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Landscape ecology of algal symbionts creates variation in episodes of coral bleaching

Abstract

Reef-building corals are obligate, mutualistic symbioses of heterotrophic animals and phototrophic dinoflagellates (Symbiodinium spp.)1. Contrary to the earlier, widely accepted belief that corals harbour only one symbiont, we found that the ecologically dominant Caribbean corals Montastraea annularis and M. faveolata can act as hosts to dynamic, multi-species communities of Symbiodinium. Composition of these communities follows gradients of environmental irradiance, implying that physiological acclimatization2,3,4 is not the only mechanism by which corals cope with environmental heterogeneity. The importance of this diversity was underlined by analysis of a natural episode of coral bleaching. Patterns of bleaching could be explained by the preferential elimination of a symbiont associated with low irradiance from the brightest parts of its distribution. Comparative analyses of symbionts before and after bleaching from the same corals supported this interpretation, and suggested that some corals were protected from bleaching by hosting an additional symbiont that is more tolerant of high irradiance and temperature. This ‘natural experiment’ suggests that temporal and spatial variability can favour the coexistence of diverse symbionts within a host, despite the potential for destabilizing competition among them5,6.

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Figure 1: Symbiont communities in M. annularis
Figure 2: Symbiont zonation in columns of M. annularis.
Figure 3: Bleaching in M. annularis (a, c) and M. faveolata (b, d) at the study site on 28 October 1995 showing ‘shallow’ (a, b) and ‘deep’ (c, d) patterns. e, Sea surface temperatures (three-week running means, from satellite data30) at the San Blas Islands, Panama.
Figure 4: Symbiont communities before (January 1995) and during (October 1995) an episode of coral bleaching.

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References

  1. Trench, R. K. Microalgal-invertebrate symbioses: a review. Endocytobiosis Cell Res. 9, 135–175 (1993).

    Google Scholar 

  2. Falkowski, P. G., Jokiel, P. L. & Kinzie, R. A. II in Ecosystems of the World Vol. 25, Coral Reefs (ed. Dubinsky, Z.) 89–107 (Elsevier, Amsterdam, (1990)).

    Google Scholar 

  3. Brown, B. E. Coral bleaching: Causes and consequences. Coral Reefs (in the press).

  4. Iglesias-Prieto, R. & Trench, R. K. Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar. Ecol. Prog. Ser. 113, 163–175 (1994).

    Google Scholar 

  5. Maynard Smith, J. & Szathmáry, E. The Major Transitions in Evolution(Oxford, Univ. Press, New York, (1995)).

  6. Leigh, E. G. J & Rowell, T. E. The evolution of mutalism and other forms of harmony at various levels of biological organization. Ecologie 26, 131–158 (1995).

    Google Scholar 

  7. Rowan, R. & Knowlton, N. Intraspecific diversity and ecological zonation in coral–algal symbioses. Proc. Natl Acad. Sci. USA 92, 2850–2853 (1995).

    Google Scholar 

  8. Glynn, P. W. Coral reef bleaching: ecological perspectives. Coral Reefs 12, 1–17 (1993).

    Google Scholar 

  9. Williams, E. H. J & Bunkley-Williams, L. The world-wide coral reef bleaching cycle and related sources of coral mortality. Atoll Res. Bull. 335, 1–71 (1990).

    Google Scholar 

  10. Sandeman, I. M. in Mass Bleaching of Coral Reefs in the Caribbean: A Research Strategy (eds Ogden, J. & Wicklund, R.) (Natl. Undersea Res. Prog. Res. Rep. 88-2) 46–48 (NOAA, Washington DC, (1988)).

    Google Scholar 

  11. Edmunds, P. J. Evidence that reef-wide patterns of coral bleaching may be the result of the distribution of bleaching-susceptible clones. Mar. Biol. 121, 127–142 (1994).

    Google Scholar 

  12. Lesser, M. P., Stochaj, W. R., Tapley, D. W. & Shick, J. M. Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8, 225–232 (1990).

    Google Scholar 

  13. Fitt, W. K. & Warner, M. E. Bleaching patterns of four species of Caribbean reef corals. Biol. Bull. 189, 298–307 (1995).

