Conservation of reef corals in the South China Sea based on species and evolutionary diversity

Biodiversity and Conservation

Volumn 25, Issue 2, 2016, Pages 331-344

  Huang, Danwei ^a   Hoeksema, Bert W ^b   Affendi, Yang Amri ^c   Ang, Put O ^d   Chen, Chaolun A ^e,f   Huang, Hui ^g,h   Lane, David J W ⁱ   Licuanan, Wilfredo Y ^j   Vibol, Ouk ^k   Vo, Si Tuan ^l   Yeemin, Thamasak ^m   Chou, Loke Ming ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATURALIS BIODIVERSITY CENTER   (Netherlands)

^c UNIVERSITY OF MALAYA   (Malaysia)

^d CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^e BIODIVERSITY RESEARCH CENTER   (Taiwan)

^f NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^g Tropical Marine Biological Research Station in Hainan   (China)

^h SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

ⁱ UNIVERSITI BRUNEI DARUSSALAM   (Brunei Darussalam)

^j DE LA SALLE UNIVERSITY   (Philippines)

^k Ministry of Agriculture   (Cambodia)

^l GRADUATE UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Viet Nam)

^m RAMKHAMHAENG UNIVERSITY   (Thailand)

more..

Author keywords

IUCN Red List; Marine biodiversity; Phylogenetic diversity; Rarity; Scleractinia; Species richness

Indexed keywords

BIODIVERSITY; CONSERVATION PLANNING; CONSERVATION STATUS; CORAL REEF; EXTINCTION RISK; GLOBAL CLIMATE; MARINE ENVIRONMENT; PHYLOGENETICS; PROTECTED AREA; RARITY; RED LIST; SPECIES DIVERSITY; SPECIES RICHNESS;

INDIAN OCEAN; MALAYSIA; PACIFIC OCEAN; PACIFIC OCEAN (CENTRAL); PARACEL ISLANDS; PHILIPPINES; SOUTH CHINA SEA; VIET NAM; WEST MALAYSIA;

ANTHOZOA; SCLERACTINIA;

EID: 84957956782     PISSN: 09603115     EISSN: 15729710     Source Type: Journal    
DOI: 10.1007/s10531-016-1052-7     Document Type: Article

References (99)

1. Altschul SF, Lipman DL (1990) Equal Anim. Nature 348:493–494. doi:10.1038/348493c0
2. Arponen A (2012) Prioritizing species for conservation planning. Biodivers Conserv 21:875–893. doi:10.1007/s10531-012-0242-1
3. Barbeitos MS, Romano SL, Lasker HR (2010) Repeated loss of coloniality and symbiosis in scleractinian corals. Proc Natl Acad Sci USA 107:11877–11882. doi:10.1073/pnas.0914380107
4. Beger M, McGowan J, Treml EA et al (2015) Integrating regional conservation priorities for multiple objectives into national policy. Nat Commun 6:8208. doi:10.1038/ncomms9208
5. Bellwood DR, Hoey AS, Choat JH (2003) Limited functional redundancy in high diversity systems: resilience and ecosystem function on coral reefs. Ecol Lett 6:281–285. doi:10.1046/j.1461-0248.2003.00432.x
6. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833. doi:10.1038/nature02691
7. Bellwood DR, Hughes TP, Hoey AS (2006) Sleeping functional group drives coral-reef recovery. Curr Biol 16:2434–2439. doi:10.1016/j.cub.2006.10.030
8. Bennett JR, Elliott G, Mellish B et al (2014) Balancing phylogenetic diversity and species numbers in conservation prioritization, using a case study of threatened species in New Zealand. Biol Conserv 174:47–54. doi:10.1016/j.biocon.2014.03.013
9. Cadotte MW (2013) Experimental evidence that evolutionarily diverse assemblages result in higher productivity. Proc Natl Acad Sci USA 110:8996–9000. doi:10.1073/pnas.1301685110
10. Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. Proc Natl Acad Sci USA 105:17012–17017. doi:10.1073/pnas.0805962105
11. Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087. doi:10.1111/j.1365-2664.2011.02048.x
12. Carpenter KE, Abrar M, Aeby GS et al (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563. doi:10.1126/science.1159196
13. Chong-Seng KM, Mannering TD, Pratchett MS et al (2012) The influence of coral reef benthic condition on associated fish assemblages. PLoS One 7:e42167. doi:10.1371/journal.pone.0042167
14. 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
15. Curnick DJ, Head CEI, Huang D et al (2015) Setting evolutionary-based conservation priorities for a phylogenetically data-poor taxonomic group (Scleractinia). Anim Conserv 18:303–312. doi:10.1111/acv.12185
16. D’agata S, Mouillot D, Kulbicki M et al (2014) Human-mediated loss of phylogenetic and functional diversity in coral reef fishes. Curr Biol 24:555–560. doi:10.1016/j.cub.2014.01.049
17. Darling ES, Alvarez-Filip L, Oliver TA et al (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386. doi:10.1111/j.1461-0248.2012.01861.x
18. Darling ES, McClanahan TR, Côté IM (2013) Life histories predict coral community disassembly under multiple stressors. Glob Chang Biol 19:1930–1940. doi:10.1111/gcb.12191
19. Davies TJ, Fritz SA, Grenyer R et al (2008) Phylogenetic trees and the future of mammalian biodiversity. Proc Natl Acad Sci USA 105:11556–11563. doi:10.1073/pnas.0801917105
20. Devictor V, Mouillot D, Meynard C et al (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 3:1030–1040. doi:10.1111/j.1461-0248.2010.01493.x
21. Díaz M, Madin JS (2011) Macroecological relationships between coral species’ traits and disease potential. Coral Reefs 30:73–84. doi:10.1007/s00338-010-0668-4
22. Fabricius KE, De’ath G, Noonan S, Uthicke S (2014) Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc Roy Soc B-Biol Sci 281:20132479. doi:10.1098/rspb.2013.2479
23. Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. doi:10.1016/0006-3207(92)91201-3
24. Faith DP, Magallón S, Hendry AP et al (2010) Evosystem services: an evolutionary perspective on the links between biodiversity and human well-being. Curr Opin Environ Sustain 2:66–74. doi:10.1016/j.cosust.2010.04.002
25. Flynn DFB, Mirotchnick N, Jain M et al (2011) Functional and phylogenetic diversity as predictors of biodiversity–ecosystem-function relationships. Ecology 92:1573–1581. doi:10.1890/10-1245.1
26. Forest F, Grenyer R, Rouget M et al (2007) Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445:757–760. doi:10.1038/nature05587
27. Fritz SA, Purvis A (2010) Phylogenetic diversity does not capture body size variation at risk in the world’s mammals. Proc Roy Soc B 277:2435–2441. doi:10.1098/rspb.2010.0030
28. Gaston KJ (1994) Rarity. Chapman & Hall, London
29. 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
30. Graham NAJ, Wilson SK, Jennings S et al (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci USA 103:8425–8429. doi:10.1073/pnas.0600693103
31. Harnik PG, Simpson C, Payne JL (2012) Long-term differences in extinction risk among the seven forms of rarity. Proc Roy Soc B 279:4969–4976. doi:10.1098/rspb.2012.1902
32. Hoeksema BW (1989) Taxonomy, phylogeny and biogeography of mushroom corals (Scleractinia: Fungiidae). Zool Verh Leiden 254:1–295
33. Hoeksema BW (1993) Historical biogeography of Fungia (Pleuractis) spp. (Scleractinia: Fungiidae), including a new species from the Seychelles. Zool Meded Leiden 67:639–654
34. Hoeksema BW (2012) Evolutionary trends in onshore-offshore distribution patterns of mushroom coral species (Scleractinia: Fungiidae). Contrib Zool 81:199–221
35. Hoeksema BW (2015) Latitudinal species diversity gradient of mushroom corals off eastern Australia: a baseline from the 1970s. Estuar Coast Shelf Sci 165:190–198. doi:10.1016/j.ecss.2015.05.015
36. Hoeksema BW, van der Meij SET, Fransen CHJM (2012) The mushroom coral as a habitat. J Mar Biol Assoc UK 92:647–663. doi:10.1017/S0025315411001445
37. Hooper DU, Chapin FS III, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. doi:10.1890/04-0922
38. Hooper DU, Adair EC, Cardinale BJ et al (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108. doi:10.1038/nature11118
39. Huang D (2012) Threatened reef corals of the world. PLoS One 7:e34459. doi:10.1371/journal.pone.0034459
40. Huang D, Roy K (2013) Anthropogenic extinction threats and future loss of evolutionary history in reef corals. Ecol Evol 3:1184–1193. doi:10.1002/ece3.527
41. Huang D, Licuanan WY, Hoeksema BW et al (2015) Extraordinary diversity of reef corals in the South China Sea. Mar Biodivers 45:157–168. doi:10.1007/s12526-014-0236-1
42. Idjadi JA, Edmunds PJ (2006) Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Mar Ecol Prog Ser 319:117–127. doi:10.3354/meps319117
43. Isaac NJB, Turvey ST, Collen B et al (2007) Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS One 2:e296. doi:10.1371/journal.pone.0000296
44. IUCN (2001) IUCN Red List Categories and Criteria: Version 3.1. IUCN, Gland, Switzerland and Cambridge
45. Jain M, Flynn DFB, Prager CM et al (2014) The importance of rare species: a trait-based assessment of rare species contributions to functional diversity and possible ecosystem function in tall-grass prairies. Ecol Evol 4:104–112. doi:10.1002/ece3.915
46. Jones AM, Berkelmans R, Houston W (2011) Species richness and community structure on a high latitude reef: implications for conservation and management. Diversity 3:329–355. doi:10.3390/d3030329
47. Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. doi:10.1093/bioinformatics/btq166
48. Kimura T, Dai C-F, Park H-S et al (2008) Status of coral reefs in East and North Asia (China, Hong Kong, Taiwan, South Korea and Japan). In: Wilkinson C (ed) Status of Coral Reefs of the World: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, pp 145–158
49. Klein CJ, Ban NC, Halpern BS et al (2010) Prioritizing land and sea conservation investments to protect coral reefs. PLoS One 5:e12431. doi:10.1371/journal.pone.0012431
50. Lennon JJ, Koleff P, Greenwood JJD, Gaston KJ (2004) Contribution of rarity and commonness to patterns of species richness. Ecol Lett 7:81–87. doi:10.1046/j.1461-0248.2004.00548.x
51. Leroy B, Petillon J, Gallon R et al (2012) Improving occurrence-based rarity metrics in conservation studies by including multiple rarity cut-off points. Insect Conserv Divers 5:159–168. doi:10.1111/j.1752-4598.2011.00148.x
52. Leroy B, Canard A, Ysnel F (2013) Integrating multiple scales in rarity assessments of invertebrate taxa. Divers Distrib 19:794–803. doi:10.1111/ddi.12040
53. Lyons KG, Brigham CA, Traut BH, Schwartz MW (2005) Rare species and ecosystem functioning. Conserv Biol 19:1019–1024. doi:10.1111/j.1523-1739.2005.00106.x
54. Mace GM, Gittleman JL, Purvis A (2003) Preserving the tree of life. Science 300:1707–1709. doi:10.1126/science.1085510
55. Madin EMP (2015) Halt reef destruction in South China Sea. Nature 524:291. doi:10.1038/524291a
56. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748. doi:10.1126/science.1143082
57. May RM (1990) Taxonomy as destiny. Nature 347:129–130. doi:10.1038/347129a0
58. McCann KS (2000) The diversity–stability debate. Nature 405:228–233. doi:10.1038/35012234
59. McManus JW (1994) The Spratly Islands: a marine park? Ambio 23:181–186
60. 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
61. McManus JW, Meñez LAB (1997) The proposed international Spratly Island marine park: ecological considerations. In: Proceedings of the 8th international coral reef symposium, vol 2, pp 1943–1948
62. 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
63. MOE Japan (2010) ICRI East Asia regional strategy on MPA Networks 2010. Ministry of the Environment, Tokyo
64. Morton B, Blackmore G (2001) South China Sea. Mar Pollut Bull 42:1236–1263
65. Mouillot D, Bellwood DR, Baraloto C et al (2013) Rare species support vulnerable functions in high-diversity ecosystems. PLoS Biol 11:e1001569. doi:10.1371/journal.pbio.1001569
66. Mouillot D, Villéger S, Parravicini V et al (2014) Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs. Proc Natl Acad Sci USA 111:13757–13762. doi:10.1073/pnas.1317625111
67. Murdoch W, Polasky S, Wilson KA et al (2007) Maximizing return on investment in conservation. Biol Conserv 139:375–388. doi:10.1016/j.biocon.2007.07.011
68. Nee S, May RM (1997) Extinction and the loss of evolutionary history. Science 278:692–694. doi:10.1126/science.278.5338.692
69. Nyström M (2006) Redundancy and response diversity of functional groups: implications for the resilience of coral reefs. Ambio 35:30–35. doi:10.1579/0044-7447-35.1.30
70. Orme CDL, Davies RG, Burgess M et al (2005) Global hotspots of species richness are not congruent with endemism or threat. Nature 436:1016–1019. doi:10.1038/nature03850
71. Orme CDL, Freckleton RP, Thomas GH, et al. (2013) caper: Comparative Analyses of Phylogenetics and Evolution in R. R Package Version 0.5.2. http://caper.r-forge.r-project.org. Accessed 19 Feb 2014
72. Parhar RK, Mooers AØ (2011) Phylogenetically clustered extinction risks do not substantially prune the Tree of Life. PLoS One 6:e23528. doi:10.1371/journal.pone.0023528
73. Posadas P, Esquivel DRM, Crisci JV (2001) Using phylogenetic diversity measures to set priorities in conservation: an example from southern South America. Conserv Biol 15:1325–1334
74. Pratchett MS, Wilson SK, Graham NAJ, Munday PL (2009) Coral bleaching and consequences for motile reef organisms: past, present and uncertain future effects. In: van Oppen MJH, Lough JM (eds) Ecological studies: coral bleaching. Springer, Berlin, pp 139–158
75. Prendergast PR, Quinn RM, Lawton JH et al (2002) Rare species, the coincidence of diversity hotspots and conservation strategies. Nature 365:335–337. doi:10.1038/365335a0
76. Purvis A, Hector A (2000) Getting the measure of biodiversity. Nature 405:212–219. doi:10.1038/35012221
77. Purvis A, Agapow P-M, Gittleman JL, Mace GM (2000) Nonrandom extinction and the loss of evolutionary history. Science 288:328–330. doi:10.1126/science.288.5464.328
78. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 19 Feb 2014
79. Randall JE, Lim KKP (2000) A checklist of the fishes of the South China Sea. Raffles Bull Zool Suppl 8:569–667
80. Robbirt KM, Roberts DL, Hawkins JA (2006) Comparing IUCN and probabilistic assessments of threat: do IUCN red list criteria conflate rarity and threat? Biodivers Conserv 15:1903–1912. doi:10.1007/s10531-005-4307-2
81. Roberts CM, McClean CJ, Veron JEN et al (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284. doi:10.1126/science.1067728
82. Rodrigues ASL, Gaston KJ (2002) Maximising phylogenetic diversity in the selection of networks of conservation areas. Biol Conserv 105:103–111. doi:10.1016/S0006-3207(01)00208-7
83. Rosauer DF, Mooers AØ (2013) Nurturing the use of evolutionary diversity in nature conservation. Trends Ecol Evol 28:322–323. doi:10.1016/j.tree.2013.01.014
84. Sechrest W, Brooks TM, da Fonseca GAB et al (2002) Hotspots and the conservation of evolutionary history. Proc Natl Acad Sci USA 99:2067–2071. doi:10.1073/pnas.251680798
85. Tun K, Chou LM, Yeemin T et al (2008) Status of coral reefs in Southeast Asia. In: Wilkinson C (ed) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, pp 131–144
86. UNEP (2007) Reversing environmental degradation trends in the South China Sea and Gulf of Thailand. Report of the Eighth Meeting of the Regional Working Group on Coral Reefs. UNEP/GEF/SCS/RWG-CR.8/3, Bangkok
87. Vamosi JC, Wilson JRU (2008) Nonrandom extinction leads to elevated loss of angiosperm evolutionary history. Ecol Lett 11:1047–1053. doi:10.1111/j.1461-0248.2008.01215.x
88. Vane-Wright RI, Humphries CJ, Williams PH (1991) What to protect?—systematics and the agony of choice. Biol Conserv 55:235–254. doi:10.1016/0006-3207(91)90030-D
89. Veron JEN, DeVantier LM, Turak E et al (2009) Delineating the Coral Triangle. Galaxea 11:91–100. doi:10.3755/galaxea.11.91
90. Veron JEN, DeVantier LM, Turak E et al (2011) The Coral Triangle. In: Dubinsky Z, Stambler N (eds) Coral Reefs: an ecosystem in transition. Springer, Dordrecht, pp 47–55
91. Veron J, Stafford-Smith M, DeVantier L, Turak E (2015) Overview of distribution patterns of zooxanthellate Scleractinia. Front Mar Sci 1:81. doi:10.3389/fmars.2014.00081
92. 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
93. Vo ST, DeVantier LM, Tuyen HT, Hoàng PK (2014) Ninh Hai waters (south Vietnam): a hotspot of reef corals in the western South China Sea. Raffles Bull Zool 62:513–520
94. 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
95. Walton A, White AT, Tighe S et al (2014) Establishing a functional region-wide Coral Triangle Marine Protected Area System. Coast Manag 42:107–127. doi:10.1080/08920753.2014.877765
96. White AT, Aliño PM, Cros A et al (2014) Marine protected areas in the Coral Triangle: progress, issues, and options. Coast Manag 42:87–106. doi:10.1080/08920753.2014.878177
97. Wilson SK, Graham NAJ, Pratchett MS et al (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob Chang Biol 12:2220–2234. doi:10.1111/j.1365-2486.2006.01252.x
98. Witting L, Loeschcke V (1995) The optimization of biodiversity conservation. Biol Conserv 71:205–207. doi:10.1016/0006-3207(94)00041-N
99. Zhang SY, Speare KE, Long ZT et al (2014) Is coral richness related to community resistance to and recovery from disturbance? PeerJ 2:e308. doi:10.7717/peerj.308