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Habitat correlation of Symbiodinium diversity in two reef-building coral species in an upwelling region, eastern Hainan Island, China

Published online by Cambridge University Press:  21 October 2011

G. Zhou ,
H. Huang ,
J. Lian ,
C. Zhang  and
X. Li
G. Zhou
Affiliation:
Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China National Experiment Station of Tropical Marine Biology, Sanya 572000, China
H. Huang*
Affiliation:
Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China National Experiment Station of Tropical Marine Biology, Sanya 572000, China
J. Lian
Affiliation:
Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
C. Zhang
Affiliation:
Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
X. Li
Affiliation:
Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
*
Correspondence should be addressed to: H. Huang, Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 West Xingang Road, Guangzhou, 510301, People's Republic of China email: huanghui@scsio.ac.cn
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Abstract

Reef-building corals are fundamental to the most diverse marine ecosystems, and the coral–dinoflagellate (zooxanthellae) associations on fine scale remains largely unknown. Spatial variation in the diversity of symbiotic dinoflagellates of two scleractinian coral species was studied in an upwelling region near Qinlan Harbor in eastern Hainan Island, China. Results showed that stress-tolerant Symbiodinium trenchi in individual colonies of Galaxea fascicularis occurred more frequently in shallow back-reef than in deep fore-reef. The higher symbiont diversity was found in colonies of G. fascicularis in shallow and close to the harbour mouth whereas the coral Pocillipora damicornis always harboured Symbiodinium internal transcribed spacer 2 (ITS2) types C1c or C42a. Furthermore, both corals were found to simultaneously contain Symbiodinium ITS2 types belonging to two distinct phylogenetic clades (C and D). This indicates that the distribution of genetically distinct Symbiodinium may correlate with light regime and possibly temperature in some (but not all) colonies at particular locations, which we interpret as holobiont acclimation to the local environmental conditions. Therefore, we conclude that reef-building corals can adapt to the local environment by harbouring genetically distinct symbionts but depend on their respective symbiont transmission modes.

Keywords

scleractinian coralSymbiodiniumsymbiosisSouth China Sea
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 92 , Issue 6 , September 2012 , pp. 1309 - 1316
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

