UvA-DARE (Digital Academic Repository)

Transcription

1 UvA-DARE (Digital Academic Repository) Corals through the light : phylogenetics, functional diversity and adaptive strategies of coral-symbiont associations over a large depth range Rodrigues Frade, P. Link to publication Citation for published version (APA): Rodrigues Frade, P. (2009). Corals through the light : phylogenetics, functional diversity and adaptive strategies of coral-symbiont associations over a large depth range General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam ( Download date: 14 Dec 2018

2 Ab r e g o D, Ulstrup KE, Willis BL, va n Oppen MJH (2008) Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proceedings of the Royal Society B-Biological Sciences 275: Al l a k h v e r d i e v SI, Haya s h i H, Ni s h i ya m a Y, Iva n o v AG, Aliev JA, Kl i m o v VV, Mu r ata N, Carpentier R (2003) Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. Journal of Plant Physiology 160: Al l a k h v e r d i e v SI, Lo s DA, Mo h a n t y P, Ni s h i ya m a Y, Mu r ata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochimica et Biophysica Acta 1767: Alt s c h u l SF, Ma d d e n TL, Sc h a f f e r AA, Zh a n g JH, Zh a n g Z, Miller W, Li p m a n DJ (1997) Gapped b l a s t and psi-b l a s t: a new generation of protein database search programs. Nucleic Acids Research 25: Anderson E, Stebbins GL (1954) Hybridization as an evolutionary stimulus. Evolution 8: An d r e l l RM, Ly S, Ha g e d o r n M, Carter VL, Ya n c e y PH (2006) Glycine betaine as the major osmolyte in larva and adult Fungia scutaria coral. Integrative and Comparative Biology 46 (Suppl. 1): E165 An t h o n y KRN, Fa b r i c i u s KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. Journal of Experimental Marine Biology and Ecology 252: An t h o n y KRN, Ho e g h-guldberg O (2003) Variation in coral photosynthesis, respiration and growth characteristics in contrasting light microhabitats: An analogue to plants in forest gaps and understoreys? Functional Ecology 17: An t h o n y KRN, Ho o g e n b o o m MO, Co n n o l ly SR (2005) Adaptive variation in coral geometry and the optimization of internal colony light climates. Functional Ecology 19:17-26 An t h o n i U, Ch r i s t o p h e r s e n C, Ho u g a a r d L, Nielsen PH (1991) Quaternary ammonium compounds in the biosphere an example of a versatile adaptive strategy. Comparative Biochemistry and Physiology. B, Comparative Biochemistry 99: 1-18 Apprill AM, Gates RD (2007) Recognizing diversity in coral symbiotic dinoflagellate communities. Molecular Ecology 16: Apprill AM, Bi d i g a r e RR, Gates RD (2007) Visibly healthy corals exhibit variable pigment concentrations and symbiont phenotypes. Coral Reefs 26: Av i s e JC, Ar n o l d J, Ba l l RM, Be r m i n g h a m E, La m b T, Neigel JE, Reeb CA, Sa u n d e r s NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics 18: Baillie BK, Belda-Baillie CA, Silvestre V, Si s o n M, Go m e z AV, Go m e z ED, Mo n j e V (2000) Genetic variation in Symbiodinium isolates from giant clams based on random-amplifiedpolymorphic DNA (RAPD) patterns. Marine Biology 136: Ba i r d ME, At k i n s o n MJ (1997) Measurement and prediction of mass transfer to experimental coral reef communities. Limnology and Oceanography 42: Ba k RPM (1977) Coral reefs and their zonation in the Netherlands Antilles. The American Association of Petroleum Geologists 4:3-16 Ba k RPM, Ni e u w l a n d G, Meesters EH (2005) Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curaçao and Bonaire. Coral Reefs 24: Ba k RPM, Jo e n j e M, d e Jo n g I, La m b r e c h t s DYM, Ni e u w l a n d G (1998) Bacterial suspension feeding by coral reef benthic organisms. Marine Ecology-Progress Series 175: Baker AC (2001) Ecosystems - Reef corals bleach to survive change. Nature 411: Baker AC (2002) Ecology - Is coral bleaching really adaptive? Reply. Nature 415: Ba k e r AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology Evolution and Systematics 138

