Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas

Molecular Ecology

Volumn 21, Issue 17, 2012, Pages 4393-4407

  Keshavmurthy, Shashank ^a   Hsu, Chia Min ^a,b   Kuo, Chao Yang ^a   Meng, Pei Jie ^c,d   Wang, Jih Terng ^e   Chen, Chaolun A ^a,b,f  

^a BIODIVERSITY RESEARCH CENTER   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c NATIONAL MUSEUM OF MARINE BIOLOGY AND AQUARIUM   (Taiwan)

^d NATIONAL DONG HWA UNIVERSITY   (Taiwan)

^e TAJEN UNIVERSITY   (Taiwan)

^f ACADEMIA SINICA   (Taiwan)

Author keywords

acclimatization; heat tolerance; Platygyra verweyi; Symbiodinium D1a; thermal water discharge

Indexed keywords

PROTOZOAL DNA; RIBOSOMAL SPACER DNA;

ACCLIMATIZATION; ANIMAL; ANTHOZOA; ARTICLE; DINOFLAGELLATE; GENETICS; MICROBIOLOGY; NUCLEAR POWER PLANT; PHYSIOLOGY; POPULATION GENETICS; SYMBIOSIS; TAIWAN; TEMPERATURE;

ACCLIMATIZATION; ANIMALS; ANTHOZOA; DINOFLAGELLIDA; DNA, PROTOZOAN; DNA, RIBOSOMAL SPACER; GENETICS, POPULATION; NUCLEAR POWER PLANTS; SYMBIOSIS; TAIWAN; TEMPERATURE;

ANTHOZOA; PLATYGYRA; PLATYGYRA VERWEYI; SYMBIODINIUM;

EID: 84865487914     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05704.x     Document Type: Article

References (95)