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References

REFERENCES

Baker, A.C. (2003) Flexibility and specificity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematics 34, 661–689.CrossRefGoogle Scholar
Barneah, O., Weis, V.M., Perez, S. and Benayahu, Y. (2004) Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition matters. Marine Ecology Progress Series 275, 89–95.CrossRefGoogle Scholar
Berkelmans, R. and van Oppen, M.J.H. (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 the Royal Society of London, Series B—Biological Sciences 273, 2305–2312.Google Scholar
Clarke, K.R. and Warwick, R.M. (2001) Changes in marine communities: an approach to statistical analysis and interpretation. 2nd edition. Plymouth, UK: PRIMER-E Ltd.Google Scholar
Dong, Z., Huang, H., Huang, L. and Li, Y. (2009) Diversity of symbiotic algae of the genus Symbiodinium in scleractinian corals of the Xisha Islands in the South China Sea. Journal of Systematics and Evolution 47, 321–326.CrossRefGoogle Scholar
Fitt, W.K. and Cook, C.B. (2001) The effects of feeding or addition of dissolved inorganic nutrients in maintaining the symbiosis between dinoflagellates and a tropical marine cnidarian. Marine Biology 139, 507–517.Google Scholar
Frade, P.R., De Jongh, F., Vermeulen, F., Van Bleijswijk, J. and Bak, R.P.M. (2008) Variation in symbiont distribution between closely related coral species over large depth ranges. Molecular Ecology 17, 691–703.CrossRefGoogle ScholarPubMed
Garren, M., Walsh, S.M., Caccone, A. and Knowlton, N. (2006) Patterns of association between Symbiodinium and members of the Montastraea annularis species complex on spatial scales ranging from within colonies to between geographic regions. Coral Reefs 25, 503–512.CrossRefGoogle Scholar
Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P., Gomez, E., Harvell, C.D., Sale, P.F., Edwards, A.J., Caldeira, K., Knowlton, N., Eakin, C.M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A. and Hatziolos, M.E. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742.CrossRefGoogle ScholarPubMed
Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P., Gomez, E., Harvell, C.D., Sale, P.F., Edwards, A.J., Caldeira, K., Knowlton, N., Eakin, C.M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A. and Hatziolos, M.E. (2008) Coral adaptation in the face of climate change—response. Science 320, 315–316.Google Scholar
Huang, H., Dong, Z., Huang, L. and Zhang, J. (2006) Restriction fragment length polymorphism analysis of large subunit rDNA of symbiotic dinoflagellates from scleractinian corals in the Zhubi Coral Reef of the Nansha Islands. Journal of Integrative Plant Biology 48, 148–152.CrossRefGoogle Scholar
Iglesias-Prieto, R., Beltran, V.H., LaJeunesse, T.C., Reyes-Bonilla, H. and Thome, P.E. (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proceedings of the Royal Society of London, Series B—Biological Sciences 271, 1757–1763.CrossRefGoogle ScholarPubMed
Jing, Z., Qi, Y., Hua, Z. and Zhang, H. (2009) Numerical study on the summer upwelling system in the northern continental shelf of the South China Sea. Continental Shelf Research 29, 467–478.CrossRefGoogle Scholar
Jones, A.M., Berkelmans, R., van Oppen, M.J.H., Mieog, J.C. and Sinclair, W. (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society of London, Series B—Biological Sciences 275, 1359–1365.Google ScholarPubMed
LaJeunesse, T.C. (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141, 387–400.Google Scholar
LaJeunesse, T.C., Loh, W.K.W., van Woesik, R., Hoegh-Guldberg, O., Schmidt, G.W. and Fitt, W.K. (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnology and Oceanography 48, 2046–2054.CrossRefGoogle Scholar
LaJeunesse, T.C., Bhagooli, R., Hidaka, M., DeVantier, L., Done, T., Schmidt, G.W., Fitt, W.K. and Hoegh-Guldberg, O. (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Marine Ecology Progress Series 284, 147–161.CrossRefGoogle Scholar
LaJeunesse, T.C., Bonilla, H.R., Warner, M.E., Wills, M., Schmidt, G.W. and Fitt, W.K. (2008) Specificity and stability in high latitude eastern Pacific coral–algal symbioses. Limnology and Oceanography 53, 719–727.CrossRefGoogle Scholar
LaJeunesse, T.C., Smith, R., Walther, M., Pinzon, J., Pettay, D.T., McGinley, M., Aschaffenburg, M., Medina-Rosas, P., Cupul-Magana, A.L., Perez, A.L., Reyes-Bonilla, H. and Warner, M.E. (2010) Host–symbiont recombination versus natural selection in the response of coral–dinoflagellate symbioses to environmental disturbance. Proceedings of the Royal Society of London, Series B—Biological Sciences 277, 2925–2934.Google ScholarPubMed
Lin, S.J., Zhang, H., Hou, Y., Miranda, L. and Bhattacharya, D. (2006) Development of a dinoflagellate-oriented PCR primer set leads to detection of picoplanktonic dinoflagellates from Long Island Sound. Applied and Environmental Microbiology 72, 5626–5630.CrossRefGoogle ScholarPubMed
Loh, W.K.W., Loi, T., Carter, D. and Hoegh-Guldberg, O. (2001) Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Marine Ecology Progress Series 222, 97–107.CrossRefGoogle Scholar
Mostafavi, P.G., Fatemi, S.M.R., Shahhosseiny, M.H., Hoegh-Guldberg, O. and Loh, W.K.W. (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.CrossRefGoogle Scholar
Oliver, T.A. and Palumbi, S.R. (2009) Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Marine Ecology Progress Series 378, 93–103.CrossRefGoogle Scholar
Pochon, X. and Gates, R.D. (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Molecular Phylogenetics and Evolution 56, 492–497.CrossRefGoogle ScholarPubMed
Richmond, R.H. and Hunter, C.L. (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the tropical Pacific and the Red Sea. Marine Ecology Progress Series 60, 185–203.CrossRefGoogle Scholar
Rodriguez-Lanetty, M., Loh, W., Carter, D. and Hoegh-Guldberg, O. (2001) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Marine Biology 138, 1175–1181.Google Scholar
Rowan, R., Knowlton, N., Baker, A. and Jara, J. (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388, 265–269.CrossRefGoogle ScholarPubMed
Sampayo, E.M., Franceschinis, L., Hoegh-Guldberg, O. and Dove, S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Molecular Ecology 16, 3721–3733.CrossRefGoogle ScholarPubMed
Sampayo, E.M., Ridgway, T., Bongaerts, P. and Hoegh-Guldberg, O. (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proceedings of the National Academy of Sciences of the United States of America 105, 10444–10449.CrossRefGoogle ScholarPubMed
Santos, S.R., Taylor, D.J., Kinzie, R.A. III, Hidaka, M., Sakai, K. and Coffroth, M.A. (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Molecular Phylogenetics and Evolution 23, 97–111.CrossRefGoogle ScholarPubMed
Stat, M., Loh, W.K.W., Hoegh-Guldberg, O. and Carter, D.A. (2008) Symbiont acquisition strategy drives host–symbiont associations in the southern Great Barrier Reef. Coral Reefs 27, 763–772.CrossRefGoogle Scholar
Tchernov, D., Gorbunov, M.Y., Devargas, C., Yadav, S.N., Milligan, A.J., Haggblom, M. and Falkowski, P.G. (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proceedings of the National Academy of Sciences of the United States of America 101, 13531–13535.CrossRefGoogle ScholarPubMed
ter Braak, C.J. (1995) Ordination. In Jongman, R.H., ter Braak, C.J. and Van Tongeren, O.F. (eds) Data analysis in community and landscape ecology. Cambridge: Cambridge University Press, pp. 91–173.CrossRefGoogle Scholar
Thornhill, D.J., LaJeunesse, T.C., Kemp, D.W., Fitt, W.K. and Schmidt, G.W. (2006a) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Marine Biology 148, 711–722.CrossRefGoogle Scholar
Thornhill, D.J., Fitt, W.K. and Schmidt, G.W. (2006b) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25, 515–519.CrossRefGoogle Scholar
Thornhill, D.J., Lajeunesse, T.C. and Santos, S.R. (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Molecular Ecology 16, 5326–5340.CrossRefGoogle ScholarPubMed
Thornhill, D.J., Xiang, Y., Fitt, W.K. and Santos, S.R. (2009) Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS ONE 4, e6262.CrossRefGoogle ScholarPubMed
Thornhill, D.J., Kemp, D.W., Sampayo, E.M. and Schmidt, G.W. (2010) Comparative analyses of amplicon migration behavior in differing denaturing gradient gel electrophoresis (DGGE) systems. Coral Reefs 29, 83–91.CrossRefGoogle Scholar
Toller, W.W., Rowan, R. and Knowlton, N. (2001) Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biological Bulletin. Marine Biological Laboratory, Woods Hole 201, 348–359.CrossRefGoogle ScholarPubMed
van Oppen, M.J.H. (2004) Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Marine Biology 144, 1–7.CrossRefGoogle Scholar