Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage

Journal of Experimental Marine Biology and Ecology

Volumn 461, Issue , 2014, Pages 469-478

  Baumann, Justin ^a,b   Grottoli, Andréa G ^a   Hughes, Adam D ^a,c   Matsui, Yohei ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c Scottish Assoc for Marine Science   (Germany)

Author keywords

Coral bleaching; Heterotrophy; Lipid storage; Lipid synthesis; Lipids; Photoautotrophy

Indexed keywords

BLEACHING; CARBOHYDRATE; CARBON; CORAL REEF; HETEROTROPHY; LIPID; MOLECULAR ANALYSIS; PARAMETERIZATION; PHOTOAUTOTROPHY; PHYSIOLOGY; PROTEIN;

ANTHOZOA;

EID: 84908657102     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2014.09.017     Document Type: Article

References (61)

1. Alamaru A., Loya Y., Brokovich E., Yam R., Shemesh A. Carbon and nitrogen utilization in two species of Red Sea corals along a depth gradient: insights from stable isotope analysis of total organic material and lipids. Geochim. Cosmochim. Acta 2009, 73:5333-5342.
2. Anthony K.R.N. Coral suspension feeding on fine particulate matter. J. Exp. Mar. Biol. Ecol. 1999, 232:85-106.
3. Anthony K.R.N., Fabricius K.E. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J. Exp. Mar. Biol. Ecol. 2000, 252:221-253.
4. Anthony K.R.N., Hoogenboom M.O., Maynard J.A., Grottoli A.G., Middlebrook R. Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct. Ecol. 2009, 23:539-550.
5. Bachar A., Achituv Y., Pastemak Z., Dubinsky Z. Autotrophy versus heterotrophy: the origin of carbon determines its fate in a symbiotic sea anemone. J. Exp. Mar. Biol. Ecol. 2007, 349:295-298.
6. Battey J.F., Patton J.S. A reevaluation of the role of glycerol in carbon translocation in zooxanthellae-coelenterate symbiosis. Mar. Biol. 1984, 79:27-38.
7. Birsoy K., Festuccia W.T., Laplante M. A comparative perspective on lipid storage in animals. J. Cell Sci. 2013, 126:1541-1552.
8. Brown B.E., Bythell J.C. Perspectives on mucus secretion in reef corals. Mar. Ecol. Prog. Ser. 2005, 296:291-309.
9. Buddemeier R.W., Kleypas J.A., Aronson R.B. Coral Reefs and Global Climate Change: Potential Contributions of Climate Change to Stresses on Coral Reef Ecosystems 2004, Pew Center on Global Climate Change, Arlington, VA 56.
10. Carricart-Ganivet J.P., Cabanillas-Teran N., Cruz-Ortega I., Blanchon P. Sensitivity of calcification to thermal stress varies among genera of massive reef-building corals. PLoS One 2012, 7.
11. Christie W., Han X. Lipid Analysis: Isolation, Separation, Identification and Lipidomic Analysis 2010, Oily Press.
12. Connolly S.R., Lopez-Yglesias M.A., Anthony K.R.N. Food availability promotes rapid recovery from thermal stress in a scleractinian coral. Coral Reefs 2012, 31:951-960.
13. Cox E.F. Continuation of sexual reproduction in Montipora capitata following bleaching. Coral Reefs 2007, 26:721-724.
14. D'Croz L., Mate J.L., Oke J.E. Responses to elevated seawater temperature and UV radiation in the coral Porites lobata from upwelling and non-upwelling environments on the Pacific coast of Panama. Bull. Mar. Sci. 2001, 69:203-214.
15. deGroot P.A. Handbook of Stable Isotope Analytical Techniques 2004, Elsevier, Amsterdam.
16. Donner S.D. Coping with commitment: projected thermal stress on coral reefs under different future scenarios. PLoS One 2009, 4.
17. Donner S.D., Knutson T.R., Oppenheimer M. Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:5483-5488.
18. Falkowski P.G., Dubinsky Z., Muscatine L., McCloskey L. Population-control in symbiotic corals. Bioscience 1993, 43:606-611.
19. Fitt W.K., Spero H.J., Halas J., White M.W., Porter J.W. Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean "bleaching event". Coral Reefs 1993, 12:57-64.
20. Frieler K., Meinshausen M., Golly A., Mengel M., Lebek K., Donner S.D., Hoegh-Guldberg O. Limiting global warming to 2°C is unlikely to save most coral reefs. Nat. Clim. Change 2013, 3:165-170.
21. Glynn P. Coral reef bleaching: facts, hypotheses and implications. Glob. Change Biol. 1996, 2:495-509.
22. Goreau T.F., Yonge C.M., Goreau N.I. Reef coral - autotrophs or heterotrophs?. Biol. Bull. 1971, 141:247
23. Grottoli A.G., Rodrigues L.J. Bleached Porites compressa and Montipora capitata corals catabolize delta C-13-enriched lipids. Coral Reefs 2011, 30:687-692.
24. Grottoli A.G., Rodrigues L.J., Juarez C. Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar. Biol. 2004, 145:621-631.
25. Grottoli A.G., Rodrigues L.J., Palardy J.E. Heterotrophic plasticity and resilience in bleached corals. Nature 2006, 440:1186-1189.
26. Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshw. Res. 1999, 50:839-866.
27. 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., Hatziolos M.E. Coral reefs under rapid climate change and ocean acidification. Science 2007, 318:1737-1742.
28. Houlbreque F., Ferrier-Pages C. Heterotrophy in tropical scleractinian corals. Biol. Rev. 2009, 84:1-17.
29. Hughes A.D., Grottoli A.G. Heterotrophic compensation: a possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress?. PLoS One 2013, 8:e81172.
30. Hughes A.D., Grottoli A.G., Pease T.K., Matsui Y. Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar. Ecol. Prog. Ser. 2010, 420:91-101.
31. Hughes T.P., Baird A.H., Bellwood D.R., Card M., Connolly S.R., Folke C., Grosberg R., Hoegh-Guldberg O., Jackson J.B.C., Kleypas J., Lough J.M., Marshall P., Nystrom M., Palumbi S.R., Pandolfi J.M., Rosen B., Roughgarden J. Climate change, human impacts, and the resilience of coral reefs. Science 2003, 301:929-933.
32. Jokiel P.L., Coles S.L. Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 1990, 8:155-162.
33. Leder J.J., Szmant A.M., Swart P.K. The effect of prolonged bleaching on skeletal banding and stable isotopic composition in Montastrea annularis - preliminary observations. Coral Reefs 1991, 10:19-27.
34. Lesser M.P. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 1997, 16:187-192.
35. Levas S.J. Biogeochemistry and Physiology of Bleached and Recoverying Hawaiian and Caribbean Corals 2012.
36. Levas S.J., Grottoli A.G., Hughes A., Osburn C.L., Matsui Y. Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals. PLoS One 2013, 8:e63267.
37. Moran M.D. Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 2003, 100:403-405.
38. Muscatine L., McCloskey L.R., Marian R.E. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr. 1981, 26:601-611.
39. Omori M., Fukami H., Kobinata H., Hatta M. Significant drop of fertilization of Acropora corals in 1999: an after-effect of heavy coral bleaching?. Limnol. Oceanogr. 1999, 46:704-706.
40. Palardy J.E., Rodrigues L.J., Grottoli A.G. The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. J. Exp. Mar. Biol. Ecol. 2008, 367:180-188.
41. Patton J.S., Abraham S., Benson A.A. Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae: evidence for a light-driven carbon cycle between symbiont and host. Mar. Biol. 1977, 44:235-247.
42. 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. U. S. A. 1989, 86:9342-9346.
43. Quinn G.P., Keough M.J. Experimental Design and Data Analysis for Biologists 2002, Cambridge University Press, Cambridge, UK; New York.
44. Rodrigues L.J., Grottoli A.G. Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals. Geochim. Cosmochim. Acta 2006, 70:2781-2789.
45. Rodrigues L.J., Grottoli A.G. Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol. Oceanogr. 2007, 52:1874-1882.
46. Rodrigues L.J., Grottoli A.G., Lesser M.P. Long-term changes in the chlorophyll fluorescence of bleached and recovering corals from Hawaii. J. Exp. Biol. 2008, 211:2502-2509.
47. Rodrigues L.J., Grottoli A.G., Pease T.K. Lipid class composition of bleached and recovering Porites compressa (Dana, 1846) and Montipora capitata (Dana, 1846) corals from Hawaii. J. Exp. Mar. Biol. Ecol. 2008, 358:136-143.
48. Stanley G.D. The evolution of modern corals and their early history. Earth Sci. Rev. 2003, 60:195-225.
49. Stimson J.S. Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. Bull. Mar. Sci. 1987, 41:889-904.
50. Sudek M., Aeby G.S., Davy S.K. Localized bleaching in Hawaii causes tissue loss and a reduction in the number of gametes in Porites compressa. Coral Reefs 2012, 31:351-355.
51. Szmant A.M., Gassman N.J. The effects of prolonged bleaching on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 1990, 8:217-224.
52. Tremblay P., Peirano A., Ferrier-Pages C. Heterotrophy in the Mediterranean symbiotic coral Cladocora caespitosa: comparison with two other scleractinian species. Mar. Ecol. Prog. Ser. 2011, 422:165-177.
53. Tremblay P., Naumann M.S., Sikorski S., Grover R., Ferrier-Pagès C. Experimental assessment of organic carbon fluxes in the scleractinian coral Stylophora pistillata during a thermal and photo stress event. Mar. Ecol. Prog. Ser. 2012, 453:63-77.
54. van Hooidonk R., Maynard J.A., Planes S. Temporary refugia for coral reefs in a warming world. Nat. Clim. Change 2013, 3:508-511.
55. 2. Mar. Pollut. Bull. 2009, 58:1428-1436.
56. Ward S. Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis. Coral Reefs 1995, 14:87-90.
57. Ward S., Harrison P.J., Hoegh-Guldberg O. Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. Proceedings of the 9th International Coral Reef Symposium 2000, 2:1123-1128.
58. Warner M.E., Fitt W.K., Schmidt G.W. The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ. 1996, 19:291-299.
59. Wilkinson C. Status of Coral Reefs of the World: 2000 2000, Australian Institute for Marine Science, Townsville.
60. Winer B. Statistical Problems in Experimental Design 1971, McGraw-Hill, New York.
61. Wooldridge S., Done T., Berkelmans R., Jones R., Marshall P. Precursors for resilience in coral communities in a warming climate: a belief network approach. Mar. Ecol. Prog. Ser. 2005, 295:157-169.