1. Abrego D, Ulstrup KE, Willis BL, van Oppen MJH, (2008) Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proceeding of Royal Society London B, 275, 2273-2282.
2. Baird AH, Maynard JA, (2008) Coral adaptation in the face of climate change. Science, 320, 315-316.
3. Baird AH, Bhagooli R, Ralph PJ, Takahashi S, (2009) Coral bleaching. The role of the host. Trends in Ecology and Evolution, 24, 16-20.
4. Baker AC, (2001) Reef corals bleach to survive change. Nature, 411, 765-766. (Pubitemid 32588090)
5. Baker AC, (2003a) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology and Systematics, 34, 661-689. (Pubitemid 38171434)
6. Baker AC, (2003b) Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience. In: Coral Health and Disease (eds, Rosenberg E, and, Loya Y,), pp. 177-191. Springer, Berlin.
7. Baker AC, Romanski AM, (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: comment on Goulet. Marine Ecology Progress Series, 335, 237-242. (Pubitemid 46797410)
8. Baker AC, Starger CJ, McClanahan TR, Glynn PW, (2004) Corals' adaptive response to climate change. Nature, 403, 741.
9. Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Brikeland C, (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Molecular Ecolology, 19, 1705-1720.
10. Baums IB, Hughes CR, Hellberg ME, (2005) Mendelian micro- satellite loci for the Caribbean coral Acropora palmata. Marine Ecology Progress in Series, 288, 115-127. (Pubitemid 40554677)
11. Baums IB, Johnson ME, Devlin-Durante MK, Miller MW, (2010) Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean. Coral Reefs, 29, 835-842.
12. Bellantuono AJ, Hoegh-Guldberg O, Rodriguez-Lanetty M, (2012) Resistance to thermal stress in corals without changes in symbiont composition. Proceedings of Royal Society B, 279, 1100-1107.
13. Berkelmans R, (2002) Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Marine Ecology Progress Series, 229, 73-82. (Pubitemid 34305641)
14. Berkelmans R, van Oppen MJH, (2006) The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proceedings of Royal Society of London B, 273, 2305-2312. (Pubitemid 44387337)
15. Berkelmans R, De'ath G, Kininmonth S, Skirving WJ, (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns and predictions. Coral Reefs, 23, 74-83. (Pubitemid 38658985)
16. Brown BE, (1997) Adaptations of reef corals to physical environmental stress. Advances in Marine Biology, 31, 221-299. (Pubitemid 127820405)
17. Brown BE, Dunne RP, Scoffin TP, Le Tissier MDA, (1994) Solar damage in intertidal corals. Marine Ecology Progress Series, 105, 219-230. (Pubitemid 2080714)
18. Buddemeier RW, Fautin DG, (1993) Coral bleaching as an adaptive mechanism: a testable hypothesis. BioSciene, 43, 320-326.
19. Burt J, Al-Harthi S, Al-Cibahy A, (2011) Long-term impacts of coral bleaching events on the world's warmest reefs. Marine Environmental Research, 72, 225-229.
20. Chen CA, Wang JT, Fang LS, Yang YW, (2005) Fluctuating algal symbiont communities in Acropora palifera (Cnidaria; Scleractinia) from Taiwan. Marine Ecology Progress Series, 295, 113-121. (Pubitemid 41026816)
21. Chiou WD, Cheng LZ, Ou HC, (1993) Relationship between the dispersion of thermal effluent and the tidal current in the waters near the outlet of the third nuclear power plant in southern Taiwan. Journal of Fisheries Society of Taiwan, 20, 207-220.
22. Clement M, Posada D, Crandall KA, (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
23. Cockerham CC, Weir BS, (1993) Estimation of gene flow from F-statistics. Evolution, 47, 855-863.
24. Csaszar NBM, Ralph P, Frankham R, Berkelmans R, van Oppen MJH, (2010) Estimating the potential for adaptation of corals to climate warming. PLoS One 5, e9751. doi:10.1371/journal.pone.0009751.
25. Dunn SR, Thomason JC, Le Tissier MDA, Bythell JC, (2004) Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death and Differentiation, 11, 1213-1222. (Pubitemid 39529964)
26. Edmunds PJ, (2005) The effect of sub-lethal increases in temperature on the growth and population trajectories of three scleractinian corals on the southern Great Barrier Reef. Oecologia, 146, 350-364. (Pubitemid 41547117)
27. Edmunds PJ, Gates RD, (2008) Acclimatization in tropical reef corals. Marine Ecology Progress Series, 361, 307-310. (Pubitemid 351975521)
28. Excoffier L, Smouse PE, Quattro JM, (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479-491.
29. Excoffier L, Laval G, Schneider S, (2005) An integrated software package for population genetics data analysis. Evolutionary Bioinformatics, 1, 47-50.
30. Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH, (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Molecular Ecology, 13, 2445-2458. (Pubitemid 38946432)
31. Fan KL, (1991) The thermal effluent problems of three nuclear power plants in Taiwan. In: Oceanography of Asian Marginal Seas, (ed, Takano K,), Elsevier Oceanography Series, Amsterdam, The Netherlands 54, 393-403.
32. Fang LS, Liao CW, Liu MC, (1995) Pigment composition in different colored scleractinian corals before and during bleaching process. Zoological Studies, 34, 10-17.
33. Ferrara GB, Murgia B, Parodi AM, et al. (2006) The assessment of DNA from marine organisms via a modified salting-out protocol. Cellular and Molecular Biology Letters, 11, 155-160. (Pubitemid 44492474)
