Abstract
Laboratory and field data bearing on the adaptive bleaching hypothesis (ABH) are largely consistent with it; no data of which we are aware refute it. We generalize the ABH in light of these data and observations. The population of zooxanthellae within an organism is dynamic, the diversity of zooxanthellae is both surprising and difficult to ascertain, and field experiments demonstrate both turn-over in zooxanthella types and habitat-holobiont correlations. Dynamic change in symbiont communities, and the idea of an equilibrium or optimal community that matches the environment at a particular place and time, are concepts that underlie or emerge from much of the recent literature. The mechanism we proposed to explain responses to acute bleaching appears to operate continuously, thereby enabling the host-symbiont holobiont to track even subtle environmental changes and respond promptly to them. These findings enhance the potential importance of the ABH in the outcomes of acute bleaching, which can (1) accelerate this process of holobiont change, and (2) change the set of possible trajectories for how symbiont communities might recover.
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References
F. A. Al-Horani S. M. Al-Moghrabi D. de Beer (2003) ArticleTitleThe mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis Marine Biology 142 419–426 Occurrence Handle1:CAS:528:DC%2BD3sXht1Clsr4%3D
O. R. Anderson C. Langdon T. Danelian (1998) ArticleTitleFine structure of a large dinoflagellate symbiont associated with a colonial radiolarian (Collozoum sp.) in the Banda Sea Symbiosis 24 259–270
A. C. Baker (2001) ArticleTitleReef corals bleach to survive change Nature 411 765–766 Occurrence Handle11459046 Occurrence Handle1:CAS:528:DC%2BD3MXksFOqsbc%3D
Baker, A. C., 2002. Is coral bleaching really adaptive? Nature 415: 602.
A. C. Baker (2003) ArticleTitleFlexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium Annual Review of Ecology, Evolution, and Systematics 34 661–689 Occurrence Handle10.1146/annurev.ecolsys.34.011802.132417
A. C. Baker (2004) Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience In Rosenberg E. (ed.), Coral Health and Disease, Springer-Verlag, Heidelberg: 177–194
Y. Benayahu M. H. Schleyer (1998) ArticleTitleReproduction in Anthelia glauca (Octocorallia: Xeniidae) II. Transmission of algal symbionts during planular brooding. Marine Biology 131 433–442
R. Bhagooli M. Hidaka (2003) ArticleTitleComparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species Journal of Experimental Marine Biology and Ecology 291 181–197
R. W. Buddemeier D. G. Fautin (1993) ArticleTitleCoral bleaching as an adaptive mechanism: a testable hypothesis BioScience 43 320–326
R. W. Buddemeier S. V. Smith (1999) ArticleTitleCoral adaptation and acclimatization: a most ingenious paradox American Zoologist 39 1–9
R. W. Buddemeier A. C. Baker D. G. Fautin J. R. Jacobs (2004) The adaptive hypothesis of bleaching In Rosenberg E. (ed.), Coral Health and Disease, Springer-Verlag, Heidelberg: 427–444
W. J. Burnett (2002) ArticleTitleLongitudinal variation in algal symbionts (zooxanthelle) from the Indian Ocean zoanthid Palythoa caesia Marine Ecology Progress Series 234 105–109
L. S. Ciereszko (1991) ArticleTitleSterol and diterpenoid production by zooxanthellae in coral reefs: a review Biological Oceanography 6 (for 1988/1989) 363–374
