The cumulative impact of annual coral bleaching can turn some coral species winners into losers

Global Change Biology

Volumn 20, Issue 12, 2014, Pages 3823-3833

  Grottoli, Andréa G ^a   Warner, Mark E ^b   Levas, Stephen J ^a,c   Aschaffenburg, Matthew D ^b   Schoepf, Verena ^a,d   Mcginley, Michael ^b   Baumann, Justin ^a,e   Matsui, Yohei ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

^c VILLANOVA UNIVERSITY   (United States)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Annual coral bleaching; Energy reserves; Symbiodinium type; Winners and losers

Indexed keywords

ANTHOZOA; SYMBIODINIUM;

ACCLIMATIZATION; ANALYSIS OF VARIANCE; ANIMAL; ANTHOZOA; CARIBBEAN; DINOFLAGELLATE; MICROBIOLOGY; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SPECIES DIFFERENCE; SYMBIOSIS; TEMPERATURE;

ACCLIMATIZATION; ANALYSIS OF VARIANCE; ANIMALS; ANTHOZOA; CARIBBEAN REGION; DINOFLAGELLIDA; PHOTOSYNTHESIS; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL; SYMBIOSIS; TEMPERATURE;

EID: 84912032433     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.12658     Document Type: Article

References (55)

1. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences of the United States of America, 105, 17442-17446.
2. Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: A case study of coral bleaching. Functional Ecology, 23, 539-550.
3. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals' adaptive response to climate change. Nature, 430, 741.
4. Baker AC, Glynn PW, Riegl BM (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuarine, Coastal and Shelf Science, 80, 435-471.
5. Bellantuono AJ, Hoegh-Guldberg H, Rodriguez-Lanetty M (2012) Resistance to thermal stress in corals without changes in symbiont composition. Proceedings of the Royal Society B-Biological Sciences, 279, 1100-1107.
6. 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 the Royal Society B-Biological Sciences, 273, 2305-2312.
7. Budd AF, Fukami H, Smith ND, Knowlton N (2012) Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia). Zoological Journal of the Linnean Society, 166, 465-529.
8. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. BioScience, 43, 320-326.
9. Dunn SR, Pernice M, Green K, Hoegh-Guldberg O, Dove SG (2012) Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: are the batteries of the reef going to run out? PLoS ONE, 7, E39024.
10. Eakin CM, Lough JM, Heron SF (2009) Climate variability and change: monitoring data and evidence for increased coral bleaching stress. In: Coral Bleaching: Patterns, Processes, Causes and Consequences (eds Van Oppen MJH, Lough JM), pp. 41-67. Springer-Verlag, Berlin.
11. Edmunds PJ, Gates RD (2002) Normalizing physiological data for scleractinian corals. Coral Reefs, 21, 193-197.
12. Fabricius KE (2011) Factors determining the resilience of coral reefs to eutrophication: a review and conceptual model. In: Coral Reefs: An Ecosystem in Transition. (ed. Dubinsky ZSN), pp. 493-506. Springer Science, New York.
13. Fisk DA, Done TJ(1985) Taxonomic and bathymetric patterns of bleaching in corals, Myrmidion Reef (Queensland). In: Proceedings of 5th Int Coral Reef Congress Vol 6 (eds Gabrie C, Harmelin M), pp. 149-154. Tahiti.
14. Fitt WK, Mcfarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnology and Oceanography, 45, 677-685.
15. 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.
16. Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K, Donner SD, Hoegh-Guldberg O (2012) Limiting global warming to 2 °C is unlikely to save most coral reefs. Nature Climate Change, 3, 165-170.
17. Glynn PW, Mate JL, Baker AC, Calderon MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997-1998 El Nino Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982-1983 event. Bulletin of Marine Science, 69, 79-109.
18. Gnaiger E, Bitterlich G (1984) Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. Oecologia, 62, 289-298.
19. Green DH, Edmunds PH, Carpenter RC (2008) Increasing relative abundance of Porites astreoides on Caribbean reefs mediated by an overall decline in coral cover. Marine Ecology Progress Series, 359, 1-10.
20. Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Marine Biology, 145, 621-631.
21. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature, 440, 1186-1189.
22. Guest JR, Baird AH, Maynard JA et al. (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE, 7, e33353.
23. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine Freshwater Research, 50, 839-866.
24. Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737-1742.
25. Houlbreque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biological Reviews, 84, 1-17.
26. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, Van Oppen MJH (2011) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Climate Change, 2, 116-120.
27. Hughes TP, Bellwood DR, Baird AH, Brodie J, Bruno JF, Pandolfi JM (2011) Shifting base-lines, declining coral cover, and the erosion of reef resilience: comment on Sweatman et al. Coral Reefs, 30, 653-660.
28. Jokiel PL, Maragos JE, Franzisket L (1978) Coral growth: buoyant weight technique. In: Coral Reefs: Research Methods (eds Stoddart DR, Johannes RE), pp. 529-541. UNESCO, Paris, France.
29. Jones A, Berkelmans R (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.
30. LaJeunesse TC, Bhagooli R, Hidaka M et al. (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.
31. LaJeunesse TC, Smith RT, Finney J, Oxenford H (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proceedings of the Royal Society B-Biological Sciences, 276, 4139-4148.
32. Levas SJ, Grottoli AG, Hughes A, Osburn C, Matsui Y (2013) Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals. PLoS ONE, 8, e63267.
33. Logan C, Dunne J, Eakin C, Donner S (2014) Incorporating adaptive responses into future projections of coral bleaching. Global Change Biology, 20, 125-139.
34. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Van Woesik R (2001) Coral bleaching: the winners and the losers. Ecology Letters, 4, 122-131.
35. Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs, 19, 155-163.
36. Maynard JA, Anthony KRN, Marshall PA, Masiri I (2012) Major bleaching events can lead to increased thermal tolerance in corals. Marine Biology, 155, 173-182.
37. McClanahan T, Muthiga N (2014) Community change and evidence for variable warm-water temperature adaptation of corals in Northern Male Atoll, Maldives. Marine Pollution Bulletin, 80, 107-113.
38. McGinley MP (2012) The Impact of Environmental Stress on Symbiodinium spp A Molecular and Community-Scale Investigation PhD. University of Delaware, Lewes, DE.
39. Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. Journal of Experimental Biology, 211, 1050-1056.
40. Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos, 100, 403-405.
41. Muscatine L, Mccloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnology and Oceanography, 26, 601-611.
42. Palardy JE, Rodrigues LJ, Grottoli AG (2008) The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. Journal of Experimental Marine Biology and Ecology, 367, 180-188.
43. Pratchett MS, Mccowan DM, Maynard JA, Heron SF (2013) Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea French Polynesia. PLoS ONE, 8, e70443.
44. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnology and Oceanography, 52, 1874-1882.
45. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature, 388, 265-269.
46. Smith TB, Brandt ME, Calnan JM et al. (2013) Convergent mortality responses of Caribbean coral species to seawater warming. Ecosphere, 4, 87.
47. Stimson J, Sakai K, Sembali H (2002) Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality. Coral Reefs, 21, 409-421.
48. Teneva L, Karnauskas M, Logan CA, Bianucci L, Currie JC, Kleypas JA (2012) Predicting coral bleaching hotspots: the role of regional variability in thermal stress and potential adaptation rates. Coral Reefs, 31, 1-12.
49. 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.
50. Van Hooidonk R, Maynard JA, Planes S (2013) Temporary refugia for coral reefs in a warming world. Nature Climate Change, 3, 508-511.
51. Veron JEN, Hoeg-Guldberg O, Lenton TM et al. (2009) The coral reef crisis: the critical importance of <350 ppm CO2. Marine Pollution Bulletin, 58, 1428-1436.
52. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proceedings of the National Academy of Science of the United States of America, 96, 8007-8012.
53. Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnology and Oceanography, 51, 1887-1897.
54. Wilkinson C, Hodgson G (1999) Coral reefs and the 1997-1998 mass bleaching and mortality. Nature & Resources, 35, 16-25.
55. Winer BJ (1971) Statistical Principles in Experimental Design 2nd edn. McGraw-Hill, New York.