Responses to High Seawater Temperatures in Zooxanthellate Octocorals

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Sammarco, Paul W ^a   Strychar, Kevin B ^b  

^a LOUISIANA UNIVERSITIES MARINE CONSORTIUM   (United States)

^b GRAND VALLEY STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEA WATER;

APOPTOSIS; ARTICLE; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CORAL; DINOFLAGELLATE; EXPERIMENTAL DESIGN; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HEAT STRESS; HIGH TEMPERATURE; HOST CELL; LOW TEMPERATURE; MOLECULAR DYNAMICS; NONHUMAN; SARCOPHYTON EHRENBERGI; SENSITIVITY ANALYSIS; SINULARIA LOCHMODES; SPECIES DIFFERENCE; SURVIVAL RATE; SYMBIONT; TAXONOMIC RANK; TEMPERATURE ACCLIMATIZATION; TEMPERATURE SENSITIVITY; TRANSMISSION ELECTRON MICROSCOPY; WATER TEMPERATURE; XENIA ELONGATA; ZOOXANTHELLATE; ANIMAL; ANTHOZOA; AUSTRALIA; HEAT; NECROSIS; PATHOPHYSIOLOGY; PHYSIOLOGY; SYMBIOSIS; TEMPERATURE;

ANIMALS; ANTHOZOA; APOPTOSIS; AUSTRALIA; HOT TEMPERATURE; NECROSIS; SEAWATER; SYMBIOSIS; TEMPERATURE;

EID: 84873538558     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054989     Document Type: Article

References (143)

1. Freudenthal HD, (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a Zooxanthella: taxonomy, life cycles and morphology. J Protozool 9: 45-52.
2. Fitt WK, Trench RK, (1983) The relations of diel patterns of cell division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture. New Phytol 94: 421-432.
3. Wijgerde T (2012) How coral reefs grow. Available: http://www.coralscience.org/main/articles/biochemistry-2/how-reefs-grow. Accessed: 04 April 2012.
4. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW, (1984) Light and the bioenergetics of a symbiotic coral. Biosci 34: 705-709.
5. Muscatine L, Porter JW, (1977) Reef corals: Mutualistic symbioses adapted to nutrient-poor environments. Biosci 27: 454-460.
6. Rodrigues LJ, Grottoli AG, (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52: 1874-1882.
7. Yonge CM, (1930a) Studies on the physiology of corals. I. Feeding mechanisms and food. Sci Rep Great Barrier Reef Exped 1: 13-57.
8. Yonge CM, (1930b) Studies on the physiology of corals. II. Assimilation and excretion. Sci Rep Great Barrier Reef Exped 1: 83-91.
9. Yonge CM, Nicholls AG, (1930) Studies on the physiology of corals. II. Digestive enzymes, with notes on the speed of digestion. Sci Rep Gr Barrier Reef Exped. 1: 59-81.
10. Yonge CM, Nicholls AG, (1931) Studies on the physiology of corals. IV. The structure, distribution and physiology of the zooxanthellae. Sci Rep Great Barrier Reef Exped 1: 135-176.
11. Goreau TF, Goreau NI, Yonge CM, (1971) Reef corals: autotrophs or heterotorphs? Biol Bull 141: 247-260.
12. Freudenthal T, (1969) Stratigraphy of Neogene deposits in the Khania province, Crete, with special reference to foraminifera of the family Planorbulinidae and the genus Heterostegina, Utrecht Micropal Bull. 1: 1-208.
13. Muscatine L, Tambutte E, Allemand D, (1997) Morphology of coral desmocytes, cells that anchor the calicoblastic epithelium to the skeleton. Coral Reefs 16: 205-213.
14. Al-Horani FA, Al-Moghrabi SM, de Beer D, (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142: 419-426.
15. Karako S, Stambler N, Dubinsky Z (2004) The taxonomy and evolution of the zooxanthellae-coral symbiosis. In: Seckbach J, editor, Cellular origin, life in extreme habitats, and astrobiology, Vol. 4, VIII, 539-557. DOI: 10.1007/0-306-48173-1-34.
16. Miao W, Simpson AGB, Fu C, Lobban CS, (2005) The giant zooxanthellae-bearing ciliate Maristentor dinoferus (Heterotrichea) is closely related to Folliculinidae. G. Eukaryot Microbiol 52: 11-16 DOI:10.1111/j.1550-7408.2005.3311r.x.
17. Jeffrey SW, Haxo FT, (1968) Photosynthetic pigments of symbiotic dinoflagellates (zooxanthellae) from corals and clams. Biol Bull 135: 149-165.
18. Fitt WK, Trench RK, (1981) Spawning, development, and acquisition of zooxanthellae by Tridacna squamosa (Mollusca, Bivalvia). Biol Bull 161: 213-235.
19. Fitt WK, Trench RK, (1983) Endocytosis of the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal by endodermal cells of the scyphistomae of Cassiopeia xamachana and resistance of the algae to host digestion. J Cell Sci 64: 195-212.
20. Thornhill DJ, Daniel MW, Lajeunesse TC, Schmidt GW, Fitt WK, (2006) Natural infections of apopsymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. J Exp Mar Biol Ecol 338: 50-56.
21. Droop MR (1963) Algae and invertebrates in symbiosis. In: Nutman, PS, editor, Symbiotic associations, 13th Symp, Soc. for Gen. Microbiology, Cambridge Univ Press, London, 171-199.
22. Davy SK, Turner JR, (2003) Early development and acquisition of zooxanthellae in the temperate symbiotic sea anemone Anthopleura ballii (Cocks). Biol Bull 205: 66-72.
23. Berner T, Achituv Y, Dubinsky Z, Benayahu Y, (1987) Pattern of distribution and adaptation to different irradiance levels of zooxanthellae in the soft coral Litophyton arboretum (Octocorallia, Alcyonacea). Symbiosis 3: 23-40.
24. Michalek-Wagner K, Willis BL, (2001) Impacts of bleaching on the soft coral Lobophytum compactum. I. Fecundity, fertilization, and offspring viability. Coral Reefs 19: 231-239.
25. Strychar KB, Coates MC, Scott PW, Piva TJ, Sammarco PW, (2005) Loss of symbiotic dinoflagellates (Symbiodinium; zooxanthellae) from bleached soft corals Sarcophyton, Sinularia, and Xenia. J Exp Mar Biol Ecol 320: 159-177.
26. Achituv Y, Dubinsky Z, (1990) Evolution and zoogeography of coral reefs. Ecosystems of the world, Vol 25: 1-8.
27. Ginsburg RN (2006) Coral reef background. Available: http://www.agrra.org/background/coralback1.html. Accessed: 01 April 2012.
28. Wells S, Hanna N (1992) Greenpeace book of coral reefs. Sterling Publishing Company. ISBN 0806987952.
29. Muscatine L, Grossman D, Doino J, (1991) Release of symbiotic algae by tropical sea anemones and corals after cold shock. Mar Ecol Prog Ser 77: 233-243.
30. Glynn PW, D'Croz L, (1990) Experimental evidence for high temperature stress as the cause of El-Niño-coincident coral mortality. Coral Reefs 8: 181-190.
31. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W, (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: Field evidence of acclimatization. Proc R Soc B 275: 1359-1365.
32. Wooldridge SA, (2010) Is the coral-algae symbiosis really 'mutually beneficial' for the partners? Bioessays 32: 615-625.
33. Romano SL, Palumbi SR, (1996) Evolution of scleractinian corals inferred from molecular systematic. Science 271: 640-642 DOI:10.1126/science.271.5249.640.
34. Stanley GD, van de Schootbrugge B, (2009) The evolution of the coral-algal symbiosis. Ecol Studies 205: 7-19 DOI:10.1007/978-3-540-69775-6-2.
35. Stanley GD, Swart PK, (1995) Evolution of the coral-zooxanthellate symbiosis during the Jurassic: A geochemical approach. Palaeobiol 21: 179-199.
36. Gould SJ, Vrba ES, (1982) Exaptation: A missing term in the science of form. Paleobiol 8: 4-15.
37. Futuyma DJ (1998) Evolutionary Biology. Sinauer Publ, Sunderland, Massachusetts.
38. McLennan DA, (2008) The concept of co-option: Why evolution often looks miraculous. Evol Edu Outreach 1: 247-258.
39. Brown BE, Howard LS, (1985) Assessing the effects of stress on reef corals. Adv Mar Biol 22: 1-55.
40. Fang LS, Huang SP, Lin KL, (1997) High temperature induces the synthesis of heat-shock proteins and the elevation of intracellular calcium in the coral Acropora grandis. Coral Reefs 16: 127-131.
41. Salm RV, Coles SL (2001) Coral bleaching and marine protected areas. Proc. Workshop on mitigating coral bleaching impact through MPA design, Bishop Museum, Honolulu, Hawaii, 29-31 May 2001. Asia Pacific Coastal Marine Program Report #0102, The Nature Conservancy, Honolulu, Hawaii, U.S.A. 118 p.
42. Strychar KB, Sammarco PW, (2009) Exaptation in corals to high seawater temperatures: Low concentrations of apoptotic and necrotic cells in host coral tissue under bleaching conditions. J Exp Mar Biol Ecol 369: 31-42.
43. Hill R, Ulstrup KE, Ralph PJ, (2009) Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated, and expelled zooxanthellae from scleractinian corals. Bull Mar Sci 85: 223-244.
44. Strychar KB, Sammarco PW, (2012) Effects of heat stress on phytopigments of zooxanthellae (Symbiodinium spp.) symbiotic with the corals Acropora hyacinthus, Porites solida, and Favites complanata. Int J Biol 4: 3-19.
45. Roth MS, Goericke R, Deheyn DD, (2012) Cold induces acute stress but heat is ultimately more deleterious for the reef building coral Acropora yongei. Sci Rep 2: 1-5.
46. Strychar KB, Coates MC, Sammarco PW, (2004a) Loss of Symbiodinium from bleached scleractinian corals: Acropora hyacinthus, Favites complanata and Porites solida. J Mar. Freshwat Res 55: 135-144.
47. Strychar KB, Coates MC, Sammarco PW, Piva TJ, (2004b) Apoptotic and necrotic stages of cell death activity: Bleaching of soft and scleractinian corals. Phycologia 43: 768-777.
48. Strychar KB, Coates MC, Sammarco PW, Piva TJ, (2004c) Bleaching as a pathogenic response in scleractinian corals, evidenced by high concentrations of apoptotic and necrotic zooxanthellae. J. Exp. Mar. Biol. Ecol. 304: 99-121.
49. Strychar KB, Sammarco PW (2010) Zooxanthellate vs. azooxanthellate corals: Insights into susceptibility to disease and efficacy of immune systems. Conf Int Soc Envtl Indicators, Univ Sci and Technol, Hefei, Anhui Province, China, 2010. Abstract.
50. Sammarco PW, Strychar KB, (2009) Effects of climate change/global warming on coral reefs: Exaptation in corals, evolution in zooxanthellae, and biogeographic shifts. Environ Bioind 4: 9-45.
51. Ameisen JC, (2002) On the origin, evolution, and nature of programmed cell death: A timeline of four billion years. Cell Death Differ 9: 367-5467.
52. Bras M, Queenan B, Susin SA, (2005) Programmed cell death via mitochondria: Different modes of dying. Biochem (Mosc) 70: 231-239.
53. Fink SL, Cookson BT, (2005) Apoptosis, pyroptosis, and necrosis: Mechanistic description of dead and dying eukaryotic cells. Infect Immun 73: 1907-1916.
54. Kerr JF, Wyllie AH, Currie AR, (1972) Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-57.
55. Vogt C (1842) Untersuchungen uber die Entwicklungsgeschichte der Geburtshelferkroete (Alytes obstetricians). Jent, Gassman, Solothurn, Switzerland.
56. Seipp S, Schmich J, Leitz T, (2001) Apoptosis - A death-inducing mechanism tightly linked with morphogenesis in Hydractina echinata (Cnidaria, Hydrozoa). Dev 128: 4891-4898.
57. Strychar KB (2002) Bleaching in soft and scleractinian corals: comparison of the physiology, genetics, and biochemistry of Symbiodinium. PhD. Thesis, Central Queensland University, Rockhampton, Australia. 294 pp.
58. Weiss IM, Tuross N, Addadi L, Weiner S, (2002) Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite. J Exp Zool 293: 478-491.
59. Dunn SR, Schnitzler CE, Weis VM, (2007) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: Every which way you lose. Proc Roy Soc B 274: 3079-3085 doi:10.1098/rspb.2007.0711.
60. Ralph PJ, Larkum AWD, Kuhl M, (2005) Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching. J Exp Mar Biol 316: 17-28.
61. Wakefield TS, Farmer MA, Kempf SC, (2000) Revised description of the fine structure of in situ zooxanthellae genus Symbiodinium. Biol Bull 199: 76-84.
62. Stambler N (2011) Zooxanthellae: The yellow symbionts inside animals. In: Dubinsky Z, Stambler N (eds) Coral Reefs: an ecosystem in transition. 87-106.
63. Stambler N (2010) Coral symbiosis under stress. In: Seckbach J, Grube M, editors, Symbioses and stress: joint ventures in biology, cellular origin, life in extreme habitats and astrobiology, 197-224.
64. Richter M, Ruhle W, Wild A, (1990) Studies on the mechanism of photosystem II photoinhibition II. The involvement of toxic oxygen species. Photosyn Res 24: 237-243.
65. Macpherson AN, Telfer A, Barber J, Truscott TG, (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centers. Biochem Biophys Acta 1143: 301-309.
66. Lupi{dotless}nkova L, Komenda J, (2004) Oxidative modifications of the photosystem II D1 protein by reactive oxygen species: from isolated protein to cyanobacterial cells. Photochem Photobiol 79: 152-162.
67. Lesser MP, (1996) Exposure of symbiotic dinoflagellates to elevated temperatures and ultraviolet radiation causes oxidative stress and inhibits photosynthesis. Limnol Oceanogr 41: 271-283.
68. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16: 187-192.
69. (2011) Coral bleaching: causes and mechanisms. In: Dubinsky Z, Stambler N, editors, Coral reefs: An ecosystem in transition. Springer. 405-419.
70. Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ, editors, Photoinhibition. Elsevier, Amsterdam, 228-287.
71. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U, (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21: 1219-1230.
72. Nishiyama Y, H Yamamoto, S I Allakhverdiev, M Inaba, A Yokota, et al. (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. Eur Mol Biol Organ (EMBO) 20: 5587-5594.
73. Takahashi S, Nakamura T, Sakamizu M, van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45, 251-255 DOI: 10.1093/pcp/pch028.
74. Hoogenboom MO, Campbell DA, Beraud E, DeZeeuw K, Ferrier-Pagès C, (2012) Effects of light, food availability and temperature stress on the function of photosystem II and phytosystem I of coral symbionts. PLoS one 7: 1-14.
75. Crawley A, Kline DI, Dunn K, Anthony K, Dove S, (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biol 16: 851-863.
76. Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, 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. J. Exp. Mar. Biol. Ecol. 373: 102-110.
77. Tchernov D, Kvitt H, Haramaty L, Bibby TS, Gorbunov MY, et al. (2011) Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc Natl Acad Sci 108: 9905-9909.
78. Baird AH, Bhagooli R, Ralph PJ, Takahashi S, (2009) Coral bleaching: The role of the host. TREE 24: 16-20.
79. Haslun JA, Strychar KB, Buck GW, Sammarco PW, (2011) Coral bleaching susceptibility is decreased following short-term (1-3 Year) prior temperature exposure and evolutionary history. J Mar Biol. 2011: 1-13.
80. Cervino JM, Hayes R, Goreau TJ, Smith GW, (2004) Zooxanthellae regulation in yellow blotch/band and other coral diseases contrasted with temperature related bleaching: In situ destruction vs expulsion. Symbiosis 37: 63-85.
81. Vivekanandan E, Jayasankar J, (2008) Vulnerability of corals to seawater warming. Indian Council of Agricultural Research 1: 117-122.
82. Harithsa S, Raghukumar C, Dalal SG, (2005) Stress response of two coral species in the Kavaratti Atoll of the Lakshadweep Archipelago, India. Coral Reefs 23: 463-474.
83. Ambariyanto, Hoegh Guldberg O, (1997) The effects of nutrient enrichment on the biomass, growth and calcification of giant clam, Tridacna maxima. Mar Biol 129: 635-642.
84. Geddes P, (1882) Further research on animals containing chlorophyll. Nature, Lond. 25: 303-305.
85. McLaughlin JJA, Zahl PA, (1957) Studies in marine biology. II. In vitro culture of zooxanthellae. Proc Soc Exp Biol Med 95: 115-120.
86. Steele RD, Goreau N, (1977) The breakdown of symbiotic zooxanthellae in the sea anemone Phyllactis (= Oulactis) flosculifera (Actiniara). J Zool Lond 181: 421-437.
87. Titlyanov EA, Titlyanova TV, Leletkin VA, Tsukahara J, van Woesik R, et al. (1996) Degradation of zooxanthellae and regulation of their density in hermatypic corals. Mar Ecol Prog Ser 139: 167-178.
88. Fabricius KE, (1995) Slow population turnover in the soft coral genera Sinularia and Sarcophyton on mid- and outer-shelf reefs of the Great Barrier Reef. Mar Ecol Prog Ser 126: 145-152.
89. Strychar KB, Coates MC, Scott PW, Piva TJ, Sammarco PW, (2005) Loss of symbiotic dinoflagellates (Symbiodinium; zooxanthellae) from bleached soft corals Sarcophyton, Sinularia, and Xenia. J Exp Mar Biol Ecol 320: 159-177.
90. Marshall PA, Baird AH, (2000) Bleaching of corals on the Great Barrier Reef: Differential susceptibilities among taxa. Coral Reefs 19: 155-163.
91. Strychar KB, Coates MC, Sammarco PW, (2005) Loss of Symbiodinium from bleached soft corals Sarcophyton ehrenbergi, Sinularia sp, and Xenia sp. J Exp Mar Biol Ecol 320: 159-177.
92. Gomez E, Mingoa-Lucuanan S, (1998) Mortalities of giant clams associated with unusually high temperatures and coral bleaching. Reef Encounter 24: 19-24.
93. Harvell D, Kim K, Quirolo C, Weir J, Smith G, (2001) Coral bleaching and disease: contributors to 1998 mass mortality in Briareum asbestinum (Octocorallia, Gorgonacea). Hydrobiol 460: 97-104.
94. Hoegh Guldberg O (1994) Mass-bleaching of coral reefs in French Polynesia, April 1994. Climate Impacts Series, Vol. 1. Greenpeace International. 36 p.
95. Obura D, Suleiman M, Motta H, Schleyer M (2000) Status of coral reefs in East Africa: Kenya, Mozambique, South Africa and Tanzania. In: Wilkinson C, editor. Status of Coral Reefs of the World: 2000. Australian Institute of Marine Sciences, Townsville, Australia. 65-76.
96. Smith AH, Archibald M, Bailey T, Bouchon C, Brathwaite A, et al. (2000) Status of coral reefs in South Asia: Bangladesh, India, Maldives and Sri Lanka. In: Wilkinson C, editor. Status of Coral Reefs of the World: 2000. Australian Institute of Marine Science, Townsville, Australia. 315-330.
97. Schleyer MH, Kruger A, Celliers L, (2008) Long-term community changes on a high-latitude coral reef in the Greater St Lucia Wetland Park, South Africa. Mar Poll Bull 56: 493-502 DOI:10.1016/j.marpolbul.2007.11.011.
98. Goulet TL, Simmons C, Goulet D, (2008) Worldwide biogeography of Symbiodinium in tropical octocorals. Mar Ecol Prog Ser 355: 45-58.
99. van Oppen MJH, Mahiny AJ, Done TJ, (2005a) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24: 482-487.
100. LaJeunesse TC, (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141: 387-400.
101. Tchernov D, Gorbunov MV, de Vargas C, Yadav SN, Milligan AJ, et al. (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Nat Acad Sci USA 101: 13531-13535.
102. Abrego D, Ulstrup KE, Willis BL, van Oppen MJH, (2008) Species specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc Lond B 275: 2273-2282.
103. Oliver T, Palumbi SR, (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30: 429-440.
104. Krueger T, Gates RD, (2012) Cultivating endosymbionts - host environmental mimics support the survival of Symbiodinium C15 ex hospite. J Exp Mar Biol Ecol 413: 169-176.
105. Tsubokawa R, Wedeen CJ, (1999) Cell death in late embryogenesis of the leech Helobdella. Dev Genes Evol 209: 515-525 DOI:10.1007/s004270050284.
106. Zhang L, Li L, Zhang G, (2011) Gene discovery, comparative analysis, and expression profile reveal the complexity of the Crassostrea gigas apoptosis system. Dev Comp Immunol 35: 603-610 doi:10.1016/j.dci.2011.01.005.
107. Thurber RV, Epel D, (2007) Apoptosis in early development of the sea urchin, Strongylocentrotus purpuratus. Dev Biol 303: 336-346 DOI:10.1016/j.ydbio.2006.11.018.
108. Terahara K, Takahashi KG, (2008) Mechanisms and immunological roles of apoptosis in molluscs. Curr. Pharmaceut. Design 14: 131-137.
109. Xue D, Horvitz HR, (1995) Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377: 248-251.
110. Huang Z, Banton MC, Tunnacliffe A, (2010) Modeling anhydrobiosis: Activation of the mitogen-activated protein kinase ERK by dehydration in both human cells and nematodes. J Exp Zool 313A: 660-670.
111. Wiens M, Müller WEG, (2006) Cell death in Porifera: Molecular players in the game of apoptotic cell death in living fossils. Can J Zool 84: 307-321.
112. Kevin MK, Hall WT, Mclaughlin JJA, Zahl PA, (1969) Symbiodinium microadriaticum Freudenthal: A revised taxonomic description, ultrastructure. J Phycol 5: 341-350.
113. Pardy RL, (1974) Some factors affecting the growth and distribution of the algal endosymbioants of Hydra viridis. Mar Biol Bull 147: 105-118.
114. Drew EA, (1972) The biology and physiology of algae-invertebrate symbiosis II. The density of symbiotic algal cells in a number of hermatypic hard corals and alcyonarians from various depths. J Exp Mar Biol Ecol 9: 71-75.
115. Trench RK (1987) Dinoflagellates in non-parisitic symbiosis. In: The Biology of Dinoflagellates. Taylor FJR, editor, Blackwell, Oxford, 530-570.
116. Muscatine L Mclosky LR, Manan RE, (1981) Estimating the daily contribution of carbon from zooxanthellae to animal respiration. Limnol Oceanogr 26: 601-611.
117. Muscatine L, Falkowski PG, Dubinsky Z, Cook P A, McCloskey LR, (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc R Soc Lond B 236: 311-324.
118. Taylor CEL, Muscatine L, Jefferson DR, (1989) Maintenance and breakdown of the Hydra-Chlorella symbiosis: a computer model. Proc R Soc Lond B 238: 277-289.
119. Sammarco PW, La Barre SC, Coll JC, (1987) Defensive strategies of soft corals (Coelenterata:Octocorallia) of the Great Barrier Reef. III. The relationship between toxicity and morphology. Oecologia 74: 93-101.
120. Hochberg E J, Apprill AM, Atkinson MJ, Bidigare RR, (2006) Bio-optical modeling of photosynthetic pigments in corals. Coral Reefs 25: 99-109.
121. Oswald F, Schmitt F, Leutenegger A, Ivanchenko S, DAngelo C, et al. (2007) Contributions of host and symbiont pigments to the coloration of reef corals. FEBS J. 274: 1102-1109.
122. Muscatine L, McNeil PL, (1989) Endosymbiosis in Hydra and the evolution of internal defense systems. Am Zool 29: 371-386.
123. Hill M, Hill A (2012) The magnesium inhibition and arrested phagosome hypotheses: new perspectives on the evolution and ecology of Symbiodinium symbioses. Biol Rev (in press).
124. Goreau TF, Goreau NI, Goreau TJ, (1979) Corals and coral reefs. Sci Am 241: 110-120.
125. Perez SF, Cook CB, Brooks WR, (2001) The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. J Exp Mar Biol Ecol 256: 1-14.
126. Welsh MF, (1936) Oxygen production by zooxanthellae in a Bermudan turbellarian. Biol Bull 70: 282.
127. Buck B, Rosenthal, Saint-Paul U, (2002) Effect of increased irradiance and thermal stress on the symbiosis of Symbiodinium microadriaticum and Tridacna gigas. Aquat Liv Res 15: 107-117 DOI:10.1016/S0990-7440(02)01159-2.
128. Rowan R, (2004) Coral bleaching- thermal adaptation in reef coral symbionts. Nature 430: 742-742.
129. 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. Proc R Soc Biol Sci Ser B 273: 2305-2312.
130. Fabricius KE, Mieog JC, Colin PL, Idip D, VanOpen MJH, (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13: 2445-58.
131. Sokal RR, Rohlf FJ (1981) Biometry. The principles and practice of statistics in biological research. WH Freeman and Co, San Francisco, USA.
132. Reynolds RW, Smith TM, (1994) Improved global sea surface temperature analyses. J Climate 7: 929-948.
133. Rajasuriya A, Zahir H, Muley EV, Subramanian BR, Venkataraman K, et al. (2000) Status of coral reefs in South Asia: Bangladesh, India, Maldives and Sri Lanka. In: Wilkinson C, editor. Status of Coral Reefs of the World: 2000. Australian Institute of Marine Science, Townsville, Australia. 95-115.
134. Wilkinson C (2000) The 1997-98 mass coral bleaching and mortality event: 2 years on. In: Wilkinson C, editor. Status of Coral Reefs of the World: 2000. Australian Institute of Marine Science, Townsville, Australia. 21-34.
135. Podesta GP, Glynn PW, (1997) Sea surface temperature variability in Panamá and Galápagos: Extreme temperatures causing coral bleaching. J Geophys Res 102: 15749-15759.
136. Sandeman IM, (2006) Fragmentation of the gastrodermis and detachment of zooxanthellae in symbiotic cnidarians: a role for hydrogen peroxide and Ca2+ in coral bleaching and algal density control. Rev Biol Trop 54: 79-96.
137. Hoegh Guldberg O, (1999) Climate change, coral bleaching and the future of the world's coral reefs. J Mar Freshw Res 50: 839-866.
138. Goreau T, McClanahan T, Hayes R, Strong A, (2000) Conservation of coral reefs after the 1998 global bleaching event. Conserv Biol 14: 5-16.
139. Sotka EE, Thacker RW, (2004) Do some corals like it hot? TRENDS Ecol Evol 20: 59-62.
140. Riegl B, (2003) Climate change and coral reefs: different effects in two high-latitude areas (Arabian Gulf, South Africa). Coral Reefs 22: 433-446.
141. Suharsono RK, Brown BE, (1992) Comparative measurements of mitotic index in zooxanthellae from a symbiotic cnidarian subject to temperature increase. J Exp Mar Biol Ecol 158: 179-188.
142. Rinkevich B, Loya Y, (1979) The reproduction of the Red Sea coral Stylophora pistillata. I. Gonads and planulae. Mar Ecol Prog Ser 1: 133-144.
143. Banin E, Israely T, Kushmaro A, Loya Y, Orr E, et al. (2000) Penetration of the coral-bleaching bacterium Vibrio shiloi into Oculina patagonica. Appl Environ Microbiol 66: 3031-3036.