3 34: Ba k e r AC, Ro wa n R (1997) Diversity of symbiotic dinoflagellates (zooxanthellae) in Scleractinian corals of the Caribbean and Eastern Pacific. Proceedings of the 8th International Coral Reef Symposium 2: Ba k e r AC, Ro m a n s k i AM (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: Comment on Goulet (2006). Marine Ecology-Progress Series 335: Ba k e r AC, Gly n n PW, Ri e g l B (2008) Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuarine Coastal and Shelf Science 80: Ba k e r AC, Sta r g e r CJ, McCl a n a h a n TR, Gly n n PW (2004) Corals' adaptive response to climate change. Nature 430: Ba n a s z a k AT, LaJe u n e s s e TC, Tr e n c h RK (2000) The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. Journal of Experimental Marine Biology and Ecology 249: Banaszak AT, Santos MG, LaJeunesse TC, Lesser MP (2006) The distribution of mycosporinelike amino acids (MAAs) and the phylogenetic identity of symbiotic dinoflagellates in cnidarian hosts from the Mexican Caribbean. Journal of Experimental Marine Biology and Ecology 337: Ba r b r o o k AC, Vi s r a m S, Do u g l a s AE, Ho w e CJ (2006) Molecular diversity of dinoflagellate symbionts of Cnidaria: The psba minicircle of Symbiodinium. Protist 157: Beer S, Il a n M, Es h e l A, Weil A, Br i c k n e r I (1998) Use of pulse amplitude modulated (PAM) fluorometry for in situ measurements of photosynthesis in two Red Sea faviid corals. Marine Biology 131: Be n n i o n BJ, Da g g e t t V (2004) Counteraction of urea-induced protein denaturation by trimethylamine N-oxide: a chemical chaperone at atomic resolution. Proceedings of the National Academy of Sciences of the United States of America 101: Be r k e l m a n s R, va n 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. Proceedings of the Royal Society B-Biological Sciences 273: Bh a g o o l i R, Hi d a k a M (2003) Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species. Journal of Experimental Marine Biology and Ecology 291: Bl a n k RJ (1987) Cell architecture of the dinoflagellate Symbiodinium sp. inhabiting the Hawaiian stony coral Montipora verrucosa. Marine Biology 94: Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell Science Ltd, Oxford Bl u n d e n G, Go r d o n SM (1986) Betaines and their sulphonio analogues in marine algae. Progress in Phycological Research 4: Bo e h n l e i n JM, Sa n t i a g o-vazquez LZ, Ke r r RG (2005) Diterpene biosynthesis by the dinoflagellate symbiont of the Caribbean gorgonian Pseudopterogorgia bipinnata. Marine Ecology- Progress Series 303: Bo h o n a k AJ (1999) Dispersal, gene flow, and population structure. Quarterly Review of Biology 74:21-45 Borell EM, Yu l i a n t r i AR, Bi s c h o f K, Richter C (2008) The effect of heterotrophy on photosynthesis and tissue composition of two scleractinian corals under elevated temperature. Journal of Experimental Marine Biology and Ecology 364: Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129-S138 Br o w n BE, Letissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Marine Biology 122: Br o w n BE, Do w n s CA, Du n n e RP, Gi b b SW (2002a) Preliminary evidence for tissue retraction as a factor in photoprotection of corals incapable of xanthophyll cycling. Journal of 139

4 Experimental Marine Biology and Ecology 277: Br o w n BE, Do w n s CA, Du n n e RP, Gi b b SW (2002b) Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Marine Ecology-Progress Series 242: Br o w n BE, Am b a r s a r i I, Wa r n e r ME, Fitt WK, Du n n e RP, Gi b b SW, Cu m m i n g s DG (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18: Br u n o JF, Ed m u n d s PJ (1997) Clonal variation for phenotypic plasticity in the coral Madracis mirabilis. Ecology 78: Bu c k l e r ES, Ippolito A, Ho lt s f o r d TP (1997) The evolution of ribosomal DNA: Divergent paralogues and phylogenetic implications. Genetics 145: Bu d d AF, Jo h n s o n KG (1999) Origination preceding extinction during late Cenozoic turnover of Caribbean reefs. Paleobiology 25: Bu d d AF, Pa n d o l f i JM (2004) Overlapping species boundaries and hybridization within the Montastraea annularis reef coral complex in the Pleistocene of the Bahama Islands. Paleobiology 30: Bu d d AF, St e m a n n TA, Jo h n s o n KG (1994) Stratigraphic distributions of genera and species of Neogene to recent caribbean reef corals. Journal of Paleontology 68: Bu d d AF, Jo h n s o n KG, Ed wa r d s JC (1995) Caribbean reef coral diversity during the early to middle Miocene - an example from the Anguilla formation. Coral Reefs 14: Bu d d e m e i e r RW, Fa u t i n DG (1993) Coral bleaching as an adaptive mechanism A testable hypothesis. Bioscience 43: Bu r r i s RH (1983) Uptake and assimilation of 15 + NH 4 by a variety of corals. Marine Biology 75: Carpenter KE, Ab r a r M, Ae b y G, Ar o n s o n RB, Ba n k s S, Br u c k n e r A, Ch i r i b o g a A, Cortes J, Delbeek JC, DeVa n t i e r L, Ed g a r GJ, Ed wa r d s AJ, Fe n n e r D, Gu z m a n HM, Ho e k s e m a BW, Ho d g s o n G, Jo h a n O, Li c u a n a n WY, Li v i n g s t o n e SR, Lo v e l l ER, Mo o r e JA, Ob u r a DO, Oc h av i l l o D, Po l i d o r o BA, Pr e c h t WF, Qu i b i l a n MC, Re b o t o n C, Ri c h a r d s ZT, Ro g e r s AD, Sa n c i a n g c o J, Sh e p pa r d A, Sh e p pa r d C, Sm i t h J, St u a rt S, Tu r a k E, Ve r o n JEN, Wa l l a c e C, Weil E, Wo o d E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321: Ch a n g SS, Prezelin BB, Tr e n c h RK (1983) Mechanisms of photoadaptation in 3 strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Marine Biology 76: Ch e n CA, Ya n g YW, Wei NV, Ts a i WS, Fa n g LS (2005) Symbiont diversity in scleractinian corals from tropical reefs and subtropical non-reef communities in Taiwan. Coral Reefs 24:11-22 Ch e n FCM, Be n o i t o n NL (1976) A new method of quaternizing amines and its use in amino acid and peptide chemistry. Canadian Journal of Chemistry 54: Ch e n THH, Mu r ata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Current Opinion in Plant Biology 5: Ch e n THH, Mu r ata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends in Plant Science 13: Co f f r o t h MA, Sa n t o s SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19-34 Co l e m a n AW, Su a r e z A, Go f f LJ (1994) Molecular delineation of species and syngens in volvocacean green-algae (Chlorophyta). Journal of Phycology 30:80-90 Co n c e p c i o n GT, Me d i n a M, To o n e n RJ (2006) Noncoding mitochondrial loci for corals. Molecular Ecology Notes 6: Co r r e a AMS, Ba k e r AC (2009) Understanding diversity in coral-algal symbiosis: a cluster-based approach to interpreting fine-scale genetic variation in the genus Symbiodinium. Coral Reefs 28:81-93 Darwin CR (1842) The structure and distribution of coral reefs. Smith, Elder and Co, London Da r w i n CR (1859) On the origin of species by means of natural selection, or the preservation of 140

