Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res. 1999;50:839–66.
Hoegh-Guldberg O, Poloczanska ES, Skirving W, Dove S. Coral reef ecosystems under climate change and ocean acidification. Front Mar Sci. 2017;4:158.
Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, Matz MV. Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol. 2013;22:4335–48.
Bay RA, Palumbi SR. Multilocus adaptation associated with heat resistance in reef-building corals. Curr Biol. 2014;24:2952–6.
Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV. Genomic determinants of coral heat tolerance across latitudes. Science. 2015;348:1460.
Howells EJ, Abrego D, Meyer E, Kirk NL, Burt JA. Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob Change Biol. 2016;22:2702–14.
Morikawa MK, Palumbi SR. Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proc Natl Acad Sci USA. 2019;116:10586.
Berkelmans R, van Oppen MJH. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc Biol Sci. 2006;273:2305–12.
Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci USA. 2008;105:10444.
LaJeunesse TC, Smith RT, Finney J, Oxenford H. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. Proc R Soc B: Biol Sci. 2009;276:4139–48.
Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Change. 2011;2:116.
LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol. 2018;28:2570–.e6.
Bellantuono AJ, Granados-Cifuentes C, Miller DJ, Hoegh-Guldberg O, Rodriguez-Lanetty M. Coral thermal tolerance: tuning gene expression to resist thermal stress. PLoS ONE. 2012;7:e50685.
Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA. Mechanisms of reef coral resistance to future climate change. Science. 2014;344:895.
Sawall Y, Al-Sofyani A, Hohn S, Banguera-Hinestroza E, Voolstra CR, Wahl M. Extensive phenotypic plasticity of a Red Sea coral over a strong latitudinal temperature gradient suggests limited acclimatization potential to warming. Sci Rep. 2015;5:8940.
Torda G, Donelson JM, Aranda M, Barshis DJ, Bay L, Berumen ML, et al. Rapid adaptive responses to climate change in corals. Nat Clim Change. 2017;7:627.
Baker AC. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol, Evolution, Syst. 2003;34:661–89.
Boulotte NM, Dalton SJ, Carroll AG, Harrison PL, Putnam HM, Peplow LM, et al. Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J. 2016;10:2693–701.
Cunning R, Silverstein RN, Baker AC. Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals. Coral Reefs. 2018;37:145–52.
Stat M, Loh WKW, LaJeunesse TC, Hoegh-Guldberg O, Carter DA. Stability of coral–endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs. 2009;28:709–13.
Putnam HM, Stat M, Pochon X, Gates RG. Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc R Soc B: Biol Sci. 2012;279:4352–61.
Stat M, Morris E, Gates RD. Functional diversity in coral–dinoflagellate symbiosis. Proc Natl Acad Sci USA. 2008;105:9256.
Starzak DE, Quinnell RG, Nitschke MR, Davy SK. The influence of symbiont type on photosynthetic carbon flux in a model cnidarian–dinoflagellate symbiosis. Mar Biol. 2014;161:711–24.
Gabay Y, Weis VM, Davy SK. Symbiont identity influences patterns of symbiosis establishment, host growth, and asexual reproduction in a model cnidarian-dinoflagellate symbiosis. Biol Bull. 2018;234:1–10.
Quigley KM, Bay LK, Willis BL. Temperature and water quality-related patterns in sediment-associated Symbiodinium communities impact symbiont uptake and fitness of juveniles in the genus acropora. Front Mar Sci. 2017;4:401.
Cumbo VR, vanOppen MJH, Baird AH. Temperature and Symbiodinium physiology affect the establishment and development of symbiosis in corals. Mar Ecol Prog Ser. 2018;587:117–27.
Ali A, Kriefall NG, Emery LE, Kenkel CD, Matz MV, Davies SW. Recruit symbiosis establishment and Symbiodiniaceae composition influenced by adult corals and reef sediment. Coral Reefs. 2019;38:405–15.
McIlroy SE, Cunning R, Baker AC, Coffroth MA. Competition and succession among coral endosymbionts. Ecol Evolution. 2019;9:12767–78.
Abrego D, Willis BL, van Oppen MJH. Impact of light and temperature on the uptake of algal symbionts by coral juveniles. PLoS ONE. 2012;7:e50311.
Schnitzler CE, Hollingsworth LL, Krupp DA, Weis VM. Elevated temperature impairs onset of symbiosis and reduces survivorship in larvae of the Hawaiian coral, Fungia scutaria. Mar Biol. 2012;159:633–42.
Hawkins TD, Hagemeyer JCG, Warner ME. Temperature moderates the infectiousness of two conspecific Symbiodinium strains isolated from the same host population. Environ Microbiol. 2016;18:5204–17.
Swain TD, