Levels of immunity parameters underpin bleaching and disease susceptibility of reef corals

FASEB Journal

Volumn 24, Issue 6, 2010, Pages 1935-1946

  Palmer, Caroline V ^a,b   Bythell, John C ^b   Willis, Bette L ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Climate change; Fluorescent protein; Melanin; Phenoloxidase; Reef resilience

Indexed keywords

MELANIN; MONOPHENOL MONOOXYGENASE;

ARTICLE; BLEACHING; CELL SIZE; CONCENTRATION (PARAMETERS); CORAL REEF; DISEASE PREDISPOSITION; ENZYME ACTIVITY; GRANULAR CELL; IMMUNITY; IMMUNOLOGICAL PARAMETERS; NONHUMAN; PRIORITY JOURNAL;

ACCLIMATIZATION; ANIMALS; ANTHOZOA; DISEASE SUSCEPTIBILITY; ENVIRONMENTAL MONITORING; GREEN FLUORESCENT PROTEINS; MARINE BIOLOGY; MELANINS; MONOPHENOL MONOOXYGENASE; PIGMENTATION;

ALCYONACEA; ANTHOZOA; INVERTEBRATA; SCLERACTINIA;

EID: 77953488633     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-152447     Document Type: Article

References (126)

1. Hoegh-Guldberg, O. (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshw. Res. 50, 839-866
2. 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., and Hatziolos, M. E. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318, 1737-1742
3. Harvell, C. D. C. E. Mitchell, J. R. Ward, Altizer, S. A. P. Dobson, R. S. Ostfeld, and M. D. Samual(2002) Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158
4. Bruno, J. F., Selig, E. R., Casey, K. S., Page, C. A., Willis, B. L., Harvell, C. D., Sweatman, H., and Melendy, A. M. (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol. 5, 1-8
5. Harvell, C. D., Jordan, E., Merkel, S., Raymundo, L., Rosenberg, E., Smith, G., Weil, E., and Willis, B. L. (2007) Coral disease: environmental change and the balance between coral and microbes. Oceanography 20, 58-81
6. Hughes, T. P. (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265, 1547-1551
7. Aronson, R. B., Bruno, J. F., Precht, W. F., Glynn, P. W., Harvell, C. D., Kaufman, L., Rogers, C. S., Shinn, E. A., and Valentine, J. F. (2003) Causes of coral reef degradation. Science 302, 1502-1502
8. Aronson, R. B., Macintyre, I. G., Wapnick, C. M., and O'Neill, M. W. (2004) Phase shifts, alternative states, and the unprecedented convergence of two reef systems. Ecology 85, 1876-1891
9. Bellwood, D. R., Hughes, T. P., Folke, C., and Nystrom, M. (2004) Confronting the coral reef crisis. Nature 429, 827-833
10. Mydlarz, L. D., Holthouse, S. F., Peters, E. C., and Harvell, C. D. (2008) Celluar responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors. PloS One 3, e1811
11. Palmer, C. V., Mydlarz, L. D., and Willis, B. L. (2008) Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals. Proc. R. Soc. Lond. B Biol. Sci. 275, 2687-2693
12. Palmer, C. V., Roth, M. S., and Gates, R. D. (2009a) Red fluorescent protein responsible for pigmentation in trematode-infected Porites compressa tissues. Biol. Bull. 215, 68
13. Stearns, S. C. (1993) The Evolution of Life Histories, Oxford University Press, Oxford, UK
14. Sandland, G. J., and Minchella, D. J. (2003) Costs of immume defense: an enigma wrapped in an environmental cloak? Trends Parasitol. 19, 571-574
15. Sadd, B. M., and Schmid-Hempel, P. (2009) Principles of ecological immunology. Evol. Appl. 2, 113-121
16. Rolff, J., and Siva-Jothy, M. T. (2003) Invertebrate ecological immunity. Science 301, 472-475
17. Rinkevich, B. (1996) Do reproduction and regeneration in damaged corals compete for energy allocation? Mar. Ecol. Prog. Ser. 143, 297-302
18. Sheldon, B. C., and Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321 (Pubitemid 27003142)
19. Hosken, D. J. (2001) Sex and death: microevolutionary trade-offs between reproductive and immune investment in dung flies. Curr. Biol. 11, R379-R380
20. Marshall, P. A., and Baird, A. H. (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19, 155-163
21. Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H., and van Woesik, R. (2001) Coral bleaching: the winners and the losers. Ecol. Lett. 4, 122-131
22. Baird, A. H., and Marshall, P. A. (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 237, 133-141
23. McClanahan, T. R., Baird, A. H., Marshall, P. A., and Toscano, M. A. (2004) Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Mar. Pollut. Bull. 48, 327-335
24. Willis, B. L., Page, C. A., and Dinsdale, E. A. (2004) Coral disease on the Great Barrier Reef. In Coral Health and Disease (Rosenberg, E., and Loya, Y., eds) pp. 69-104, Springer, New York
25. Page, C. A., and Willis, B. L. (2006) Distribution, host range and large-scale spatial variability in black band disease prevalence on the Great Barrier Reef, Australia. Dis. Aquat. Org. 69, 41-51
26. Page, C. A., and Willis, B. L. (2008) Epidemiology of skeletal eroding band on the Great Barrier Reef and the role of injury in the initiation of this widespread coral disease. Coral Reefs 27, 257-272
27. Bythell, J. C. (1988) A total nitrogen and carbon budget for the elkhorn coral Acropora palmata (Lamarck). Proc. 6th Int. Coral Reef Symp. 6, 535-540
28. Gates, R. D., Baghdasarian, G., and Muscatine, L. (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol. Bull. 182, 324-332 (Pubitemid 23402250)
29. Brown, B. E. (1997) Coral bleaching: causes and consequences. Coral Reefs 16, S129-S138
30. Weis, V. M. (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 211, 3059-3066
31. Raymundo, L. J., Rosell, K. B., Reboton, C. T., and Kaczmarsky, L. (2005) Coral diseases on Philippine reefs: genus Porites is a dominant host. Dis. Aquat. Org. 64, 181-191
32. Hoegh-Guldberg, O., and Smith, G. J. (1989) The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J. Exp. Mar. Biol. Ecol. 129, 279-303
33. Muscatine, L., Grossman, D., and Doino, J. (1991) Release of symbiotic algae by tropical sea anemones and corals after cold shock. Mar. Ecol. Prog. Ser. 77, 233-243
34. Berkelmans, R., and Oliver, J. K. (1999) Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18, 55-60
35. Nishiyama, Y., Allakhverdiev, S. I., and Murata, N. (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta 1757, 742-749
36. Jones, R. J., Hoegh-Guldberg, O., Larkum, A. W. D., and Schreiber, U. (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation menchanisms of zooxanthellae. Plant Cell Environ. 21, 1219-1230 (Pubitemid 29051743)
37. Baird, A. H., Bhagooli, R., Ralph, P. J., and Takahashi, S. (2008) Coral bleaching: the role of the host. Trends Ecol. Evol. 24, 16-20
38. McClanahan, T. R. (2004) The relationship between bleaching and mortality of common corals. Mar. Biol. 144, 1239-1245
39. Fabricius, K., De'ath, G., McCook, L., Turak, E., and Williams, D. M. (2005) Changes in algal, coral and fish assemblages along water quality gradients on the inshore Great Barrier Reef. Mar. Poll. Bull. 51, 384-398
40. Abrego, D., Ulstrup, K. E., Willis, B. L., and van Oppen, M. J. H. (2008) Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc. R. Soc. Lond. B Biol. Sci. 275, 2273-2282
41. Fitt, W. K., Gates, R. D., Hoegh-Guldberg, O., Bythell, J. C., Jatkar, A., Grottoli, A. G., Gomez, M., Fisher, P., Lajuenesse, T. C., Pantos, O., Iglesias-Prieto, R., Franklin, D. J., Rodrigues, L. J., Torregiani, J. M., van Woesik, R., and Lesser, M. P. (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. J. Exp. Mar. Biol. Ecol. 373, 102-110
42. Brown, B. E., Dunne, R. P., Goodson, M. S., and Douglas, A. E. (2000) Bleaching patterns in reef corals. Nature 404, 142-143
43. Brown, B. E., Dunne, R. P., Goodson, M. S., and Douglas, A. E. (2002) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21, 119-126 (Pubitemid 36064610)
44. Shick, J. M., and Dunlap, W. C. (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu. Rev. Physiol. 64, 223-262
45. Lesser, M. P. (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu. Rev. Physiol. 68, 253-278
46. Salih, A., Larkum, A., Cox, G., Kuhl, M., and Hoegh-Guldberg, O. (2000) Fluorescent pigments in corals are photoprotective. Nature 408, 850-853
47. Dove, S. G., Hoegh-Guldberg, O., and Ranganathan, S. (2001) Major colour patterns of reef-building corals are due to a family of GFP-like proteins. Coral Reefs 19
48. Matz, M. V., A. F. Fradkov, Y. A. Labas, A. P. Savitsky, A. G. Zaraisky, M. L. Markelov, and Lukyanov., S. A. (1999) Fluorescent proteins from nonbioluminescent Anthozoa species. Nat. Biotechnol. 17, 969-973
49. Kelmanson, I. V., and Matz, M. V. (2003) Molecular basis and evolutionary origins of color diversity in great star coral Montastraea cavernosa (Scleractinia: Faviida). Mol. Biol. Evol. 20, 1125-1133
50. Alieva, N. O., K. A. Konzen, S. F. Field, E. A. Meleshkevitch, M. E. Hunt, V. Beltran-Ramirez, D. J. Miller, J. Wiedenmann, A. Salih, and Matz., M. V. (2008) Diversity and evolution of coral fluorescent proteins. PloS One 3, e2680
51. Tsien, R. Y. (1998) The green fluorescent protein. Annu. Rev. Biochem. 67, 509-544
52. Salih, A., Hoegh-Guldberg, O., and Cox, G. (1998) Photoprotection of symbiotic dinoflagellates by fluorescent pigments in reef corals. In Proceedings of the Australian Coral Reef Society 75th Anniversary Conference, Heron Island October 1997. (Greenwood, J. G., and Hall, N. J., eds) pp. 217-230, University of Queensland, Brisbane, Australia
53. Dove, S. G., Ortiz, J. C., Enr?íquez, S., Fine, M., Fisher, P., Iglesias-Prieto, R., Thornhill, D., and Hoegh-Guldberg, O. (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol. Oceanogr. 51, 1149-1158
54. Bou-Abdallah, F., D. N. Chasteen, and Lesser., M. (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim. Biophys. Acta 1760, 1690-1695
55. Palmer, C. V., Modi, C. K., and Mydlarz, L. D. (2009b) Coral fluorescent proteins as antioxidants. PLoS One 4, e7298
56. Lesser, M. P. (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol. Oceanogr. 41, 271-283
57. Costantini, D., and Moller, A. P. (2009) Does immune response cause oxidative stress in birds? A meta-analysis. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 153, 339-344
58. Hawkridge, J. M., Pipe, R. K., and Brown, B. E. (2000) Localization of antioxidant enzymes in the cnidarians Anemonia viridis and Goniopora stokesi. Mar. Biol. 137, 1-9
59. Mydlarz, L. D., and Harvell, C. D. (2007) Peroxidase activity and inducibility in the sea fan coral exposed to a fungal pathogen. Comp. Biochem. Physiol. A. 146, 54-62
60. Harvell, C. D., Kim, K., Burkholder, J. M., Colwell, R. R., Epstein, P. R., Grimes, D. J., Hofmann, E. E., Lipp, E. K., Osterhaus, A. D., Overstreet, R. M., Porter, J. W., Smith, G. W., and Vasta, G. R. (1999) Emerging marine diseases - climate links and anthropogenic factors. Science 285, 1505-1510
61. Mydlarz, L. D., Jones, L. E., and Harvell, C. D. (2006) Innate immunity, environmental drivers, and disease ecology of marine and freshwater invertebrates. Annu. Rev. Ecol. Evol. Syst. 37, 251-288