5 favoured races in the struggle for life. In: Murray J (ed). content/frameset?itemid=f373&viewtype=text&pageseq=1, London Dawkins R (1990) The selfish gene. Oxford University Press, USA Day T, Na g e l L, Va n Oppen MJH, Caley MJ (2008) Factors affecting the evolution of bleaching resistance in corals. American Naturalist 171:E72-E88 DeBo s e JL, Le m a SC, Nevitt GA (2008) Dimethylsulfoniopropionate as a foraging cue for reef fishes. Science 319: 1356 DeLo n g EF, Ka r l DM (2005) Genomic perspectives in microbial oceanography. Nature 437: De s a lv o MK, RVo o l s t r a C, Su n a g awa S, Sc h wa r z JA, Stillman JH, Co f f r o t h MA, Sz m a n t AM, Me d i n a M (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Molecular Ecology 17: Di e k m a n n OE (2003) The coral genus Madracis. PhD thesis, University of Amsterdam Di e k m a n n OE, Ba k RPM, Sta m WT, Olsen JL (2001) Molecular genetic evidence for probable reticulate speciation in the coral genus Madracis from a Caribbean fringing reef slope. Marine Biology 139: Di e k m a n n OE, Olsen JL, Sta m WT, Ba k RPM (2003) Genetic variation within Symbiodinium clade B from the coral genus Madracis in the Caribbean (Netherlands Antilles). Coral Reefs 22:29-33 Di e k m a n n OE, Ba k RPM, To n k L, Sta m WT, Olsen JL (2002) No habitat correlation of zooxanthellae in the coral genus Madracis on a Curaçao reef. Marine Ecology-Progress Series 227: Do n RH, Co x PT, Wa i n w r i g h t BJ, Ba k e r K, Mattick JS (1991) Touchdown PCR to circumvent spurious priming during gene amplification. Nucleic Acids Research 19: Do n n e r SD, Kn u t s o n TR, Oppenheimer M (2007) Model-based assessment of the role of humaninduced climate change in the 2005 Caribbean coral bleaching event. Proceedings of the National Academy of Sciences of the United States of America 104: Do n o g h u e MJ (1985) A critique of the biological species concept and recommendations for a phylogenetic alternative. The Bryologist 88: Douglas AE (2003) Coral bleaching - How and why? Marine Pollution Bulletin 46: Do v e S, Ort i z JC, En r i q u e z S, Fi n e M, Fi s h e r P, Ig l e s i a s-prieto R, Th o r n h i l l D, Ho e g h-guldberg O (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnology and Oceanography 51: Do v e SG, Ho e g h-guldberg O, Ra n g a n at h a n S (2001) Major colour patterns of reef-building corals are due to a family of GFP-like proteins. Coral Reefs 19: Dr e w EA (1972) The biology and physiology of alga-invertebrate symbiosis. II. The density of symbiotic algal cells in a number of hermatypic hard corals and alcyonarians from various depths. Journal of Experimental Marine Biology and Ecology 9:71-75 Du b i n s k y Z, Fa l k o w s k i PG, Porter JW, Mu s c at i n e L (1984) Absorption and utilization of radiant energy by light-adapted and shade-adapted colonies of the hermatypic coral Stylophora pistillata. Proceedings of the Royal Society of London Series B-Biological Sciences 222: Du b i n s k y Z, Stambler N, Be n z i o n M, Mc c l o s k e y LR, Mu s c at i n e L, Fa l k o w s k i PG (1990) The effect of external nutrient resources on the optical-properties and photosynthetic efficiency of Stylophora pistillata. Proceedings of the Royal Society of London Series B-Biological Sciences 239: Du s ta n P (1975) Growth and form in reef-building coral Montastrea annularis. Marine Biology 33: Ed m u n d s PJ, Gates RD (2008) Acclimatization in tropical reef corals. Marine Ecology-Progress Series 361: En n o s RA, Fr e n c h GC, Ho l l i n g s w o rt h PM (2005) Conserving taxonomic complexity. Trends in Ecology & Evolution 20:

6 En r i q u e z S, Me n d e z ER, Ig l e s i a s-pr i e to R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnology and Oceanography 50: Ex c o f f i e r L, Sm o u s e PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes - Application to human mitochondrial-dna restriction data. Genetics 131: Ex c o f f i e r L, Lava l G, Sc h n e i d e r S (2005) a r l e q u i n ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1:47-50 Fa b r i c i u s KE (2006) Effects of irradiance, flow, and colony pigmentation on the temperature microenvironment around corals: Implications for coral bleaching? Limnology and Oceanography 51:30-37 Fa l k o w s k i PG, Du b i n s k y Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289: Fa l k o w s k i PG, La r o c h e J (1991) Acclimation to spectral irradiance in algae. Journal of Phycology 27:8-14 Fa l k o w s k i PG, Kat z ME, Kn o l l AH, Qu i g g A, Rav e n JA, Sc h o f i e l d O, Tay l o r FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305: Fa u t i n DG, Bu d d e m e i e r RW (2004) Adaptive bleaching: a general phenomenon. Hydrobiologia : Fe n n e r DP (1993) Species distinctions among several Caribbean stony corals. Bulletin of Marine Science 53: Fe r r i e r-pa g e s C, Witting J, Ta m b u t t e E, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22: Field SF, Bu l i n a MY, Ke l m a n s o n IV, Bielawski JP, Mat z MV (2006) Adaptive evolution of multicolored fluorescent proteins in reef-building corals. Journal of Molecular Evolution 62:332-U315 Fitt WK, Co o k CB (2001) The effects of feeding or addition of dissolved inorganic nutrients in maintaining the symbiosis between dinoflagellates and a tropical marine cnidarian. Marine Biology 139: Fitt WK, McFa r l a n d FK, Wa r n e r ME, Ch i l c o at GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnology and Oceanography 45: Fitt WK, Br o w n BE, Wa r n e r ME, Du n n e RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51-65 Fr a d e PR, Englebert N, Fa r i a J, Visser PM, Ba k RPM (2008a) Distribution and photobiology of Symbiodinium types in different light environments for three colour morphs of the coral Madracis pharensis: is there more to it than total irradiance? Coral Reefs 27: Fr a d e PR, Bo n g a e rt s P, Wi n k e l h a g e n AJS, To n k L, Ba k RPM (2008b) In situ photobiology of corals over large depth ranges: A multivariate analysis on the roles of environment, host, and algal symbiont. Limnology and Oceanography 53: Fr a d e PR, d e Jo n g h F, Vermeulen F, va n Bleijswijk J, Ba k RPM (2008c) Variation in symbiont distribution between closely related coral species over large depth ranges. Molecular Ecology 17: Fr a n k l i n DJ, Ho e g h-gu l d b e r g P, Jo n e s RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Marine Ecology-Progress Series 272: Fr e u d e n t h a l HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella - Taxonomy, life cycle, and morphology. Journal of Protozoology 9:45-& Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: Fu k a m i H, Bu d d AF, Le v i ta n DR, Ja r a J, Ke r s a n a c h R, Kn o w lt o n N (2004a) Geographic differences in species boundaries among members of the Montastraea annularis complex based on 142

7 molecular and morphological markers. Evolution 58: Fu k a m i H, Bu d d AF, Pa u l ay G, So l e-cava A, Ch e n CLA, Iw a o K, Kn o w lt o n N (2004b) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427: Gates RD, Ed m u n d s PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. American Zoologist 39:30-43 Gates RD, Apprill AM, Wheeler BR (2005) Using molecular markers - A cautionary tale. Proceedings of the Workshop Understanding the stress response of corals and Symbiodinium in a rapidly changing environment, UNAM, Mexico Gly n n PW, Mat e JL, Ba k e r AC, Ca l d e r o n MO (2001) Coral bleaching and mortality in panama and Ecuador during the El Nino-Southern oscillation event: Spatial/temporal patterns and comparisons with the event. Bulletin of Marine Science 69: Go m e z -Ca b r e r a MD, Ort i z JC, Lo h WKW, Wa r d S, Ho e g h-gu l d b e r g O (2008) Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus. Coral Reefs 27: Go o d s o n MS, Wh i t e h e a d LF, Do u g l a s AE (2001) Symbiotic dinoflagellates in marine Cnidaria: Diversity and function. Hydrobiologia 461:79-82 Go r b u n o v MY, Kolber ZS, Lesser MP, Fa l k o w s k i PG (2001) Photosynthesis and photoprotection in symbiotic corals. Limnology and Oceanography 46:75-85 Go u l e t TL (2006) Most corals may not change their symbionts. Marine Ecology-Progress Series 321:1-7 Go u l e t TL, Co f f r o t h MA (2004) The genetic identity of dinoflagellate symbionts in Caribbean octocorals. Coral Reefs 23: Go u l e t TL, Co o k CB, Go u l e t D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallidal Symbiodinium symbiosis. Limnology and Oceanography 50: Gr o t t o l i AG, Ro d r i g u e s LJ, Pa l a r d y JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440: Ha l l TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95-98 Ha l l o c k P (2001) Coral reefs, carbonate sediments, nutrients and global change. In: Stanley Jr GD (ed) The history and sedimentology of ancient reef systems. Springer-Verlag, New York, pp Ha r r i s o n PL, Ba b c o c k RC, Bu l l GD, Oliver JK, Wa l l a c e CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223: Hat ta M, Fu k a m i H, Wa n g WQ, Om o r i M, Sh i m o i k e K, Haya s h i b a r a T, In a Y, Su g i ya m a T (1999) Reproductive and genetic evidence for a reticulate evolutionary history of mass-spawning corals. Molecular Biology and Evolution 16: He m a R, Se n t h i l-ku m a r M, Sh i va k u m a r S, Re d d y PC, Ud aya k u m a r M (2007) Chlamydomonas reinhardtii, a model system for functional validation of abiotic stress responsive genes. Planta 226: He n n i g e SJ, Su g g e t t DJ, Wa r n e r ME, McDo u g a l l KE, Sm i t h DJ (2009) Photobiology of Symbiodinium revisited: Bio-physical and bio-optical signatures. Coral Reefs 28: He n ry LA, Ha rt M (2005) Regeneration from injury and resource allocation in sponges and corals - A review. International Review of Hydrobiology 90: Hill R, Ra l p h PJ (2008) Dark-induced reduction of the plastoquinone pool in zooxanthellae of scleractinian corals and implications for measurements of chlorophyll a fluorescence. Symbiosis 46:45-56 Hill R, La r k u m AWD, Fr a n k a rt C, Kü h l M, Ra l p h PJ (2004) Loss of functional photosystem II reaction centres in zooxanthellae of corals exposed to bleaching conditions: Using 143

8 fluorescence rise kinetics. Photosynthesis Research 82: Hill RW, Da c e y JWH, Kr u p p DA (1995) Dimethylsulfoniopropionate in reef corals. Bulletin of Marine Science 57: Hinderstei n LM, Ma r r JCA, Ma rt i n e z FA, Do w g i a l l o MJ, Pu g l i s e KA, Zawa d a D, Py l e R (in press) Mesophotic coral ecosystems: Research strategies and ecological characterization. Coral Reefs Hi r o s e M, Kinzie RA, Hi d a k a M (2001) Timing and process of entry of zooxanthellae into oocytes of hermatypic corals. Coral Reefs 20: Hi r o s e M, Ya m a m o t o H, No n a k a M (2008) Metamorphosis and acquisition of symbiotic algae in planula larvae and primary polyps of Acropora spp. Coral Reefs 27: Hoegh-Guldberg O (2004) Coral reefs in a century of rapid environmental change. Symbiosis 37:1-31 Ho e g h-guldberg O, Jo n e s RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Marine Ecology-Progress Series 183:73-86 Ho e g h-guldberg O, Jo n e s RJ, Wa r d S, Lo h WK (2002) Ecology - Is coral bleaching really adaptive? Nature 415: Ho e g h-guldberg O, Mu m b y PJ, Ho o t e n AJ, Steneck RS, Greenfield P, Go m e z E, Ha rv e l l CD, Sa l e PF, Ed wa r d s AJ, Ca l d e i r a K, Kn o w lt o n N, Ea k i n CM, Ig l e s i a s-prieto R, Mu t h i g a N, Br a d b u ry RH, Du b i A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: Ho o g e n b o o m MO, An t h o n y KRN, Co n n o l ly SR (2006) Energetic cost of photoinhibition in corals. Marine Ecology-Progress Series 313:1-12 Ho u l b r e q u e F, Fe r r i e r-pages C (2009) Heterotrophy in tropical scleractinian corals. Biological Reviews 84:1-17 Ho u l b r e q u e F, Ta m b u t t e E, Fe r r i e r-pages C (2003) Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. Journal of Experimental Marine Biology and Ecology 296: Hu a n g D, Meier R, To d d PA, Ch o u LM (2008a) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding Journal of Molecular Evolution 66: Hu a n g HJ, Wa n g LH, Ch e n WNU, Fa n g LS, Ch e n CS (2008b) Developmentally regulated localization of endosymbiotic dinoflagellates in different tissue layers of coral larvae. Coral Reefs 27: Hu g h e s TP, Ay r e D, Co n n e l l JH (1992) The evolutionary ecology of corals. Trends in Ecology & Evolution 7: Hu i s m a n J, Matthijs HCP, Visser PM, Ba l k e H, Si g o n CAM, Pa s s a r g e J, Weissing FJ, Mu r LR (2002) Principles of the light-limited chemostat: theory and ecological applications. Antonie van Leeuwenhoek International Journal of General and Molecular Microbiology 81: Hu n t e r C, Mo r d e n CW, Sm i t h C (1997) The utility of ITS sequences in assessing relationships among zooxanthellae and corals. Proceedings of the 8th International Coral Reef Symposium 2: Hu x l e y J (1942) Evolution: The Modern Synthesis, London (reprinted with new Introduction, Science Editions, 1964) Ig l e s i a s-prieto R, Tr e n c h RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates.1. Responses of the photosynthetic unit to changes in photon flux-density. Marine Ecology-Progress Series 113: Ig l e s i a s-prieto R, Tr e n c h RK (1997a) Photoadaptation, photoacclimation and niche diversification in invertebrate-dinoflagellate symbioses. Proceedings of the 8th International Coral Reef Symposium 2: Ig l e s i a s-prieto R, Tr e n c h RK (1997b) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux 144

9 densities. Marine Biology 130:23-33 Ig l e s i a s-pr i e to R, Beltran VH, LaJe u n e s s e TC, Reyes-Bo n i l l a H, Th o m e PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proceedings of the Royal Society of London Series B-Biological Sciences 271: Ja r m a n SN, Wa r d RD, Elliott NG (2002) Oligonucleotide primers for PCR amplification of coelomate introns. Marine Biotechnology 4: Jerlov NG (1966) Optical Oceanography. Elsevier, Amsterdam Jolliffe IT, Tr e n d a f i l o v NT, Ud d i n M (2003) A modified principal component technique based on the LASSO. Journal of Computational and Graphical Statistics 12: Jo n e s AM, Be r k e l m a n s R, va n Oppen MJH, Mi e o g JC, Si n c l a i r W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B-Biological Sciences 275: Jo n e s RJ, Yellowlees D (1997) Regulation and control of intracellular algae (equals zooxanthellae) in hard corals. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 352: Jo n e s RJ, Ho e g h-gu l d b e r g O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant, Cell & Environment 24:89-99 Ka a n d o r p JA, Sl o o t PMA, Me r k s RMH, Ba k RPM, Vermeij MJA, Ma i e r C (2005) Morphogenesis of the branching reef coral Madracis mirabilis. Proceedings of the Royal Society B-Biological Sciences 272: Ka n i e w s k a P, An t h o n y KRN, Ho e g h-gu l d b e r g O (2008) Variation in colony geometry modulates internal light levels in branching corals, Acropora humilis and Stylophora pistillata. Marine Biology 155: Kasumyan AO, Døving KB (2003) Taste preferences in fishes. Fish and Fisheries 4: Kawa g u t i S (1944) On the physiology of reef corals VII. Zooxanthella of the reef coral is Gymnodinium sp., Dinoflagellata; its culture in vitro. Palao Tropical Biological Station Studies 2: Kinzie III RA, Ta k aya m a M, Sa n t o s SR, Co f f r o t h MA (2001) The adaptive bleaching hypothesis: Experimental tests of critical assumptions. Biological Bulletin 200:51-58 Ki r k JTO (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, London New York Kl i m o v VV, Al l a k h v e r d i e v SI, Ni s h i ya m a Y, Kh o r o b ry k h AA, Mu r ata N (2003) Stabilization of the oxygen-evolving complex of photosystem II by bicarbonate and glycinebetaine in thylakoid and subthylakoid preparations. Functional Plant Biology 30: Klueter A, Lo h W, Ho e g h-gu l d b e r g O, Do v e S (2006) Physiological and genetic properties of two fluorescent colour morphs of the coral Montipora digitata. Symbiosis 42: Kn o w lt o n N, Mat e JL, Gu z m a n HM, Ro wa n R, Ja r a J (1997) Direct evidence for reproductive isolation among the three species of the Montastraea annularis complex in Central America (Panama and Honduras). Marine Biology 127: LaJe u n e s s e TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: In search of a "species" level marker. Journal of Phycology 37: LaJe u n e s s e TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141: LaJeunesse TC (2005) "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo- Pacific since the Miocene-Pliocene transition. Molecular Biology and Evolution 22: LaJe u n e s s e TC, Tr e n c h RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biological 145

