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Life History and Stress Response of Scleractinian Corals

  • Michio HidakaEmail author
Chapter
Part of the Coral Reefs of the World book series (CORW, volume 5)

Abstract

Symbiosis with zooxanthellae (symbiotic dinoflagellates) and high capacities for clonal reproduction and regeneration are important life history traits of reef-building corals. This chapter reviews the life history of reef-building corals and the symbiotic relationships between corals and their algal symbionts and discusses possible collaborative defense systems against environmental stresses as well as mechanisms of adaptation to environmental changes in coral–zooxanthella symbiotic systems. Most corals associate with one main type of symbiont, although minor or cryptic symbiont types are often detected within a colony. The association between the coral host and algal symbiont appears to be stable, and the original symbiont often returns when corals recover from bleaching. Some corals, such as the massive Porites, exhibit high fidelity to certain types of algal symbionts and still have high stress tolerance as well as long life spans suggesting the possibility that stem cells and algal symbiont cells in such long-lived colonies accumulate mutations; in turn, if cells with a higher fitness for a new environment proliferate within a colony, the colony may be able to adapt to the new environment.

Keywords

Life history Planula Symbiosis Stress response Zooxanthella 

References

  1. Abrego D, van Oppen MJH, Willis BL (2009a) Highly infectious symbiont dominates initial uptake in coral juveniles. Mol Ecol 18:3518–3531CrossRefGoogle Scholar
  2. Abrego D, van Oppen MJH, Willis BL (2009b) Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Mol Ecol 18:3532–3543CrossRefGoogle Scholar
  3. Adams LM, Cumbo VR, Takabayashi M (2009) Exposure to sediment enhances primary acquisition of Symbiodinium by asymbiotic coral larvae. Mar Ecol Prog Ser 377:149–156CrossRefGoogle Scholar
  4. Ahsan MK, Nakamura H, Yodoi J (2010) Redox regulation by thioredoxin in cardiovascular diseases. In: Das DK (ed) Methods in redox signaling. Mary Ann Liebert, New York, pp 159–165Google Scholar
  5. Ainsworth TD, Hoegh-Guldberg O, Heron SF, Skirving WJ, Leggat W (2008) Early cellular changes are indicators of pre-bleaching thermal stress in the coral host. J Exp Mar Biol Ecol 364:63–71CrossRefGoogle Scholar
  6. Ainsworth TD, Wasmund K, Ukani L, Seneca F, Yellowees D, Miller D, Leggat W (2011) Defining the tipping point. A complex cellular life/death balance in corals in response to stress. Sci Rep 1:160. doi: 10.1038/srep00160 Google Scholar
  7. Apprill AM, Gates RD (2007) Recognizing diversity in coral symbiotic dinoflagellate communities. Mol Ecol 16:1127–1134CrossRefGoogle Scholar
  8. Ayre DJ, Resing JM (1986) Sexual and asexual production of planulae in reef corals. Mar Biol 90:187–190CrossRefGoogle Scholar
  9. Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116CrossRefGoogle Scholar
  10. Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20CrossRefGoogle Scholar
  11. Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766CrossRefGoogle Scholar
  12. Baker AC, Starger CJ, McClanahan T, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 430:741CrossRefGoogle Scholar
  13. Balskus EP, Walsh CT (2010) The genetic and molecular basis for sunscreen biosynthesis in cyanobacteria. Science 329:1653–1656CrossRefGoogle Scholar
  14. Bertucci A, Tambutté E, Tambutté S, Aallemand D, Zoccola D (2010) Symbiosis-dependent gene expression in coral-dinoflagellate association: cloning and characterization of a P-type H+-ATPase gene. Proc R Soc B 277:87–95CrossRefGoogle Scholar
  15. Bhagooli R, Hidaka M (2003) Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species. J Exp Mar Biol Ecol 291:181–197CrossRefGoogle Scholar
  16. Bhagooli R, Hidaka M (2004a) Release of zooxanthellae with intact photosynthetic activity by the coral Galaxea fascicularis in response to high temperature stress. Mar Biol 145:329–337CrossRefGoogle Scholar
  17. Bhagooli R, Hidaka M (2004b) Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis Stylophora pistillata, in response to thermal and light stresse. Comp Biochem Physiol Part A 137:547–555Google Scholar
  18. Bouchard JN, Yamasaki H (2008) Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: a possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol 49:641–652CrossRefGoogle Scholar
  19. Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim Biophys Acta 1760:1690–1695CrossRefGoogle Scholar
  20. Brown BE, LeTissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Mar Biol 122:655–663CrossRefGoogle Scholar
  21. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. BioScience 43:320–326CrossRefGoogle Scholar
  22. Byler KA, Carmi-Veal M, Fine M, Goulet TL (2013) Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. PLoS One 8(3):e59596CrossRefGoogle Scholar
  23. Coffroth MA, Poland DM, Petrou EL, Brazeau DA, Holmberg JC (2010) Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLoS One 5(10):e13258CrossRefGoogle Scholar
  24. Correa AMS, Baker AC (2009) Understanding diversity in coral-algal symbiosis: a cluster-based approach to interpreting fine-scale genetic variation in the genus Symbiodinium. Coral Reefs 28:81–93CrossRefGoogle Scholar
  25. Correa AMS, Baker AC (2011) Disaster taxa in microbially mediated metazoans: how endosymbionts and environmental catastrophes influence the adaptive capacity of reef corals. Glob Chang Biol 17:68–75CrossRefGoogle Scholar
  26. Correa AMS, McDonald MD, Baker AC (2009) Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detect clade D symbionts in Caribbean corals. Mar Biol 156:2403–2411CrossRefGoogle Scholar
  27. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261CrossRefGoogle Scholar
  28. Desalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, Szmant AM, Medina M (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17:3952–3971CrossRefGoogle Scholar
  29. Domart-Coulon I, Tambutté S, Tambutté E, Allemand D (2004) Short term viability of soft tissue detached from the skeleton of reef-building corals. J Exp Mar Biol Ecol 309:199–217CrossRefGoogle Scholar
  30. Downs CA, Fauth JE, Downs VD, Ostrander GK (2010) In vivo cell-toxicity screening as an alternative animal model for coral toxicology: effects of heat stress, sulfide, rotenone, cyanide, and cuprous oxide on cell viability and mitochondrial function. Ecotoxicology 19:171–184CrossRefGoogle Scholar
  31. Dunn SR, Bythell JC, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272:29–53CrossRefGoogle Scholar
  32. 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 R Soc B 274:3079–3085CrossRefGoogle Scholar
  33. Fautin DG, Mariscal RN (1991) Cnidaria: anthozoa. In: Microscopic anatomy of invertebrates, vol 2, Placozoa, Porifera, Cnidaria, and Ctenophora. Wiley-Liss, New York, pp 267–358Google Scholar
  34. Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Prog Ser 272:117–130CrossRefGoogle Scholar
  35. Geller JB, Fitzgerald LJ, King CE (2005) Fission in sea anemones: integrative studies of life cycle evolution. Integr Comp Biol 45:615–622CrossRefGoogle Scholar
  36. Gold DA, Jacobs DK (2013) Stem cell dynamics in Cnidaria: are there unifying principles? Dev Genes Evol 223:53–66CrossRefGoogle Scholar
  37. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189CrossRefGoogle Scholar
  38. Hansen G, Daugbjerg N (2009) Symbiodinium natans sp. nov.: a ‘free-living’ dinoflagellate from Tenerife (Northeast-Atlantic Ocean). J Phycol 45:251–263CrossRefGoogle Scholar
  39. Harii S, Yasuda N, Lodoriguez-Lanetty IT, Hidaka M (2009) Onset of symbiosis and distribution patterns of symbiotic dinoflagellates in the larvae of scleractinian corals. Mar Biol 156:1203–1212CrossRefGoogle Scholar
  40. Harii S, Yamamoto M, Hoegh-Guldberg O (2010) The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Mar Biol 157:1215–1224CrossRefGoogle Scholar
  41. Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 59–85CrossRefGoogle Scholar
  42. Haryanti D, Hidaka M (2015) Temperature dependence of respiration in larvae and adult colonies of the corals Acropora tenuis Pocillopora damicornis. J Mar Sci Eng 3:509–519. doi: 10.3390/jmse3030509 CrossRefGoogle Scholar