M. A. Coffroth S. R. Santos T. L. Goulet (2001) ArticleTitleEarly ontogenetic expression of specificity in a cnidarian-algal symbiosis Marine Ecology Progress Series 222 85–96
H. T. Darius P. M. V. Martin P. A. D. Grimont C. Dauga (2000) ArticleTitleSmall subunit rDNA sequence analysis of symbiotic dinoflagellates from seven scleractinian corals in a Tahitian lagoon Journal of Phycology 36 951–959 Occurrence Handle10.1046/j.1529-8817.2000.99088.x Occurrence Handle1:CAS:528:DC%2BD3cXos1Oqsbg%3D
S. K. Davy I. A. N. Lucas J. R. Turner (1997) ArticleTitleUptake and persistence of homologous and heterologous zooxanthellae in the temperate sea anemone Cereus pedunculatus (Pennant) Biological Bulletin 192 208–216
O. E. Diekmann R. P. M. Bak L. Tonk W. T. Stam J. L. Olsen (2002) ArticleTitleNo habitat correlation of zooxanthellae in the coral genus Madracis on a Curaçao reef Marine Ecology Progress Series 227 221–232
A. E. Douglas (2003) ArticleTitleCoral bleaching–how and why Marine Pollution Bulletin 46 385–392 Occurrence Handle10.1016/S0025-326X(03)00037-7 Occurrence Handle12705909 Occurrence Handle1:CAS:528:DC%2BD3sXivV2gs74%3D
P. J. Edmunds (1994) ArticleTitleEvidence that reef-wide patterns of coral bleaching may be the result of the distribution of bleaching-susceptible clones Marine Biology 121 137–142 Occurrence Handle10.1007/BF00349482
I. Fagoonee H. B. Wilson M. P. Hassell J. R. Turner (1999) ArticleTitleThe dynamics of zooxanthellae populations: a long-term study in the field Science 238 843–845
P. G. Falkowski Z. Dubinsky L. Muscatine L. McCloskey (1993) ArticleTitlePopulation control in symbiotic corals BioScience 43 606–611
W. K. Fitt (1985) ArticleTitleEffect of different strains of the zooxanthella Symbiodinium microadriaticum on growth and survival of their coelenterate and molluscan hosts Proceedings of the Fifth International Coral Reef Congress 6 131–136
W. K. Fitt M. E. Warner (1995) ArticleTitleBleaching patterns of four species of Caribbean reef corals Biological Bulletin 189 298–307
W. K. Fitt R. K. McFarland M. E. Warner G. C. Chilcoat (2000) ArticleTitleSeasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching Limnology and Oceanography 45 677–685 Occurrence Handle1:CAS:528:DC%2BD3cXjsV2ltbg%3D Occurrence Handle10.4319/lo.2000.45.3.0677
W. K. Fitt B. E. Brown M. E. Warner R. P. Dunne (2001) ArticleTitleCoral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals Coral Reefs 20 51–65 Occurrence Handle10.1007/s003380100146
R. D. Gates P. J. Edmunds (1999) ArticleTitleThe physiological mechanisms of acclimatization in tropical reef corals American Zoologist 39 30–43
P. W. Glynn J. I. Maté A. C. Baker M. O. Calderon (2001) ArticleTitleCoral bleaching and mortality in Panama and Ecuador during the 1997-1998 El Niño–southern oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event Bulletin of Marine Science 69 79–109
T. L. Goulet M. A. Coffroth (2003a) ArticleTitleGenetic composition of zooxanthellae between and within colonies of the octocoral Plexaura kuna, based on small subunit rDNA and multilocus DNA fingerprinting Marine Biology 142 233–239 Occurrence Handle1:CAS:528:DC%2BD3sXpslSqtw%3D%3D
T. L. Goulet M. A. Coffroth (2003b) ArticleTitleStability of an octocoral-algal symbiosis over time and space Marine Ecology Progress Series 250 117–124
M. Hill T. Wilcox (1998) ArticleTitleUnusual mode of symbiont repopulation after bleaching in Anthosigmella varians: acquisition of different zooxanthellae strains Symbiosis 25 279–289
O. Hoegh-Guldberg (1999) ArticleTitleClimate change, coral bleaching and the future of the world’s coral reefs Marine and Freshwater Research 50 839–866 Occurrence Handle10.1071/MF99078
O Hoegh-Guldberg R. J. Jones S. Ward W. K. Loh (2002) ArticleTitleIs coral bleaching really adaptive Nature 415 601–602 Occurrence Handle10.1038/415601a Occurrence Handle11832932 Occurrence Handle1:CAS:528:DC%2BD38XhsVCjs78%3D
T. Hughes A. P. D. H. Baird M. R. Bellwood S. Card C. R. Connolly R. Folke O. Grosberg J. Hoegh-Guldberg J. B. C. Jackson J. Kleypas P. M. Lough M. Marshall S. Nyström J. R. Palumbi B. M. Pandolfi J. Roughgarden Rosen (2003) ArticleTitleClimate change, human impacts, and the resilience of coral reefs Science 301 929–933 Occurrence Handle10.1126/science.1085046 Occurrence Handle12920289 Occurrence Handle1:CAS:528:DC%2BD3sXmt1elsb4%3D
R. Kinzie III A. G. S. Chee (1979) ArticleTitleThe effect of different zooxanthellae on the growth of experimentally reinfected hosts Biological Bulletin 156 315–327 Occurrence Handle36925
R. Kinzie III A. S. M. Takayama M. R. Santos A. Coffroth (2001) ArticleTitleThe adaptive bleaching hypothesis: experimental tests of critical assumptions Biological Bulletin 200 51–58 Occurrence Handle11249211
T. C. LaJeunesse (2002) ArticleTitleDiversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs Marine Biology 141 387–400
T. C. LaJeunesse W. K. W. Loh R. van Woesik O. Hoegh-Guldberg G. W. Schmidt W. K. Fitt (2003) ArticleTitleLow symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean Limnology and Oceanography 48 2046–2054 Occurrence Handle10.4319/lo.2003.48.5.2046
Merriam-Webster, 1997. Merriam Webster’s Collegiate Dictionary (10th ed.), Merriam-Webster, Inc., Springfield MA, U.S.A.
M. K. Montgomery P. M. Kremer (1995) ArticleTitleTransmission of symbiotic dinoflagellates through the sexual cycle of the host scyphozoan Linuche unguiculata Marine Biology 124 147–155 Occurrence Handle10.1007/BF00349156
M. D. Piercey-Normore P. T. DePriest (2001) ArticleTitleAlgal switching among lichen symbiosis American Journal of Botany 88 1490–1498 Occurrence Handle1:CAS:528:DC%2BD3MXmsVyhtbs%3D
P. J. Ralph R. Gademann A. W. D. Larkum (2001) ArticleTitleZooxanthellae expelled from bleached corals at 33° C are photosynthetically competent Marine Ecology Progress Series 220 163–168 Occurrence Handle1:CAS:528:DC%2BD3MXpt1Kjsr0%3D
J. K. Reaser R. Pomerance P. O. Thomas (2000) ArticleTitleCoral bleaching and global climate change: scientific findings and policy recommendations Conservation Biology 14 1500–1511 Occurrence Handle10.1046/j.1523-1739.2000.99145.x
M. Rodriguez-Lanetty W. Loh D. Carter O. Hoegh-Guldberg (2001) ArticleTitleLatitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora Marine Biology 138 1175–1181 Occurrence Handle1:CAS:528:DC%2BD3MXls1Sls78%3D
M. Rodriguez-Lanetty H. R. Cha J. I. Song (2002) ArticleTitleGenetic diversity of symbiotic dinoflagellates associated with anthozoans from Korean waters Proceedings of the Ninth International Coral Reef Symposium 1 163–166
M. Rodriguez-Lanetty S.-J. Chang J.-I. Song (2003) ArticleTitleSpecificity of two temperate dinoflagellate-anthozoan associations from the north-western Pacific Ocean Marine Biology 143 1193–1199
R. Rowan (1998) ArticleTitleDiversity and ecology of zooxanthellae on coral reefs Journal of Phycology 34 407–417 Occurrence Handle10.1046/j.1529-8817.1998.340407.x
R. Rowan N. Knowlton A. Baker J. Jara (1997) ArticleTitleLandscape ecology of algal symbionts creates variation in episodes of coral bleaching Nature 388 265–269 Occurrence Handle10.1038/40843 Occurrence Handle9230434 Occurrence Handle1:CAS:528:DyaK2sXkslShu78%3D
S. R. Santos D. J. Taylor M. A. Coffroth (2001) ArticleTitleGenetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: implications for extrapolating to the intact symbiosis Journal of Phycology 37 900–912 Occurrence Handle10.1046/j.1529-8817.2001.00194.x Occurrence Handle1:CAS:528:DC%2BD3MXosFCgsrs%3D
S. Santos D. R. R. J. Taylor M. A. Kinzie III K. Sakai Hidaka M. A. Coffroth (2002) ArticleTitleMolecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences Molecular Phylogenetics and Evolution 23 97–111 Occurrence Handle10.1016/S1055-7903(02)00010-6 Occurrence Handle12069543 Occurrence Handle1:CAS:528:DC%2BD38XksFOnsb8%3D
S. R. Santos C. Gutiérrez-Rodriguez H. R. Lasker M. A. Coffroth (2003) ArticleTitleSymbiodinium sp associations in the gorgonian Pseudopterogorgia elisabethae in the Bahamas: high levels of genetic variability in symbiotic dinoflagellates. Marine Biology 143 111–120
A. M. Savage M. S. Goodson S. Visram H. Trapido-Rosenthal J. Wiedenmann A. E. Douglas (2002a) ArticleTitleMolecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and sea anemones Marine Ecology Progress Series 244 17–26
A. M. Savage H. Trapido-Rosenthal A. E. Douglas (2002b) ArticleTitleOn the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance Marine Ecology Progress Series 244 27–37
D. Secord L. Augustine (2000) ArticleTitleBiogeography and microhabitat variation in temperate algal-invertebrate symbioses: zooxanthellae and zoochlorellae in two Pacific intertidal sea anemones, Anthopleura elegantissima and A xanthogrammica. Invertebrate Biology 119 139–146
W. W. Toller R. Rowan N. Knowlton (2001a) ArticleTitleRepopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M faveolata following experimental and disease-associated bleaching. Biological Bulletin 201 360–373 Occurrence Handle1:CAS:528:DC%2BD38XltlGlug%3D%3D
W. W. Toller R. Rowan N. Knowlton (2001b) ArticleTitleZooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths Biological Bulletin 201 348–359 Occurrence Handle1:CAS:528:DC%2BD38XltlGltQ%3D%3D
R. K. Trench R. J. Blank (1987) ArticleTitleSymbiodinium microadriaticum Freudenthal, S goreauii sp. nov., S. kawagutii sp. nov. and S. pilosum sp. nov.: gymnodinioid dinoflagellate symbionts of marine invertebrates. Journal of Phycology 23 469–481
J. E. N. Veron (1995) Corals in Space & Time: the Biogeography & Evolution of the Scleractinia Comstock/Cornell Ithaca and London
J. E. N. Veron (2000) Corals of the World [three volumes] Australian Institute of Marine Science Townsville, Queensland, Australia
J. R. Ware D. G. Fautin R. W. Buddemeier (1996) ArticleTitlePatterns of coral bleaching: modeling the adaptive bleaching hypothesis Ecological Modelling 84 199–214 Occurrence Handle10.1016/0304-3800(94)00132-4
M. E. Warner W. K. Fitt G. W. Schmidt (1999) ArticleTitleDamage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching Proceedings of the National Academy of Sciences of the USA 96 8007–8012 Occurrence Handle10393938 Occurrence Handle1:CAS:528:DyaK1MXltVOku7s%3D
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Fautin, D.G., Buddemeier, R.W. Adaptive bleaching: a general phenomenon. Hydrobiologia 530, 459–467 (2004). https://doi.org/10.1007/s10750-004-2642-z
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DOI: https://doi.org/10.1007/s10750-004-2642-z