10 Bulletin 199: LaJe u n e s s e TC, Reyes-Bonilla H, Wa r n e r ME (2007) Spring "bleaching" among Pocillopora in the Sea of Cortez, eastern Pacific. Coral Reefs 26: LaJe u n e s s e TC, La m b e rt G, An d e r s e n RA, Co f f r o t h MA, Ga l b r a i t h DW (2005) Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. Journal of Phycology 41: LaJe u n e s s e TC, Lo h WKW, va n Wo e s i k R, Ho e g h-guldberg O, Sc h m i d t GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnology and Oceanography 48: LaJe u n e s s e TC, Bo n i l l a HR, Wa r n e r ME, Wills M, Sc h m i d t GW, Fitt WK (2008) Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnology and Oceanography 53: LaJeunesse TC, Bhagooli R, Hidaka M, DeVantier L, Done T, Schmidt GW, Fitt WK, Hoegh- Gu l d b e r g O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Marine Ecology-Progress Series 284: Leichter JJ, Wi n g SR, Miller SL, De n n y MW (1996) Pulsed delivery of subthermocline water to Conch Reef (Florida Keys) by internal tidal bores. Limnology and Oceanography 41: Lesser MP (2007) Coral reef bleaching and global climate change: Can corals survive the next century? Proceedings of the National Academy of Sciences of the United States of America 104: Lesser MP, Fa r r e l l JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23: Le v i ta n DR, Fu k a m i H, Ja r a J, Kl i n e D, McGo v e r n TM, McGh e e KE, Swa n s o n CA, Kn o w lt o n N (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58: Le v y O, Du b i n s k y Z, Ac h i t u v Y, Er e z J (2006a) Diurnal polyp expansion behavior in stony corals may enhance carbon availability for symbionts photosynthesis. Journal of Experimental Marine Biology and Ecology 333:1-11 Le v y O, Ac h i t u v Y, Ya c o b i YZ, Stambler N, Du b i n s k y Z (2006b) The impact of spectral composition and light periodicity on the activity of two antioxidant enzymes (SOD and CAT) in the coral Favia favus. Journal of Experimental Marine Biology and Ecology 328:35-46 Le w i s CL, Co f f r o t h MA (2004) The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304: Li n n a e u s C (1758) Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. In: Salvii L (ed). biodiversitylibrary.org/bibliography/542 Little AF, va n Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304: Lo h WKW, Lo i T, Carter D, Ho e g h-guldberg O (2001) Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Marine Ecology-Progress Series 222: Lo r a m JE, Tr a p i d o-rosenthal HG, Do u g l a s AE (2007a) Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Molecular Ecology 16: Lo r a m JE, Bo o n h a m N, O'Toole P, Tr a p i d o-rosenthal HG, Do u g l a s AE (2007b) Molecular quantification of symbiotic dinoflagellate algae of the genus Symbiodinium. Biological Bulletin 212: Lu d w i g W, St r u n k O, Westram R, Richter L, Meier H, Ya d h u k u m a r, Bu c h n e r A, La i T, Steppi S, Jo b b G, Forster W, Brettske I, Ge r b e r S, Gi n h a rt AW, Gr o s s O, Gr u m a n n S, He r m a n n S, Jo s t R, Ko n i g A, Liss T, Lu s s m a n n R, May M, No n h o f f B, Reichel B, Strehlow 146

11 R, Sta m ata k i s A, St u c k m a n n N, Vilbig A, Le n k e M, Lu d w i g T, Bo d e A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32: Ma c d o n a l d AHH, Sa m pay o EM, Ri d g way T, Schleyer MH (2008) Latitudinal symbiont zonation in Stylophora pistillata from southeast Africa. Marine Biology 154: Ma c k e n z i e JB, Mu n d ay PL, Willis BL, Miller DJ, va n Oppen MJH (2004) Unexpected patterns of genetic structuring among locations but not colour morphs in Acropora nasuta (Cnidaria; Scleractinia). Molecular Ecology 13:9-20 Ma i e r C, Patzold J, Ba k RPM (2003) The skeletal isotopic composition as an indicator of ecological and physiological plasticity in the coral genus Madracis. Coral Reefs 22: Ma r q u e z LM, va n Oppen MJH, Willis BL, Miller DJ (2002a) Sympatric populations of the highly cross-fertile coral species Acropora hyacinthus and Acropora cytherea are genetically distinct. Proceedings of the Royal Society of London Series B-Biological Sciences 269: Ma r q u e z LM, va n Oppen MJH, Willis BL, Reyes A, Miller DJ (2002b) The highly cross-fertile coral species, Acropora hyacinthus and Acropora cytherea, constitute statistically distinguishable lineages. Molecular Ecology 11: Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51: Ma rt i n DP, Wi l l i a m s o n C, Po s a d a D (2005) r d p2: recombination detection and analysis from sequence alignments. Bioinformatics 21: Ma rt i n d a l e JL, Ho l b r o o k NJ (2002) Cellular response to oxidative stress: Signaling for suicide and survival. Journal of Cellular Physiology 192:1-15 Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York McCl o s k e y LR, Mu s c at i n e L (1984) Production and respiration in the Red Sea coral Stylophora pistillata as a function of depth. Proceedings of the Royal Society London 222: McNeil SD, Nu c c i o ML, Ha n s o n AD (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiology 120: Meesters EH, Hilterman M, Ka r d i n a a l E, Keetman M, d e Vr i e s M, Ba k RPM (2001) Colony size-frequency distributions of scleractinian coral populations: spatial and interspecific variation. Marine Ecology-Progress Series 209:43-54 Me n d e l G (1865) Experiments in plant hybridization. Read at the February 8th, and March 8th, 1865, meetings of the Brünn Natural History Society. classical/gm-65.pdf Mi c h i k awa Y, Ho f h a u s G, Le r m a n LS, At ta r d i G (1997) Comprehensive, rapid and sensitive detection of sequence variants of human mitochondrial trna genes. Nucleic Acids Research 25: Mi d d l e b r o o k R, Ho e g h-gu l d b e r g O, Le g g at W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. Journal of Experimental Biology 211: Mi e o g JC, va n Oppen MJH, Ca n t i n NE, Sta m WT, Olsen JL (2007) Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: Implications for symbiont shuffling. Coral Reefs 26: Mi e o g JC, Va n Oppen MJH, Be r k e l m a n s R, Sta m WT, Olsen JL (2009) Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Molecular Ecology Resources 9:74-82 Miller K, Ba b c o c k R (1997) Conflicting morphological and reproductive species boundaries in the coral genus Platygyra. Biological Bulletin 192: Miller KJ, Ay r e DJ (2004) The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity 92: Miller KJ, Ay r e DJ (2008a) Protection of genetic diversity and maintenance of connectivity among reef corals within marine protected areas. Conservation Biology 22: Miller KJ, Ay r e DJ (2008b) Population structure is not a simple function of reproductive mode and 147