34. Fitt WK, Warner ME, (1995) Bleaching patterns of four species of Caribbean reef corals. Biological Bulletin, 189, 298-307. (Pubitemid 3024672)
35. Fitt WK, Gates RD, Hoegh-Guldberg O, et al. (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. Journal of Experimental Marine Biology and Ecology, 373, 102-110.
36. Fukami H, Budd AF, Paulay G, et al. (2004) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature, 427, 832-835. (Pubitemid 38297743)
37. Gleason DF, Wellington GM, (1995) Variation in UVB sensitivity of planula larvae of the coral Agaricia agaricites along a depth gradient. Marine Biology, 123, 693-703.
38. Haslun JA, Strychat KB, Buck G, Sammarco PW, (2011) Coral bleaching susceptibility is decreased following short-term (1-3 year) prior temperature exposure and evolutionary history. Journal of Marine Biology, 2011, 1-13.
39. Hoegh-Guldberg O, (1999) Climate change, coral bleaching and the future of the worlds coral reefs. Marine and Freshwater Research, 50, 839-866. (Pubitemid 30018479)
40. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737-1742.
41. Huang DW, Meier R, Todd PA, Chou LM, (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. Journal of Molecular Evolution, 66, 167-174.
42. Huang DW, Meier R, Todd PA, Chou LM, (2009) More evidence for pervasive paraphyly in scleractinian corals: systematic study of Southeast Asian Faviidae (Cnidaria; Scleractinia) based on molecular and morphological data. Molecular Phylogenetic Evolution, 50, 102-116.
43. Hughes TE, Baird AH, Bellwood DR, et al. (2003) Climate change, human impacts, and the resilience of coral reefs. Science, 301, 929-933. (Pubitemid 36994796)
44. Hung T-C, Huang C-C, Shao K-T, (1998) Ecological survey of coastal water adjacent to nuclear power plants in Taiwan. Chemical Ecology, 15, 129-142.
45. Hwang R-L, Tsai C-C, Lee T-M, (2004) Assessment of temperature and nutrient limitation on seasonal dynamics among species of Sargassum from a coral reef in southern Taiwan. Journal of Phycology, 40, 463-473. (Pubitemid 38740375)
46. Intergovernmental Panel on Climate Change (2007) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel of Climate Change, Cambridge University Press, Cambridge, UK.
47. Jan R-Q, Chen J-P, Lin C-Y, Shao K-T, (2001) Long-term monitoring of the coral reef fish communities around a nuclear power plant. Aquatic Ecology, 35, 233-243. (Pubitemid 32792745)
48. Jones AM, Berkelmans RWC, (2010) Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS One, 5, e10437.
49. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W, (2008) A community shift in the symbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of Royal Society B, 275, 1359-1365. (Pubitemid 351653015)
50. Keshavmurthy S, Hsu C, Kuo C, Meng P, Wang J, Chen CA, (2012) Data from: Symbiont community and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas. Dryad Digital Repository. doi:10.5061/dryad.v3144.
51. Knowlton N, Jackson JBC, (2008) Shifting baselines, local impacts, and global change on coral reefs. PLOS Biology, 6, 215-220.
52. LaJeunesse TC, (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology, 141, 387-400.
53. LaJeunesse TC, Trench RK, (2000) The biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal anemone, Anthopleura elegantissima (Brandt). Biological Bulletin, 199, 126-134.
54. Lam K, Morton B, (2003) Morphological and ITS1, 5.8S, and partial ITS2 ribosomal DNA sequence distinctions between two species Playtygyra (Cnidaria: Scleractinia) from Hong Kong. Marine Biotechnology, 5, 555-567. (Pubitemid 38106640)
55. Lee H-J, Chao S-Y, Fan K-L, Wang Y-H, Liang N-K, (1997) Tidally induced upwelling in a semi-enclosed basin: Nan Wan Bay. Journal of Oceanography, 53, 467-480. (Pubitemid 127660667)
56. Librado P, Rozas J, (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
57. Lien YT, Nakano Y, Plathong S, Fukami H, Wang JT, Chen CA, (2007) Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs, 26, 35-44. (Pubitemid 46491145)
58. Little AF, van Oppen MJH, Willis BL, (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science, 304, 1492-1494. (Pubitemid 38720927)
59. Long JC, (1986) The allelic correlation structure of gainj- andkalam-speaking people. I. The estimation and interpretation of Wright's F-statistics. Genetics, 112, 629-647.
60. Loya Y, Sakai K, Yamazato Y, Nakano H, Sambali R, van Woesik R, (2001) Coral bleaching: the winners and losers. Ecological Letters, 4, 122-131.
61. Mackenzie JB, Munday PL, Willis BL, Miller DJ, van Oppen MJH, (2004) Unexpected patterns of genetic structuring among locations but not colour morphs in Acropora nasuta (Cnidaria; Scleractinia). Molecular Ecology, 13, 9-20. (Pubitemid 38106469)
62. Magalon H, Adjeroud M, Veuille M, (2005) Patterns of genetic variation do not correlate with geographical distance in the reef- building coral Pocillopora meandrina in the South Pacific. Molecular Ecology, 14, 1861-1868. (Pubitemid 40772408)
63. Marshall PA, Baird A, (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs, 19, 155-163. (Pubitemid 30610813)
64. McClanahan TR, Muthiga NA, Mangi S, (2001) Coral and algal changes after the 1998 coral bleaching: interaction with reef management and herbivores on Kenyan reefs. Coral Reefs, 19, 380-391. (Pubitemid 32455829)