  43. Haryanti D, Hidaka M (submitted) Developmental changes in the fluorescence intensity and distribution pattern of green fluorescent protein (GFP) in coral larvae and juveniles. SubmittedGoogle Scholar
  44. Haryanti D, Yasuda N, Harii S, Hidaka M (2015) High tolerance of symbiotic larvae of Pocillopora damicornis to thermal stress. Zool Stud 54:52. doi: 10.1186/s40555-015-0134-7 CrossRefGoogle Scholar
  45. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226CrossRefGoogle Scholar
  46. Hill M, Hill A (2012) The magnesium inhibition and arrested phagosome hypotheses: new perspectives on the evolution and ecology of Symbiodinium symbioses. Biol Rev 87:804–821CrossRefGoogle Scholar
  47. Hill R, Ralph PJ (2007) Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis. Mar Ecol Prog Ser 352:137–144CrossRefGoogle Scholar
  48. Hirose M, Hidaka M (2006) Early development of zooxanthella-containing eggs of the corals Porites cylindrica and Montipora digitata: the endodermal localization of zooxanthellae. Zool Sci 23:873–881CrossRefGoogle Scholar
  49. Hirose M, Kinzie RA III, Hidaka M (2001) Timing and process of entry of zooxanthellae into oocytes of hermatypic corals. Coral Reefs 20:273–280CrossRefGoogle Scholar
  50. Hirose M, Yamamoto H, Nonaka M (2008a) Metamorphosis and acquisition of symbiotic algae in planula larvae and primary polyps of Acropora spp. Coral Reefs 27:247–254Google Scholar
  51. Hirose M, Reimer JD, Hidaka M, Suda S (2008b) Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa, Japan. Mar Biol 155:105–112CrossRefGoogle Scholar
  52. Hoadley KD, Szmant AM, Pyott SJ (2011) Circadian clock gene expression in the coral Favia fragum over diel and lunar reproductive cycles. PLoS One 6:e19755CrossRefGoogle Scholar
  53. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120CrossRefGoogle Scholar
  54. Huang H-J, Wang L-H, Chen W-NU, Fang L-S, Chen C-S (2008) Developmentally regulated localization of endosymbiotic dinoflagellates in different tissue layers of coral larvae. Coral Reefs 27:365–372CrossRefGoogle Scholar
  55. Huertas IE, Rouco M, López-Rodas V, Costas E (2011) Warming will affect phytoplankton differently: evidence through a mechanistic approach. Proc R Soc B 278:3534–3543CrossRefGoogle Scholar
  56. Hughes TP, Jackson JBC (1985) Population dynamics and life histories of foliaceous coral. Ecol Monogr 55:141–166CrossRefGoogle Scholar
  57. Jokiel PL, Bigger CH (1994) Aspects of histocompatibility and regeneration in the solitary reef coral Fungia scutaria. Biol Bull 186:72–80CrossRefGoogle Scholar
  58. Jones RJ, Hoegh-Gulberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230CrossRefGoogle Scholar
  59. Kerr AM, Baird AH, Hughes TP (2011) Correlated evolution of sex and reproductive mode in corals (Anthozoa: Scleractinia). Proc R Soc B 278:75–81CrossRefGoogle Scholar
  60. Kinzie RA III, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: experimental tests of critical assumptions. Biol Bull 200:51–58CrossRefGoogle Scholar
  61. Kojis BL (1986) Sexual reproduction in Acropora (Isopora) (Coelenterata: Scleractinia) I. A. cuneata and A. palifera on Heron Island reef, Great Barrier Reef. Mar Biol 91:291–309CrossRefGoogle Scholar
  62. Kopecky EJ, Ostrander GK (1999) Isolation and primary culture of viable multicellular endothelial isolates from hard corals. In Vitro Cell Dev Biol-Anim 35:616–624CrossRefGoogle Scholar
  63. Kramarsky-Winter E, Loya Y (1996) Regeneration versus budding in fungiid corals: a trade-off. Mar Ecol Prog Ser 134:179–185CrossRefGoogle Scholar
  64. LaJeunesse TC (2004) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581CrossRefGoogle Scholar
  65. LaJeunesse TC, Thornhill DJ (2011) Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS One 6(12):e29013CrossRefGoogle Scholar
  66. LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Shifts in relative dominance between closely related Symbiodinium spp. in coral reef host communities over environmental, latitudinal, and biogeographic gradients. Mar Ecol Prog Ser 284:147–161CrossRefGoogle Scholar
  67. LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magaña AL, Pérez AL, Reyes-Bonilla H, Warner ME (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellates symbiosis to environmental disturbance. Proc R Soc B 277:2925–2934CrossRefGoogle Scholar
  68. Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 405–419CrossRefGoogle Scholar
  69. Levy O, Appelbaum L, Leggat W, Gothlif Y, Hayward DC, Miller DJ, Hoegh-Guldberg O (2007) Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science 318:467–480CrossRefGoogle Scholar
  70. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494CrossRefGoogle Scholar
  71. Lough JM, Barnes DJ (1997) Several centuries of variation in skeletal extension, density and calcification in massive Porites colonies from the Great Barrier Reef: a proxy for seawater temperature and a background of variability against which to identify unnatural change. J Exp Mar Biol Ecol 211:29–67CrossRefGoogle Scholar
  72. Manning MM, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53:1853–1861CrossRefGoogle Scholar
  73. Marlow HQ, Martindale MQ (2007) Embryonic development in two species of scleractinian coral embryos: Symbiodinium localization and mode of gastrulation. Evol Dev 9:355–367CrossRefGoogle Scholar
  74. McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, Warner ME (2012) Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar Ecol Prog Ser 462:1–7CrossRefGoogle Scholar
  75. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D, Colbourne JK, Willis BL, Matz MV (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genomics 10:219CrossRefGoogle Scholar
  76. Mieog JC, van Oppen MJH, Cantin NE, Stam WT, Olsen JL (2007) Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian coral across the Great Barrier Reef: implication for symbiont shuffling. Coral Reefs 26:449–457CrossRefGoogle Scholar
  77. Mieog JC, van Oppen MJH, Berkelmans R, Stam WT, Olsen JL (2009) Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol Ecol Resour 9:74–82CrossRefGoogle Scholar
  78. Miller SW, Hayward DC, Bunch TA, Miller DJ, Ball EE, Bardwell VJ, Zarkower D, Brower DL (2003) A DM domain protein from a coral, Acropora millepora, homologous to proteins important for sex determination. Evol Dev 5:251–258CrossRefGoogle Scholar
  79. Miller DJ, Ball EE, Technau U (2005) Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet 21:536–539CrossRefGoogle Scholar
  80. Mise T, Hidaka M (2003) Degradation of zooxanthellae in the coral Acropora nasuta during bleaching. Galaxea, JCRS 5:32–38Google Scholar
  81. Nakaema S, Hidaka M (2015a) Fluorescent protein content and stress tolerance of two color morphs of the coral Galaxea fascicularis. Galaxea J Coral Reef Stud 17:1–11Google Scholar
  82. Nakaema S, Hidaka M (2015b) GFP distribution and fluorescence intensity in Galaxea fascicularis: developmental changes and maternal effects. Platax 12:19–27Google Scholar
  83. Nesa B, Hidaka M (2009a) High zooxanthella density shortens the survival time of coral cell aggregates under thermal stress. J Exp Mar Biol Ecol 368:81–87Google Scholar
  84. Nesa B, Hidaka M (2009b) Thermal stress increases oxidative DNA damage in coral cell aggregates. In: Proceedings of 11th international coral reef symposium (Florida), pp 144–148Google Scholar
  85. Nesa B, Baird AH, Harii S, Yakovleva I, Hidaka M (2012) Algal symbionts increase DNA damage in coral planulae exposed to sunlight. Zool Stud 51:12–17Google Scholar
  86. Nilsson Sköld H, Obst M (2011) Potential for clonal animals in longevity and ageing studies. Biogerontology 12:387–396CrossRefGoogle Scholar
  87. Oguchi R, Terashima I, Kou J, Chow WS (2011) Operation of dual mechanisms that both lead to photoinactivation of photosystem II in leaves by visible light. Physiol Plant 142:47–55CrossRefGoogle Scholar
  88. Ojimi MC, Loya Y, Hidaka M (2012) Sperm of the solitary coral Ctenactis echinata exhibits a longer telomere than that of somatic tissues. Zool Stud 51:1475–1480Google Scholar
  89. Padilla-Gamiño JL, Pochon X, Bird C, Concepcion GT, Gates RD (2012) From parent to gamete: vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata. PLoS One 7:e38440CrossRefGoogle Scholar
  90. Padilla-Gamiño JL, Bidigare RR, Barshis DJ, Alamaru A, Hédouin L, Hernández-Pech X, Kandel F, Leon Soon S, Roth MS, Rodrigues LJ, Grottoli AG, Portocarrero C, Wagenhauser SA, Buttler F, Gates RD (2013) Are all eggs created equal? A case study from the Hawaiian reef-building coral Montipora capitata. Coral Reefs. doi: 10.1007/s00338-012-0957-1 Google Scholar
  91. Palmer CV, Chintan KM, Laura DM (2009) Coral fluorescent proteins as antioxidants. PLoS One 4:e7298. doi: 10.1371/journal.pone.0007298 CrossRefGoogle Scholar
  92. Perez S, Weis V (2006) Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. J Exp Biol 209:2804–2810CrossRefGoogle Scholar
  93. Permata DW, Hidaka M (2005) Ontogenetic changes in the capacity of the coral Pocillopora damicornis to originate branches. Zool Sci 22:1197–1203CrossRefGoogle Scholar
  94. Permata DW, Kinzie RA III, Hidaka M (2000) Histological studies on the origin of planulae of the coral Pocillopora damicornis. Mar Ecol Prog Ser 200:191–200CrossRefGoogle Scholar
  95. Pernice M, Dunn SR, Miard T, Dufour S, Dove S, Hoegh-Guldberg O (2011) Regulation of apoptotic mediators reveals dynamic responses to thermal stress in the reef building coral Acropora millepora. PLoS One 6:e16095CrossRefGoogle Scholar
  96. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497CrossRefGoogle Scholar
  97. Pochon X, Stat M, Takabayashi M, Chasqui L, Chauka LJ, Logan DDK, Gates RD (2010) Comparison of endosymbiotic and free-living Symbiodinium (Dinophyceae) diversity in a Hawaiian reef environment. J Phycol 46:53–65CrossRefGoogle Scholar
  98. Pochon X, Putnam HM, Burki F, Gates RD (2012) Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLoS One 7(1):e29816CrossRefGoogle Scholar
  99. Potts DC, Done TJ, Isdale PJ, Fisk DA (1985) Dominance of a coral community by the genus Porites (Scleractinia). Mar Ecol Prog Ser 23:79–84CrossRefGoogle Scholar
  100. Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc Roy Soc B 279:4352–4361CrossRefGoogle Scholar
  101. Ralph PJ, Gademann R, Larkum AWD (2001) Zooxanthellae expelled from bleached corals at 33°C are photosynthetically competent. Mar Ecol Prog Ser 220:163–168CrossRefGoogle Scholar
  102. Ralph PJ, Larkum AWD, Kuhl M (2005) Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching. J Exp Mar Biol Ecol 316:17–28CrossRefGoogle Scholar
  103. Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D, Furla P (2006) Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS J 273:4186–4198CrossRefGoogle Scholar
  104. Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18:5101–5114CrossRefGoogle Scholar
  105. Rosic NN (2012) Phylogenetic analysis of genes involved in mycosporine-like amino acid biosynthesis in symbiotic dinoflagellates. Appl Microbiol Biotechnol 94:29–37CrossRefGoogle Scholar
  106. Roth MS (2014) The engine of the reef: photobiology of the coral-algal symbiosis. Front Microbiol 5:422CrossRefGoogle Scholar
  107. Rowan R (2004) Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430:742CrossRefGoogle Scholar
  108. Rowan R, Powers DA (1991a) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbiosis. Science 251:1348–1351CrossRefGoogle Scholar
  109. Rowan R, Powers DA (1991b) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73CrossRefGoogle Scholar
  110. Salih A, Larkum A, Cox G, Kuhl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853CrossRefGoogle Scholar
  111. Sammarco PW (1982) Polyp bail-out: an escape response to environmental stress and a new means of reproduction in corals. Mar Ecol Prog Ser 10:57–65CrossRefGoogle Scholar
  112. Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci U S A 105:10444–10449CrossRefGoogle Scholar
  113. Sampayo EM, Dove S, LaJeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519CrossRefGoogle Scholar
  114. Santos SR, Coffroth MA (2003) Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium Freudenthal are haploid. Biol Bull 204:10–20CrossRefGoogle Scholar
  115. Saragosti E, Tchernov D, Katsir A, Shaked Y (2010) Extracellular production and degradation of superoxide in the coral Stylophora pistillata and cultured Symbiodinium. PLoS One 5:e12508CrossRefGoogle Scholar
  116. Schwarz JA, Krupp DA, Weis VM (1999) Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biol Bull 196:70–79CrossRefGoogle Scholar
  117. Shikina S, Chen CJ, Liou JY, Shao ZF, Chung YJ, Lee YH, Chang CF (2012) Germ cell development in the scleractinian coral Euphyllia ancora (Cnidaria, Anthozoa). PLoS One 7(7):e41569CrossRefGoogle Scholar
  118. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fujie M, Fujiwara M, Koyanagi R, Ikuta T, Fujiyama A, Miller DJ, Satoh N (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320–324CrossRefGoogle Scholar
  119. Shinzato C, Shoguchi E, Tanaka M, Satoh N (2012) Fluorescent protein candidate genes in the coral Acropora digitifera genome. Zool Sci 29:260–264CrossRefGoogle Scholar
  120. Silverstein RN, Correa AMS, Baker AC (2012) Specificity is rarely absolute in coral-algal symbiosis: implications for coral response to climate change. Proc R Soc B 279:2609–2618CrossRefGoogle Scholar
  121. Smith LD, Hughes TP (1999) An experimental assessment of survival, re-attachment and fecundity of coral fragments. J Exp Mar Biol Ecol 235:147–164CrossRefGoogle Scholar
  122. Smith-Keune C, Dove S (2008) Gene expression of a green fluorescent protein homolog as a host-specific biomarker of heat stress within a reef-building coral. Mar Biotechnol 10:166–180CrossRefGoogle Scholar
  123. Stanley GD Jr (2006) Photosymbiosis and the evolution of modern coral reefs. Science 312:857–858CrossRefGoogle Scholar
  124. Stanley GD, Swart PK (1995) Evolution of the coral-zooxanthellae symbiosis during the Triassic: a geochemical approach. Paleobiology 21:179–199CrossRefGoogle Scholar
  125. Stat M, Loh WKW, LaJeunesse TC, Hoegh-Guldberg O, Carter DA (2009) Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709–713CrossRefGoogle Scholar
  126. Stat M, Bird CE, Pochon X, Chasqui L, Chauka LJ, Concepcion GT, Loga D, Takabayashi M, Toonen RJ, Gates RD (2011) Variation in Symbiodinium ITS2 sequence assemblages among coral colonies. PLoS One 6(1):e15854CrossRefGoogle Scholar
  127. Stoddart JA (1983) Asexual production of planulae in the coral Pocillopora damicornis. Mar Biol 76:279–284CrossRefGoogle Scholar
  128. Strychar KB, Sammarco PW (2008) 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 369:31–42CrossRefGoogle Scholar
  129. Strychar KB, Coates M, Sammarco PW, Piva TJ (2004) Bleaching as a pathogenic response in scleractinian corals, evidenced by high concentrations of apoptotic and necrotic zooxanthellae. J Exp Mar Biol Ecol 304:99–121CrossRefGoogle Scholar
  130. Sunagawa S, Wilson EC, Thaler M, Smith ML, Ccaruso C, Pringle JR, Weis VM, Medina M, Schwarz JA (2009) Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10:258CrossRefGoogle Scholar
  131. Suwa R, Hirose M, Hidaka M (2008) Seasonal fluctuation in zooxanthella composition and photo-physiology in the corals Pavona divaricata and P. decussata in Okinawa. Mar Ecol Prog Ser 361:129–137CrossRefGoogle Scholar
  132. Szmant-Froelich AM, Reutter M, Riggs L (1985) Sexual reproduction of Favia fragum (Esper): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull Mar Sci 37:880–892Google Scholar
  133. Taguchi T, Mezaki T, Iwase F, Sekida S, Kubota S, Fukami H, Okuda K, Shinbo T, Oshima S, Iiguni Y, Testa JR, Tominaga A (2014) Molecular cytogenetic analysis of the scleractinian coral Acropora solitaryensis Veron & Wallace 1984. Zool Sci 31:89–94CrossRefGoogle Scholar
  134. 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 45:251–255CrossRefGoogle Scholar
  135. Takahashi S, Whitney SM, Badger MR (2009) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci U S A 106:3237–3242CrossRefGoogle Scholar
  136. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci U S A 101:13531–13535CrossRefGoogle Scholar
  137. Tchernov D, Kvitt H, Haramaty L, Bibby TS, Gorbunov MY, Rosenfeld H, Falkowsky PG (2011) Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc Natl Acad Sci U S A 108:9905–9909CrossRefGoogle Scholar
  138. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2005) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol. doi: 10.1007/s00227-005-0114-2 Google Scholar
  139. Trench RK, Blank RJ (1987) Symbiodinium microadriaticum Freudenthal, S. goreauii sp. nov., S. kawagutii sp. nov. and S. pilosum sp. nov.: gymnodinioid dinoflagellate symbionts of marine invertebrates. J Phycol 23:469–481CrossRefGoogle Scholar
  140. Tsuta H, Hidaka M (2013) Telomere length of the colonial coral Galaxea fascicularis at different developmental stages. Coral Reefs 32:495–502CrossRefGoogle Scholar
  141. Tsuta H, Shinzato C, Satoh N, Michio Hidaka M (2014) Telomere shortening in the colonial coral Acropora digitifera during Development. Zool Sci 31:129–134CrossRefGoogle Scholar
  142. Twan W-H, Hwang J-S, Lee Y-H, Wu H-F, Tung Y-H, Chang C-F (2006) Hormones and reproduction in scleractinian corals. Comp Biochem Physiol A 144:247–253CrossRefGoogle Scholar
  143. Udy JW, Hinde R, Vesk M (1993) Chromosomes and DNA in Symbiodinium from Australian hosts. J Phycol 29:314–320CrossRefGoogle Scholar
  144. Van Oppen MJH, Gates RD (2007) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883CrossRefGoogle Scholar
  145. Van Oppen MJH, Souter P, Howells EJ, Heyward A, Berkelmans R (2011) Novel genetic diversity through somatic mutations: fuel for adaptation of reef corals? Diversity 3:405–423CrossRefGoogle Scholar
  146. Vizel M, Loya Y, Downs C, Kramarsky-Winter E (2011) A novel method for coral explant culture and micropropagation. Mar Biotechnol 13:423–432CrossRefGoogle Scholar
  147. Voolstra CR, Schwarz JA, Schnetzer J, Sunagawa S, Desalvo MK, Szmant AM, Coffroth MA, Medina M (2009) The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol Ecol 18:1823–1833CrossRefGoogle Scholar
  148. Warner ME, Fitt WK, Schmidt G (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci U S A 96:8007–8012CrossRefGoogle Scholar
  149. Watanabe H, Hoang VT, Mättner R, Holstein TW (2009) Immortality and the base of multicellular life: lessons from cnidarians stem cells. Semin Cell Dev Biol 20:1114–1125CrossRefGoogle Scholar
  150. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066CrossRefGoogle Scholar
  151. Wewengkang DS, Watanabe T, Hidaka M (2007) Studies on morphotypes of the coral Galaxea fascicularis from Okinawa: polyp color, nematocyst shape, and coenosteum density. Galaxea J Coral Reef Stud 9:49–59CrossRefGoogle Scholar
  152. Yakovleva I, Hidaka M (2004) Differential recovery of PSII function and electron transport rate in symbiotic dinoflagellates as possible determinant of bleaching susceptibility of corals. Mar Ecol Prog Ser 268:43–53CrossRefGoogle Scholar
  153. Yakovleva IM, Bhagooli R, Takemura A, Hidaka M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comp Biochem Physiol B 139:721–730CrossRefGoogle Scholar
  154. Yakovleva IM, Baird AH, Yamamoto HH, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperature. Mar Ecol Prog Ser 378:105–112CrossRefGoogle Scholar
  155. Yamashiro H, Hidaka M, Nishihira M, Poung-In S (1989) Morphological studies on skeletons of Diaseris fragilis, a free-living coral which reproduces asexually by natural autotomy. Galaxea 8:283–294Google Scholar
  156. Yamashita H, Koike K (2013) Genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol Res 61:68–80CrossRefGoogle Scholar
  157. Yeoh SR, Dai CF (2010) The production of sexual and asexual larvae within single broods of the scleractinian coral, Pocillopora damicornis. Mar Biol 157:351–359CrossRefGoogle Scholar
  158. Yuyama I, Watanabe T, Takei Y (2010) Profiling differential gene expression of symbiotic and aposymbiotic corals using a high coverage expression profiling (HiCEP) analysis. Mar Biotechnol. doi: 10.1007/s10126-010-9265-3 Google Scholar
  159. Yuyama I, Ito Y, Watanabe T, Hidak M, Suzuki Y, Nishida M (2012) Differential gene expression in juvenile polyps of the coral Acropora tenuis exposed to thermal and chemical stresses. J Exp Mar Biol Ecol 430–431:17–24CrossRefGoogle Scholar

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© Springer Japan 2016

Authors and Affiliations

  1. 1.University of the RyukyusNishiharaJapan

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