12 larval type: insights from tropical corals. Journal of Animal Ecology 77: Mi n d e r AM, Wi d m e r A (2008) A population genomic analysis of species boundaries: neutral processes, adaptive divergence and introgression between two hybridizing plant species. Molecular Ecology 17: Mi n d e r AM, Ro t h e n b u e h l e r C, Wi d m e r A (2007) Genetic structure of hybrid zones between Silene latifolia and Silene dioica (Caryophyllaceae): Evidence for introgressive hybridization. Molecular Ecology 16: Mo o r e RJ, Huxley CJ (1976) Aversive behaviour of crown-of-thorns starfish to coral evoked by food-related chemicals. Nature 263: Muller-Parker G, D'Elia CF (1997) Interactions between corals and their symbiotic algae. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, New York, pp Muller P, Li XP, Ni y o g i KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125: Mu s c at i n e L, Porter JW (1977) Reef corals - Mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27: Mu s c at i n e L, Fa l k o w s k i PG, Porter JW, Du b i n s k y Z (1984) Fate of photosynthetic fixed carbon in light-adapted and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proceedings of the Royal Society of London Series B-Biological Sciences 222: Mu s c at i n e L, Go i r a n C, La n d L, Ja u b e rt J, Cu i f JP, Allemand D (2005) Stable isotopes (δ 13 C and δ 15 N) of organic matrix from coral skeleton. Proceedings of the National Academy of Sciences of the United States of America 102: My e r s RM, Fi s c h e r SG, Le r m a n LS, Ma n i at i s T (1985a) Nearly all single base substitutions in DNA fragments joined to a GC-clamp can be detected by denaturing gradient gelelectrophoresis. Nucleic Acids Research 13: My e r s RM, Lu m e l s k y N, Le r m a n LS, Ma n i at i s T (1985b) Detection of single base substitutions in total genomic DNA. Nature 313: Na g e l k e r k e n I, Bo u m a S, va n d e n Ak k e r S, Ba k RPM (2000) Growth and survival of unattached Madracis mirabilis fragments transplanted to different reef sites, and the implication for reef rehabilitation. Bulletin of Marine Science 66: Nu g u e s MM, Ba k RPM (2008) Long-term dynamics of the brown macroalga Lobophora variegata on deep reefs in Curaçao. Coral Reefs 27: Od o r i c o DM, Miller DJ (1997) Variation in the ribosomal internal transcribed spacers and 5.8S rdna among five species of Acropora (Cnidaria; Scleractinia): Patterns of variation consistent with reticulate evolution. Molecular Biology and Evolution 14: Or e n U, Be n aya h u Y, Lu b i n e v s k y H, Lo ya Y (2001) Colony integration during regeneration in the stony coral Favia favus. Ecology 82: Os w a l d F, Sc h m i t t F, Leutenegger A, Iva n c h e n k o S, D'Angelo C, Sa l i h A, Ma s l a k o va S, Bu l i n a M, Sc h i r m b e c k R, Ni e n h a u s GU, Mat z MV, Wi e d e n m a n n J (2007) Contributions of host and symbiont pigments to the coloration of reef corals. FEBS Journal 274: Pa l a r d y JE, Ro d r i g u e s LJ, Gr o t t o l i AG (2008) The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. Journal of Experimental Marine Biology and Ecology 367: Pa l u m b i SR (1994) Genetic-divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics 25: Pa pa g e o r g i o u GC, Mu r ata N (1995) The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem-ii complex. Photosynthesis Research 44: Pa p i n a M, Me z i a n e T, va n Wo e s i k R (2007) Acclimation effect on fatty acids of the coral Montipora digitata and its symbiotic algae. Comp Biochem Phys B 147: Pa s s a r g e J, Ho l S, Es c h e r M, Hu i s m a n J (2006) Competition for nutrients and light: Stable coexistence, alternative stable states, or competitive exclusion? Ecological Monographs 76:

13 Pe a r s e VB, Mu s c at i n e L (1971) Role of symbiotic algae (zooxanthellae) in coral calcification. Biological Bulletin 141: Pettay DT, La j e u n e s s e TC (2007) Microsatellites from clade B Symbiodinium spp. specialized for Caribbean corals in the genus Madracis. Molecular Ecology Notes 7: Po c h o n X, LaJe u n e s s e TC, Paw l o w s k i J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Marine Biology 146:17-27 Po c h o n X, Mo n t o ya-bu r g o s JI, Sta d e l m a n n B, Paw l o w s k i J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Molecular Phylogenetics and Evolution 38:20-30 Polnefuller M (1991) A novel technique for preparation of axenic cultures of Symbiodinium (Pyrrophyta) through selective digestion by amoebae. Journal of Phycology 27: Porter JW, Mu s c at i n e L, Du b i n s k y Z, Fa l k o w s k i PG (1984) Primary production and photoadaptation in light-adapted and shade-adapted colonies of the symbiotic coral, Stylophora pistillata. Proceedings of the Royal Society of London Series B-Biological Sciences 222: Po s a d a D, Cr a n d a l l KA (1998) modeltest: testing the model of DNA substitution. Bioinformatics 14: Po s a d a D, Bu c k l e y TR (2004) Model selection and model averaging in phylogenetics: Advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53: Pr a s a d KVSK, Sa r a d h i PP (2004) Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into the chloroplasts. Plant Science 166: Ra l p h PJ, Ga d e m a n n R, La r k u m AWD (2001) Zooxanthellae expelled from bleached corals at 33 degrees C are photosynthetically competent. Marine Ecology-Progress Series 220: Reeve HK, Keller L (1999) Levels of selection: Burying the units-of-selection debate and unearthing the crucial new issues. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton pp3-14 Re y n o l d s JM, Br u n s BU, Fitt WK, Sc h m i d t GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proceedings of the National Academy of Sciences of the United States of America 105: Rh o d e s D, Ha n s o n AD (1993) Quaternary ammonium and Tertiary sulfonium compounds in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 44: Ro b i s o n JD, Wa r n e r ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). Journal of Phycology 42: Ro d r i g u e s LJ, Gr o t t o l i AG (2006) Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals. Geochimica Et Cosmochimica Acta 70: Ro d r i g u e s LJ, Gr o t t o l i AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnology and Oceanography 52: Ro d r i g u e z-lanetty M (2003) Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rdna. Molecular Phylogenetics and Evolution 28: Ro d r i g u e z-lanetty M, Ho e g h-gu l d b e r g O (2003) Symbiont diversity within the widespread scleractinian coral Plesiastrea versipora, across the northwestern Pacific. Marine Biology 143: Ro d r i g u e z-lanetty M, Lo h W, Carter D, Ho e g h-gu l d b e r g O (2001) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Marine Biology 138: Ro m a n s k i AM, Ba k e r A (2005) Symbiodinium ITS-2 sequences: Inter- or intraspecific data? Implications for the detection of ecological and biogeographic patterns. Proceedings 149

14 of the Workshop Understanding the stress response of corals and Symbiodinium in a rapidly changing environment, UNAM, Mexico Ro wa n R (1998) Diversity and ecology of zooxanthellae on coral reefs. Journal of Phycology 34: Rowan R (2004) Coral bleaching - Thermal adaptation in reef coral symbionts. Nature 430: Ro wa n R, Po w e r s DA (1991a) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251: Ro wa n R, Po w e r s DA (1991b) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Marine Ecology-Progress Series 71:65-73 Ro wa n R, Kn o w lt o n N (1995) Intraspecific diversity and ecological zonation in coral algal symbiosis. Proceedings of the National Academy of Sciences of the United States of America 92: Ro wa n R, Kn o w lt o n N, Ba k e r A, Ja r a J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388: Sa k a m o t o A, Mu r ata N (2002) The role of glycine betaine in the protection of plants from stress: Clues from transgenic plants. Plant, Cell & Environment 25: Sa l i h A, La r k u m A, Co x G, Ku h l M, Ho e g h-gu l d b e r g O (2000) Fluorescent pigments in corals are photoprotective. Nature 408: Sa m pay o EM, Do v e S, La j e u n e s s e TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Molecular Ecology 18: Sa m pay o EM, Fr a n c e s c h i n i s L, Ho e g h-gu l d b e r g O, Do v e S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Molecular Ecology 16: Sa m pay o EM, Ri d g way T, Bo n g a e rt s P, Ho e g h-gu l d b e r g O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proceedings of the National Academy of Sciences of the United States of America 105: Sa n d e m a n IM (2006) Fragmentation of the gastrodermis and detachment of zooxanthellae in symbiotic cnidarians: A role for hydrogen peroxide and Ca 2+ in coral bleaching and algal density control. International Journal of Tropical Biology and Conservation 54:79-96 Sa n t o d o m i n g o N, Reyes J, Gr a c i a A, Ma rt í n e z A, Oj e d a G, Ga r c í a C (2007) Azooxanthellate Madracis coral communities off San Bernardo and Rosario Islands (Colombian Caribbean). Bulletin of Marine Science 81: Sa n t o s SR, Co f f r o t h MA (2003) Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium Freudenthal are haploid. Biological Bulletin 204:10-20 Sa n t o s SR, Tay l o r DJ, Co f f r o t h MA (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis. Journal of Phycology 37: Sa n t o s SR, Gutierrez-Ro d r i g u e z C, Co f f r o t h MA (2003a) Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23s)- ribosomal DNA sequences. Marine Biotechnology 5: Sa n t o s SR, Gutierrez-Ro d r i g u e z C, La s k e r HR, Co f f r o t h MA (2003b) Symbiodinium sp associations in the gorgonian Pseudopterogorgia elisabethae in the Bahamas: High levels of genetic variability and population structure in symbiotic dinoflagellates. Marine Biology 143: Sa n t o s SR, Sh e a r e r TL, Ha n n e s AR, Co f f r o t h MA (2004) Fine-scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean. Molecular Ecology 13: Sa n t o s SR, Tay l o r DJ, Kinzie RA, Hi d a k a M, Sa k a i K, Co f f r o t h MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Molecular Phylogenetics and Evolution 23: Sc h a f e r H, Mu y z e r G (2001) Denaturing gradient gel electrophoresis in marine microbial ecology. Methods in Microbiology, Vol 30 30: