Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event

Limnology and Oceanography

Volumn 59, Issue 3, 2014, Pages 788-797

  Kemp, Dustin W ^a   Hernandez Pech, Xavier ^b   Iglesias Prieto, Roberto ^b   Fitt, William K ^a   Schmidt, Gregory W ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84898445604     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2014.59.3.0788     Document Type: Article

References (52)

1. Abrego, D., K. E. Ulstrup, B. L. Willis, and M. J. H. van Oppen. 2008. Species-specific interactions between algal endosymbionts and coral hosts define bleaching response to heat and light stress. Proc. R. Soc. B-Biol. Sci. 275: 2273-2282, doi: 10. 1098/rspb. 2008. 0180.
2. Baker, A. C., and A. M. Romanski. 2007. Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: Comment on Goulet (2006). Mar. Ecol. Prog. Ser. 335: 237-242, doi: 10. 3354/meps335237.
3. Baker, A. C., C. J. Starger, T. R. McClanahan, and P. W. Glynn. 2004. Corals' adaptive response to climate change. Nature 430: 741, doi: 10. 1038/430741a.
4. Baker, D. M., J. P. Andras, A. G. Jordá n-Garza, and M. L. Fogel. 2013. Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades. ISME J. 7: 1248-1251, doi: 10. 1038/ismej. 2013. 12.
5. Berkelmans, R., and M. J. H. van Oppen. 2006. The role of zooxanthellae in the thermal tolerance of corals: A 'nugget of hope' for coral reefs in an era of climate change. Proc. R. Soc. B-Biol. Sci. 273: 2305-2312, doi: 10. 1098/rspb. 2006. 3567.
6. Brandt, M. E., and J. W. McManus. 2009. Disease incidence is related to bleaching extent in reef-building corals. Ecology 90: 2859-2867, doi: 10. 1890/08-0445. 1.
7. Brown, B. E. 1997. Coral bleaching: Causes and consequences. Coral Reefs 16: S129-S138, doi: 10. 1007/s003380050249.
8. Budd, A. F., H. Fukami, N. D. Smith, and N. Knowlton. 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.
9. Cantin, N. E., A. L. Cohen, K. B. Karnauskas, A. M. Tarrant, and D. C. Mccorkle. 2010. Ocean warming slows coral growth in the central Red Sea. Science 329: 322-325, doi: 10. 1126/science. 1190182.
10. Cantin, N. E., M. J. H. van Oppen, B. L. Willis, J. C. Mieog, and A. P. Negri. 2009. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28: 405-414, doi: 10. 1007/s00338-009-0478-8.
11. Fabricius, K. E., J. C. Mieog, P. L. Colin, D. Idip, and M. J. H. van Oppen. 2004. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol. Ecol. 13: 2445-2458, doi: 10. 1111/j. 1365-294X. 2004. 02230. x.
12. Falkowski, P. G., Z. Dubinsky, L. Muscatine, and L. McCloskey. 1993. Population-control in symbiotic corals. Bioscience 43: 606-611, doi: 10. 2307/1312147.
13. Fitt, W. K., F. K. McFarland, M. E. Warner, and G. C. Chilcoat. 2000. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol. Oceanogr. 45: 677-685, doi: 10. 4319/lo. 2000. 45. 3. 0677.
14. Fitt, W. K., H. J. Spero, J. Halas, M. W. White, and J. W. Porter. 1993. Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean bleaching event. Coral Reefs 12: 57-64, doi: 10. 1007/BF00302102.
15. Grottoli, A. G., L. J. Rodrigues, and J. E. Palardy. 2006. Heterotrophic plasticity and resilience in bleached corals. Nature 440: 1186-1189, doi: 10. 1038/nature04565.
16. Hoegh-Guldberg, O., and others. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742, doi: 10. 1126/science. 1152509.
17. Houlbreque, F., and C Ferrier-Pagès. 2009. Heterotropy in tropical scleractinian corals. Biol. Rev. 84: 1-17, doi: 10. 1111/j. 1469-185X. 2008. 00058. x.
18. Howells, E., V. Beltran, N. Larsen, L. Bay, B. Willis, and M. van Oppen. 2011. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat. Clim. Chang. 2: 116-120, doi: 10. 1038/nclimate1330.
19. Hutchinson, G. E. 1961. The paradox of the plankton. Am. Nat. 95: 137-145, doi: 10. 1086/282171.
20. Iglesias-Prieto, R., J. L. Matta, W. A. Robins, and R. K. Trench. 1992. Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc. Natl. Acad. Sci. USA 89: 10302-10305, doi: 10. 1073/pnas. 89. 21. 10302.
21. IPCC. 2007. Climate change 2007: Synthesis report [Internet]. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva: IPCC, [accessed 20 February 2014]. Available from http://www. ipcc. ch/publications_and_data/publications_and_data_reports. shtml.
22. Jeffrey, S. W., and G. F. Humphrey. 1975. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher-plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167: 191-194.
23. Johannes, R. E., and W. J. Wiebe. 1970. Method for determination of coral tissue biomass and composition. Limnol. Oceanogr. 15: 822-824, doi: 10. 4319/lo. 1970. 15. 5. 0822.
24. Kemp, D. W., W. K. Fitt, and G. W. Schmidt. 2008. A microsampling method for genotyping coral symbionts. Coral Reefs 27: 289-293, doi: 10. 1007/s00338-007-0333-8.
25. LaJeunesse, T. C. 2001. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: In search of a "species" level marker. J. Phycol. 37: 866-880, doi: 10. 1046/j. 1529-8817. 2001. 01031. x.
26. LaJeunesse, T. C. 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar. Biol. 141: 387-400, doi: 10. 1007/s00227-002-0829-2.
27. LaJeunesse, T. C., W. K. W. Loh, R. Van Woesik, O. Hoegh-Guldberg, G. W. Schmidt, and W. K. Fitt. 2003. Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol. Oceanogr. 48: 2046-2054, doi: 10. 4319/lo. 2003. 48. 5. 2046.
28. LaJeunesse, T. C., D. T. Pettay, E. M. Sampayo, N. Phongsuwan, B. Brown, D. O. Obura, O. Hoegh-Guldberg, and W. K. Fitt. 2010. Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J. Biogeogr. 37: 785-800, doi: 10. 1111/j. 1365-2699. 2010. 02273. x.
29. LaJeunesse, T. C., R. T. Smith, J. Finney, and H. Oxenford. 2009. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proc. R. Soc. B-Biol. Sci. 276: 4139-4148, doi: 10. 1098/rspb. 2009. 1405.
30. LaJeunesse, T. C., and D. J. Thornhill. 2011. Improved resolution of reefcoral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS One 6: e29013, doi: 10. 1371/journal. pone. 0029013.
31. Little, A. F., M. J. H. van Oppen, and B. L. Willis. 2004. Flexibility in algal endosymbioses shape growth in reef corals. Science. 304: 1492-1494, doi: 10. 1126/science. 1095733.
32. Marsh, J. 1970. Primary productivity of reef-building calcareous red algae. Ecology 51: 255-263, doi: 10. 2307/1933661.
33. Mieog, J. C., M. J. H. van Oppen, N. E. Cantin, W. T. Stam, and J. L. Olsen. 2007. Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across theGreat Barrier Reef: Implications for symbiont shuffling. Coral Reefs 26: 449-457, doi: 10. 1007/s00338-007-0244-8.
34. Piniak, G. A., F. Lipschultz, and J. McClelland. 2003. Assimilation and partitioning of prey nitrogen within two anthozoans and their endosymbiotic zooxanthellae. Mar. Ecol. Prog. Ser. 262: 125-136, doi: 10. 3354/meps262125.
35. Pochon, X., and R. D. Gates. 2010. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol. Phylogen. Evol. 56: 492-497, doi: 10. 1016/j. ympev. 2010. 03. 040.
36. Reynolds, J. M., B. U. Bruns, W. K. Fitt, and G. W. Schmidt. 2008. Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc. Natl. Acad. Sci. USA105: 13674-13678, doi: 10. 1073/pnas. 0805187105.
37. Robison, J. D., and M. E. Warner. 2006. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J. Phycol. 42: 568-579, doi: 10. 1111/j. 1529-8817. 2006. 00232. x.
38. Rodriguez-Roman, A., X. Hernandez-Pech, P. E. Thome, S. Enriquez, and R. Iglesias-Prieto. 2006. Photosynthesis and light utilization in the Caribbean coral Montastraea faveolata recovering from a bleaching event. Limnol. Oceanogr. 51: 2702-2710, doi: 10. 4319/lo. 2006. 51. 6. 2702.
39. Rowan, R. 2004. Coral bleaching: Thermal adaptation in reef coral symbionts. Nature 430: 742, doi: 10. 1038/430742a.
40. Rowan, R., and N. Knowlton. 1995. Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc. Natl. Acad. Sci. USA 92: 2850-2853, doi: 10. 1073/pnas. 92. 7. 2850.
41. Rowan, R., A. Baker, and J. Jara. 1997. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388: 265-269, doi: 10. 1038/40843.
42. Sampayo, E. M., S. Dove, and T. C. LaJeunesse. 2009. Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol. Ecol. 18: 500-519, doi: 10. 1111/j. 1365-294X. 2008. 04037. x.
43. Silverstein, R. N., A. M. S. Correa, and A. C. Baker. 2012. Specificity is rarely absolute in coral-algal symbiosis: Implications for coral response to climate change. Proc. R. Soc. B-Biol. Sci. 279: 2609-2618, doi: 10. 1098/rspb. 2012. 0055.
44. Smith, D. J., D. J. Suggett, and N. R. Baker. 2005. Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Glob. Chang. Biol. 11: 1-11, doi: 10. 1111/j. 1529-8817. 2003. 00895. x.
45. Smith, G. J., and L. Muscatine. 1999. Cell cycle of symbiotic dinoflagellates: Variation in G1 phase-duration with anemone nutritional status and macronutrient supply in the Aiptasia pulchella-Symbiodinium pulchrorum symbiosis. Mar. Biol. 134: 405-418, doi: 10. 1007/s002270050557.
46. Szmant, A. M., and N. J. Gassman. 1990. The effects of prolonged bleaching on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8: 217-224, doi: 10. 1007/BF00265014.
47. Takahashi, S., S. M. Whitney, and M. R. Badger. 2009. Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc. Natl. Acad. Sci. USA 106: 3237-3242, doi: 10. 1073/pnas. 0808363106.
48. Thornhill, D. J., T. C. LaJeunesse, D. W. Kemp, W. K. Fitt, and G. W. Schmidt. 2006. Multi-year, seasonal genotypic surveys of coralalgal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148: 711-722, doi: 10. 1007/s00227-005-0114-2.
49. Thornhill, D. J., A. M. Lewis, D. C. Wham, and T. C. LaJeunesse. 2014. Hostspecialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68: 352-367, doi: 10. 1111/evo. 12270.
50. Toller, W. W., R. Rowan, and N. Knowlton. 2001a. Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol. Bull. 201: 360-373, doi: 10. 2307/1543614.
51. Toller, W. W., R. Rowan, and N. Knowlton. 2001b. Zooxanthellae of the Montastraea annularis species complex: Patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol. Bull. 201: 348-359, doi: 10. 2307/1543613.
52. Warner, M. E., W. K. Fitt, and G. W. Schmidt. 1999. Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc. Natl. Acad. Sci. USA 96: 8007-8012, doi: 10. 1073/pnas. 96. 14. 8007.