65. Mieog JC, Van Oppen MJH, Cantin N, Stam DWT, Olsen JL, (2007) Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs, 26, 449-457. (Pubitemid 350104765)
66. Mostafavi PG, Reza Fatemi SM, Shahhosseiny MH, Guldberg OH, (2007) Predominance of clade D Symbiodinium in shallow-water reef-building corals off Kish and Larak Islands (Persian Gulf, Iran). Marine Biology, 153, 25-34. (Pubitemid 47583386)
67. Muscatine L, Grossman D, Doino J, (1991) Release of symbiotic algae by tropical sea anemones and corals after cold shock. Marine Ecology Progress Series, 77, 233-243.
68. Nunes F, Fukami H, Vollmer SV, Norris RD, Knowlton N, (2008) Re-evaluation of the systematics of the endemic corals of Brazil by molecular data. Coral Reefs, 27, 423-432.
69. Obura DO, (2005) Resilience and climate change: lessons from coral reefs and bleaching in the Western Indian Ocean. Continental Shelf Research, 63, 353-372. (Pubitemid 40588979)
70. Oliver TA, Palumbi SR, (2009) Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Marine Ecology Progress Series, 379, 93-103.
71. Oliver TA, Palumbi SR, (2011a) Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs, 30, 241-250.
72. Oliver TA, Palumbi SR, (2011b) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs, 30, 429-440.
73. van Oppen MJH, Gates RD, (2006) Conservation genetics and resilience of reef-building corals. Molecular Ecology, 15, 3863-3883. (Pubitemid 44607139)
74. van Oppen MJH, Palstra F, Piquet A, Miller D, (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proceedings of Royal Society of London B, 268, 1759-1767. (Pubitemid 32844022)
75. Pandolfi JM, Bradbury RH, Sala E, et al. (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science, 301, 955-958. (Pubitemid 36994805)
76. Pier J-J, (2011) Power uprate effect on thermal effluent of nuclear power plants in Taiwan. In: Nuclear Power-Operation, Safety and Environment (ed, Tsvetkov P,), pp. 287-302. InTech publication, Rijeka, Croatia.
77. Pochon X, Gates RD, (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'I. Molecular Phylogenetics and Evolution, 56, 492-497.
78. Pochon X, Pawlowski J, Zaninetti L, Rowan R, (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Marine Biology, 139, 1069-1078. (Pubitemid 34049858)
79. Pochon X, Montoya-Burgos JI, Stadeklmann B, Pawlowski J, (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Molecular Phylogenetics and Evolution, 38, 20-30. (Pubitemid 41773271)
80. Putnam HA, Edmunds PJ, (2011) The physiologica response of reef corals to diel fluctuations in seawater temperature. Journal of Experimental Marine Biology and Ecology, 396, 216-223.
81. Roberts HH, Rouse Jr LJ, Walker ND, Hudson JH, (1982) Cold-water stress in Florida Bay and Northern Bahamas: a product of winter cold-air outbreaks. Journal of Sedimentary Research, 52, 145-155.
82. Rowan R, (2004) Thermal adaptation in reef coral symbionts. Nature, 430, 742. (Pubitemid 39071338)
83. Sammarco PW, Strychar KB, (2009) Effects of climate change/global warming on coral reefs: adaptation/exaptaion in corals, evolution in zooxanthellae, and biogeographic shifts. Environmental Bioindicators, 4, 9-45.
84. Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O, (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proceedings of National Academy of Sciences, 105, 10444-10449.
85. Saxby TA, Dennison WC, Hoegh-Guldberg O, (2003) Photosynthetic responses of the coral Montipora digitata to cold temperature stress. Marine Ecology Progress Series, 248, 85-97. (Pubitemid 36339330)
86. Strychar KB, Sammarco PW, (2008) Exaptation in corals to high seawater temperatures: low concentrations of apoptotic and necrotic cells in host coral tissue under bleaching conditions. Journal of Experimental Marine Biology and Ecology, 369, 31-42.
87. Suwa R, Hirose M, Hidaka M, (2008) Seasonal fluctuation in zooxanthellar genotype composition and photophysiology in the corals Pavona divaricata and P. decussata. Marine Ecology Progress Series, 361, 129-137. (Pubitemid 351975505)
88. Takabayashi M, Carter DA, Loh WKW, Hoegh-Guldberg O, (1998) A coral-specific primer for PCR amplification of the internal transcribed spacer region in ribosomal DNA. Molecular Ecology, 7, 25-931.
89. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739.
90. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680. (Pubitemid 24354800)
91. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW, (2006) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Marine Biology, 148, 711-722. (Pubitemid 43183831)
92. Ulstrup KE, van Oppen MJH, (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Molecular Ecology, 12, 3477-3484. (Pubitemid 37496707)
93. Venn AA, Loram JE, Trapido-Rosenthal HG, Joyce DA, Douglas AE, (2008) Importance of time and place: patterns in abundance of Symbiodinium clades A and B in the tropical sea anemone Condylactis gigantea. Biological Bulletin, 215, 243-252.
94. Warner ME, Fitt WK, Schmidt GW, (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell and Environment, 19, 291-299.
95. van Woesik R, Sakai K, Ganase A, Loya Y, (2011) Revisiting the winners and the losers a decade after coral bleaching. Marine Ecology Progress Series, 434, 67-76.