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Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

A new conceptual model for the warm-water breakdown of the coral–algae endosymbiosis

Scott A. Wooldridge
+ Author Affiliations
- Author Affiliations

Australian Institute of Marine Science, PMB #3, Townsville MC, Qld 4810, Australia.

Marine and Freshwater Research 60(6) 483-496 https://doi.org/10.1071/MF08251
Submitted: 2 September 2008  Accepted: 28 November 2008   Published: 19 June 2009

Abstract

The symbiosis between reef-building corals and their algae endosymbionts is sensitive to temperature stress, which makes coral reefs vulnerable to climate change. However, a precise understanding of the capacity for the symbiosis to adapt to climate change is currently restricted by the lack of coherent explanation for the set of cellular events leading to its warm-water breakdown (= coral bleaching). Here, a new coral bleaching model is proposed in which the triggering event is a disruption to the ‘dark’ photosynthetic reactions of the algae endosymbionts, primarily due to a limited availability of CO2 substrate around the Rubisco enzyme (ribulose-1,5-bisphosphate carboxylase). Paradoxically, this CO2-limiting condition may be enhanced by the modern increase in atmospheric CO2 partial pressure (pCO2). Importantly, the model delivers a new standpoint from which to explain: (i) upper thermal bleaching thresholds; and (ii) the mechanism underpinning endosymbiont shuffling. Overall, the model leaves little doubt as to the diminished stability and functioning (i.e. resilience) of the coral–algae endosymbiosis due to the rising pCO2 and warming trend in the upper ocean surface layer. It is concluded that whole-colony bleaching is the destructive endpoint to a suite of cellular processes that operate near continuously in modern symbiotic corals.

Additional keywords: cell-specific density,CO2 limitation, coral bleaching, mitotic index.


Acknowledgements

This work was supported by the Australian Government’s Marine and Tropical Science Research Facility (MTSRF). The final manuscript benefited from the suggestions of several anonymous reviewers. I acknowledge the helpful editorial assistance provided by Prof. A. Boulton.


References

Ainsworth, T. D. , Hoegh-Guldberg, O. , Heron, S. F. , Skirving, W. J. , and Leggat, W. (2008). Early cellular changes are indicators of pre-bleaching thermal stress in the coral host. Journal of Experimental Marine Biology and Ecology 364, 63–71.
Crossref | GoogleScholarGoogle Scholar | Fitt W. K. (1985). Effect of different strains of zooxanthella Symbiodinium microadriaticum on growth and survival of their coelenterate and molluscan hosts. In ‘Proceedings of the 5th International Coral Reef Symposium, Tahiti, 27 May–1 June 1985, Vol. 6’. (Eds B. Delesalle, R. Galzin and B Salvat.) pp. 131–136. (Antenne Museum-EPHE: Moorea, French Polynesia.)

Fitt, W. K. (2000). Cellular growth of host and symbiont in a cnidarian-zooxanthellar symbiosis. The Biological Bulletin 198, 110–120.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | McGuire M. P., and Szmant A. M. (1997). Time course of physiological responses to NH4 enrichment by a coral–zooxanthellae symbiosis In ‘Proceedings of the 8th International Coral Reef Symposium, Panama, 24–29 June 1996, Vol. 1’. (Eds H. A. Lessios and I. G. Macintyre) pp. 909–914. (Smithsonian Tropical Research Institute: Balboa, Republic of Panama.)

Mendes, J. M. , and Woodley, J. D. (2002). Effect of the 1995–1996 bleaching event on polyp tissue depth, growth, reproduction and skeletal band formation in Montastraea annularis. Marine Ecology Progress Series 235, 93–102.
Crossref | GoogleScholarGoogle Scholar | Muscatine L., McCloskey L., and Loya Y. (1985). A comparison of the growth rates of zooxanthellae and animal tissue in the Red Sea coral Stylophora pistillata. In ‘Proceedings of the 5th International Coral Reef Symposium, Tahiti, 27 May–1 June 1985, Vol. 6’. (Eds B. Delesalle, R. Galzin and B. Salvat.) pp. 119–123. (Antenne Museum-EPHE: Moorea, French Polynesia.)

Muscatine, L. , Porter, J. W. , and Kaplan, I. R. (1989). Resource partitioning by reef corals as determined from stable isotope composition: I. δ13C of zooxanthellae and animal tissue vs. depth. Marine Biology 100, 185–193.
Crossref | GoogleScholarGoogle Scholar | Najjar R. G. (1992). Marine biogeochemistry. In ‘Climate System Modeling’. (Ed. K. Trenberth.) pp. 241–280. (Cambridge University Press, Cambridge, UK.)

Oliver, J. K. (1984). Intra-colony variation in the growth of Acropora formosa: extension rates and skeletal structure of white (zooxanthellae-free) and brown-tipped branches. Coral Reefs 3, 139–147.
Crossref | GoogleScholarGoogle Scholar | Steven A. D. L., and Broadbent A. H. (1997). Growth and metabolic responses of Acropora palifera to long term nutrient enrichment. In ‘Proceedings of the 8th International Coral Reef Symposium, Panama, 24–29 June 1996, Vol. 1’. (Eds H. A. Lessios and I. G. Macintyre.) pp. 867–872. (Smithsonian Tropical Research Institute: Balboa, Republic of Panama.)

Stimson, J. (1997). The annual cycle of density of zooxanthellae in the tissues of field and laboratory-held Pocillopora damicornis (Linnaeus). Journal of Experimental Marine Biology and Ecology 214, 35–48.
Crossref | GoogleScholarGoogle Scholar | True J. D. (2005). Massive Porites corals as indicators of environmental change. Ph.D. Thesis, James Cook University, Townsville.

Verde, E. A. , and McCloskey, L. R. (1996). Photosynthesis and respiration of two species of algal symbionts in the anemone Anthopleura elegantissima (Brandt) (Cnidaria; Anthozoa). Journal of Experimental Marine Biology and Ecology 195, 187–202.
Crossref | GoogleScholarGoogle Scholar | Wooldridge S. A., and Done T. D. (2009). Improved water quality can ameliorate effects of climate change on corals. Ecological Applications, in press.

Wooldridge, S. A. , Brodie, J. , and Furnas, M. (2006). Exposure of inner-shelf reefs to nutrient enriched runoff entering the Great Barrier Reef Lagoon: Post-European changes and the design of water quality targets. Marine Pollution Bulletin 52, 1467–1479.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |