of the world: a revision of the coral genus Acropora. CSIRO Publishing, Collingwood

    Google Scholar 

  • Wallace CC, Chen CA, Fukami H, Muir PR (2007) Recognition of separate genera within Acropora based on new morphological, reproductive and genetic evidence from Acropora togianensis, and elevation of the subgenus Isopora Studer, 1878 to genus (Scleractinia: Astrocoeniidae; Acroporidae). Coral Reefs 26:231–239. doi:10.1007/s00338-007-0203-4

    Google Scholar 

  • Wallace CC, Done BJ, Muir PR (2012a) Revision and catalogue of worldwide staghorn corals Acropora and Isopora (Scleractinia: Acroporidae) in the Museum of Tropical Queensland. Mem Qld Mus 57:1–255

    Google Scholar 

  • Wallace CC, Phongsuwan N, Muir PR (2012b) A new species of staghorn coral, Acropora sirikitiae sp. nov. (Scleractinia: Astrocoeniina: Acroporidae) from western Thailand. Phuket Mar Biol Cent Res Bull 71:117–125

    Google Scholar 

  • Wells JW (1935) The genotype of Physophyllia and a living species of Astrocoenia. Ann Mag Nat Hist Ser 10 15:339–344. doi:10.1080/00222933508654971

    Google Scholar 

  • Whitaker D, Christman M (2010) Clustsig: similarity profile analysis. R package version 1.0

  • Wilson MEJ, Rosen BR (1998) Implications of paucity of corals in the Paleogene of SE Asia: plate tectonics or Centre of Origin? In: Hall R, Holloway JD (eds) Biogeography and geological evolution of SE Asia. Backhuys Publishers, Leiden, pp 165–195

    Google Scholar 

  • Wood S, Paris CB, Ridgwell A, Hendy EJ (2014) Modelling dispersal and connectivity of broadcast spawning corals at the global scale. Glob Ecol Biogeogr 23:1–11. doi:10.1111/geb.12101

    Google Scholar 

  • Wyrtki K (1961) Physical oceanography of the Southeast Asian waters. Scientific results of marine investigations of the South China Sea and the Gulf of Thailand 1959–1961. NAGA report volume 2. Scripps Institution of Oceanography, La Jolla

  • Xu D, Malanotte-Rizzoli P (2013) The seasonal variation of the upper layers of the South China Sea (SCS) circulation and the Indonesian through flow (ITF): an ocean model study. Dyn Atmos Oceans 63:103–130. doi:10.1016/j.dynatmoce.2013.05.002

    Google Scholar 

  • Yabe H, Sugiyama T (1932) Reef corals found in the Japanese seas. Sci Rep Tôhoku Imp Univ 2nd Ser (Geol) 15:145–168

    Google Scholar 

  • Yeemin T (2001) Community structure and biodiversity of scleractinian corals at Koh Ram Ra, Prachuap Khiri Khan Province. Scientific report submitted to the Office of National Research Council of Thailand [in Thai]. Ramkhamhaeng University, Bangkok

  • Yeemin T (2002) Natural recovery of coral communities in tourism areas of Koh Tao Groups, Surat Thani Province. Scientific report submitted to the Office of National Research Council of Thailand [in Thai]. Ramkhamhaeng University, Bangkok

  • Yeemin T (2003) Status and natural recovery of coral communities at Koh Saked, Rayong Province. Scientific report submitted to Coral and Beach Conservation-Restoration Foundation, Industrial Estate Authority of Thailand [in Thai]. Ramkhamhaeng University, Bangkok

  • Yeemin T, Sudara S, Chamapun A (1994) A quantitative study of the scleractinian coral communities of Tao Island, Gulf of Thailand. In: Third ASEAN-Australia symposium on living coastal resources, Chulalongkorn University, Bangkok, 16–20 May 1994. pp 149–155

  • Yusuf Y, Affendi YA (2009) The marine habitat and resources of Batuan Tengah (Middle Rocks), Johor, Malaysia. A report submitted to the National Oceanography Directorate. Ministry of Sciences, Technology and Innovation, Malaysia, Putrajaya

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Acknowledgments

We thank Emre Turak and Lyndon DeVantier for providing unpublished data. Kari Ellingsen and an anonymous reviewer provided comments that helped improve the manuscript. DH is supported by US National Science Foundation grant DEB-1145043-1145408, POA by Hong Kong RGC GRF 460013, and STV by the Vietnam National Foundation for Science and Technology Development project 106.14-2010.67.

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Huang, D., Licuanan, W.Y., Hoeksema, B.W. et al. Extraordinary diversity of reef corals in the South China Sea. Mar Biodiv 45, 157–168 (2015). https://doi.org/10.1007/s12526-014-0236-1

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