62. Selig, E. R., Harvell, C. D., Bruno, J. F., Willis, B. L., Page, C. A., Casey, K. S., and Sweatman, H. (2006) Analyzing the relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales. In Coral Reefs and Climate Change: Science and Management (Phinney, J. T., Hoegh-Guldberg, O., J Kleypas, J., Skirving, W., and Strong, A., eds) pp. 111-128, American Geophysical Union, Washington, DC
63. Bruno, J. F., Petes, L. E., Harvell, C. D., and Hettinger, A. (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol. Lett. 6, 1056-1061
64. Ward, J. R., Rypien, K. L., Bruno, J. F., Harvell, C. D., Jordan-Dahlgren, E., Mullen, K. M., Rodriguez-Martinez, R. E., Sanchez, J., and Smith, G. (2006) Coral diversity and disease in Mexico. Dis. Aquat. Org. 69, 23-31
65. Weil, E., and Croquer, A. (2009) Spatial variability in distribution and prevalence of Caribbean scleractinian coral and octocoral diseases. I. Community-level analysis. Dis. Aquat. Org. 83, 195-208
66. Stedman, T. L. (2000) Stedman's Medical Dictionary, Lippincott, Williams and Wilkins, Baltimore, MD, USA
67. Cooper, M. D., and Koprowski, H. (2002) The Interface Between Innate and Acquired Immunity, Springer, Berlin, Germany
68. Rinkevich, B. (2004) Primitive immune systems: are your ways my ways? Immunol. Rev. 198, 25-35
69. Söderhäll, K. (1982) Prophenoloxidase activating system and melanization - a recognition mechanism of arthropods? - a review. Dev. Comp. Immunol. 6, 601-611
70. Asokan, R., Arumugam, M., and Mullainadhan, P. (1997) Activation of prophenoloxidase in the plasma and haemocytes of the marine mussel, Perna viridis Linnaeus. Dev. Comp. Immunol. 21, 1-12
71. Sugumaran, M. (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res. 15, 2-9
72. Munoz, P., Meseguer, J., and Esteban, M. A. (2006) Phenoloxidase activity in three commercial bivalve species. Changes due to natural infestation with Perkinsus atlanticus. Fish Shellfish Immunol. 20, 12-19
73. Cerenius, L., Lee, B. L., and Söderhäll, K. (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 29, 263-271
74. Rowley, A. F. (1996) The evolution of inflammatory mediators. Mediators Inflamm. 5, 3-13
75. Nappi, A. J., and Christensen, B. M. (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem. Mol. Biol. 35, 443-459
76. Nappi, A. J., and Ottaviani, E. (2000) Cytotoxicity and cytotoxic molecules in invertebrates. Bioessays 22, 469-480
77. Miller, D. J., Hemmrich, G., Ball, E. E., Hayward, D. C., Khalturin, K., Funayama, N., Agata, K., and Bosch, T. C. G. (2007) The innate immune repertoire in Cnidaria-ancestral complexity and stochastic gene loss. Genome Biol. 8, R59
78. Kvennefors, E. C. E., Leggat, W., Hoegh-Guldberg, O., Degnan, B. M., and Barnes, A. C. (2008) An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Devel. Comp. Immunol. 32, 1582-1592
79. Mydlarz, L. D., Couch, C. S., Weil, E., Smith, G., and Harvell, C. D. (2009) Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event. Dis. Aquat. Org. 87, 67-78
80. Meredith, P., Powell, B. J., Riesz, J., Nighswander-Rempel, S. P., Pederson, M. R., and Moore, E. G. (2006) Towards structureproperty-function relationships for eumelanin. Soft Matter 2, 37-44
81. Adamo, S. A. (2004) How should behavioural ecologists interpret measurements of immunity? Anim. Behav. 68, 1443-1449
82. Adamo, S. A. (2004) Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket Gryllus texensis. J. Insect Physiol. 50, 209-216
83. Newton, K., Peters, R., and Raftos, D. (2004) Phenoloxidase and QX disease resistance in Sydney rock oysters (Saccostrea glomerata). Dev. Comp. Immunol. 28, 565-569
84. Schwarzenbach, G. A., and Ward, P. I. (2007) Phenoloxidase activity and pathogen resistance in yellow dung flies Scathophaga stercoraria. J. Evol. Biol. 20, 2192-2199
85. Butt, D., and Raftos, D. (2008) Phenoloxidase-associated cellular defence in the Sydney rock oyster, Saccostrea glomerata, provides resistance against QX disease infections. Dev. Comp. Immunol. 32, 299-306
86. Wilson, K., Cotter, S. C., Reeson, A. F., and Pell, J. K. (2001) Melanism and disease resistance in insects. Ecol. Lett. 4, 637-649
87. Armitage, S. A. O., and Siva-Jothy, M. T. (2005) Immune function responds to selection for cuticular colour in Tenebrio molitor. Heredity 94, 650-656
88. Siva-Jothy, M. T., Moret, Y., and Rolff, J. (2005) Insect immunity: an evolutionary ecology perspective. Adv. Insect Physiol. 32, 1-48
89. Nosanchuk, J. D., and Casadevall, A. (2003) The contribution of melanin to microbial pathogenesis. Cell. Microbiol. 5, 203-223
90. Burkhart, C. G., and Burkhart, C. N. (2005) The mole theory: primary function of melanocytes and melanin may be antimicrobial defense and immunomodulation (not solar protection). Int. J. Dermatol. 44, 340-342
91. Söderhäll, K., and Cerenius, L. (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr. Op. Immunol. 10, 23-28
92. Laufer, Z., Beckett, R. P., and Minibayeva, F. V. (2006) Co-occurrence of the multicopper oxidases tyrosinase and laccase in lichens in sub-order Peltigerineae. Ann. Bot. 98, 1035-1042
93. Mayer, A. M., and Staples, R. C. (2002) Laccase: new functions for an old enzyme. Phytochemistry 60, 551-565
94. Barnes, A. I., and Siva-Jothy, M. T. (2000) Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L-(Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc. R. Soc. Lond. B Biol. Sci. 267, 177-182
95. Bull, A. T. (1970) Inhibition of polysaccharases by melanin - enzyme inhibition in relation to mycolysis. Arch. Biochem. Biophys. 137, 345-356
96. Brenner, M., and Hearing, V. J. (2008) The protective role of melanin against UV damage in human skin. Photochem. Photobiol. 84, 539-549
97. Domart-Coulon, I. J., Traylor-Knowles, N., Peters, E., Elbert, D., Downs, C. A., Price, K., Stubbs, J., McLaughlin, S., Cox, E., Aeby, G., Brown, P. R., and Ostrander, G. K. (2006) Comprehensive characterization of skeletal tissue growth anomalies of the finger coral Porites compressa. Coral Reefs 25, 531-543
98. Metchnikoff, E. (1892) Lecons sur la Pathologie Comparee de Inflammation [reissued 1968 in English as Lectures on the Comparative Pathology of Inflammation], Masson, New York
99. Wootton, E. C., and Pipe, R. K. (2003) Structural and functional characterisation of the blood cells of the bivalve mollusc, Scrobicularia plana. Fish Shellfish Immunol. 15, 249-262
100. Cooper, E. L. (2008) From Darwin and Metchnikoff to Burnet and beyond. Contrib. Microbiol. 15, 1-11
101. Hutton, D. M. C., and Smith, V. J. (1996) Antibacterial properties of isolated amoebocytes from the sea anemone Actinia equina. Biol. Bull. 191, 441-451
102. Meszaros, A., and Bigger, C. (1999) Qualitative and quantitative study of wound healing processes in the coelenterate, Plexaurella fusifera: spatial, temporal, and environmental (light attenuation) influences. J. Invertebr. Pathol. 73, 321-331
103. Olano, C. T., and Bigger, C. H. (2000) Phagocytic activities of the gorgonian coral Swiftia exserta. J. Invertebr. Pathol. 76, 176-184
104. Maynard, J. A., Anthony, K. R. N., Marshall, P. A., and Masiri, I. (2008) Major bleaching events can lead to increased thermal tolerance in corals. Mar. Biol. 155, 173-182
105. Thompson, D. M., and van Woesik, R. (2009) Corals escape bleaching in regions that recently and historically experienced frequent thermal stress. Proc. R. Soc. Lond. B Biol. Sci. 276, 2893-2901
106. Rinkevich, B., and Muller, W. E. G. (1996) Invertebrate Immunology, Springer, Berlin
107. Hildemann, W. H. (1977) Specific immunorecognition by histo-compatibility markers: the original polymorphic system of immunoreactivity characteristic of all multicellular animals. Immunogenetics 5, 193-202
108. Mucklow, P. T., Vizoso, D. B., Jensen, K. H., Refardt, D., and Ebert, D. (2004) Variation in phenoloxidase activity and its relation to parasite resistance within and between populations of Daphnia magna. Proc. R. Soc. Lond. B Biol. Sci 271, 1175-1183
109. Roff, G., Hoegh-Guldberg, O., and Fine, M. (2006) Intracolonial response to Acroporid "white syndrome" lesions in tabular Acropora spp. (Scleractinia). Coral Reefs 25, 255-264
110. Cox, G., Matz, M. V., and Salih, A. (2007) Fluorescence lifetime imaging of coral fluorescent proteins. Microsc. Res. Tech. 70, 243-251
111. Dove, S. G. (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar. Ecol. Prog. Ser. 272, 99-116
112. Salih, A., Larkum, A. W. D., and Cox, C. (2001) Photoprotection from photoinhibition of symbiotic algae in corals by fluorescent pigments. Photosyn. Res. 69, 221-222
113. Leutenegger, A., Kredel, S., Gundel, S., D'Angelo, C., Salih, A., and Wiedenmann, J. (2007) Analysis of fluorescent and non-fluorescent sea anemones from the Mediterranean sea during a bleaching event. J. Exp. Mar. Biol. Ecol. 353, 221-234 (Pubitemid 350137370)
114. Dove, S. G., Lovell, C., Fine, M., Deckenback, J., Hoegh-Guldberg, O., Iglesias-Prieto, R., and Anthony, K. R. N. (2008) Host pigments: potential facilitators of photosynthesis in coral symbioses. Plant Cell Environ. 31, 1523-1533
115. Smith-Keune, C., and Dove, S. (2008) Gene expression of a green fluorescent protein homolog as a host-specific biomarker of heat stress within a reef-building coral. Marine Biotechnol. 10, 166-180
116. Kramarsky-Winter, E., and Loya, Y. (1996) Regeneration versus budding in fungiid corals: a trade-off. Mar. Ecol. Progr. Ser. 134, 179-185 (Pubitemid 26270394)
117. Stearns, S. C. (1992) The Evolution of Life Histories, Oxford University Press, Oxford
118. Jackson, J. B. C. (1979) Morphological strategies in sessile organisms. In Biology and Systematics of Colonial Animals (Larwood, G., ed) pp. 499-555, Academic Press, London
119. Harrison, P. L., and Wallace, C. C. (1990) Reproduction, dispersal and recruitment of scleractinian corals. In Ecosystems of the World 25: Coral Reefs (Dubinsky, Z., ed) pp. 133-207, Elsevier, New York
120. Soong, K. (1991) Sexual reproductive patterns of shallow-water reef corals in panama. Bull. Mar. Sci. 49, 832-846
121. Soong, K. Y., and Lang, J. C. (1992) Reproductive integration in reef corals. Biol. Bull. 183, 418-431
122. Veron, J. E. N. (2000) Corals of the World, Australian Institute of Marine Science, Townsville, Australia
123. Huston, M. A. (1985) Patterns of species-diversity on coral reefs. Ann. Rev. Ecol. Syst. 16, 149-177
124. Crabbe, M. J. C. (2009) Scleractinian coral population size structures and growth rates indicate coral resilience on the fringing reefs of North Jamaica. Mar. Environ. Res. 67, 189-198
125. Leuzinger, S., Anthony, K. R. N., and Willis, B. L. (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136, 524-531
126. Lang, J. C., and Chornesky, E. A. (1990) Competion between scleractinian reef corals - a review of mechanisms and effects. In Ecosystems of the World 25: Coral Reefs (Dubinsky, Z., ed) pp. 209-252, Elsevier, New York