    Google Scholar 

  14. Jokiel, P. L. & Coles, S. L. Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8, 155–162 (1990).

    Google Scholar 

  15. CARICOMP. Studies on Caribbean coral bleaching, 1995.In Proc. 8th Int. Coral Reef Symp., Vol. 1(eds Lessios, H. A. & Macintyre, I. G.) 673–678 (Smithsonian Tropical Research Institute, Balboa, Panama, (1997)).

  16. Lasker, H. R., Peters, E. C. & Coffroth, M. A. Bleaching of reef Coelenterates in the San Blas Islands, Panama. Coral Reefs 3, 183–190 (1984).

    Google Scholar 

  17. D'Croz, L. & Robertson, D. R. Coastal oceanographic conditions affecting coral reefs on both sides of the Isthmus of Panama.In Proc. 8th Int. Coral Reef Symp., Vol. 2(eds. Lessios, H. A. & Macintyre, I. G.) 2053–2058 (Smithsonian Tropical Research Institute, Balboa, Panama, (1997)).

    Google Scholar 

  18. Porter, J. W., Fitt, W. K., Spero, H. J., Rogers, C. S. & White, M. W. Bleaching in reef corals: Physiological and stable isotopic responses. Proc. Natl Acad. Sci. USA 86s, 9342–9346 (1989).

    Google Scholar 

  19. Gates, R. D. Seawater temperature and sublethal coral bleaching in Jamaica. Coral Reefs 8, 193–197 (1990).

    Google Scholar 

  20. Goreau, T. F. The ecology of Jamaican coral reefs I. Species composition and zonation. Ecology 40, 67–90 (1959).

    Google Scholar 

  21. Gleason, D. F. & Wellington, G. M. Ultraviolet radiation and coral bleaching. Nature 365, 836–838 (1993).

    Article  ADS  Google Scholar 

  22. Dunbar, R. B. & Cole, J. E. Coral Records of Ocean-Atmosphere Variability (Clim. Glob. Change Prog. Spec. Rep. 10) (NOAA, Washington DC, (1993)).

    Google Scholar 

  23. Baker, A. C., Rowan, R. & Knowlton, N. Symbiosis ecology of two Caribbean acroporid corals.In Proc. 8th Int. Coral Reef Symp., Vol. 2(eds. Lessios, H. A. & Macintyre, I. G.) 1295–1300 (Smithsonian Tropical Research Institute, Balboa, Panama, (1997)).

    Google Scholar 

  24. Rowan, R. & Powers, D. A. Amolecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251, 1348–1351 (1991).

    Google Scholar 

  25. Buddemeier, R. W. & Fautin, D. G. Coral bleaching as an adaptive mechanism. Bioscience 43, 320–325 (1993).

    Google Scholar 

  26. Ware, J. R., Fautin, D. G. & Buddemeier, R. W. Patterns of coral bleaching: modelling the adaptive bleaching hypothesis. Ecol. Model. 84, 199–214 (1996).

    Google Scholar 

  27. Weil, E. & Knowlton, N. Amulticharacter analysis of the Caribbean coral Montastraea annularis (Ellis and Solander, 1786) and its two sibling species, M. faveolata (Ellis and Solander, 1786) and M. franksi Gregory, 1895). Bull. Mar. Sci. 55, 151–175 (1994).

    Google Scholar 

  28. Rowan, R. & Powers, D. A. The molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar. Ecol. Prog. Ser. 71, 65–73 (1991).

    Google Scholar 

  29. Jeffrey, S. W. & Haxo, F. T. Photosynthetic pigments of symbiotic dinoflagellates (zooxanthellae) from corals and clams. Biol. Bull. 135, 149–165 (1968).

    Google Scholar 

  30. Reynolds, R. W. & Smith, T. M. Improved global sea surface temperature analyses. J. Clim. 7, 929–948 (1994).

    Google Scholar 

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Acknowledgements

We thank R. Robertson for alerting us to the bleaching event; J. Maté and E. Gomez for assistance; K. Kaufmann for help with temperature records; R. W. Buddemeier, J. B. C. Jackson and W.Toller for comments on the manuscript; and the Government of Panama and the Kuna nation for allowing access to the site and collecting. This research was supported by the Smithsonian Institution, the Andrew W. Mellon Foundation, the Office of Naval Research, the NIH and NOAA.

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Correspondence to Rob Rowan.

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Rowan, R., Knowlton, N., Baker, A. et al. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388, 265–269 (1997). https://doi.org/10.1038/40843

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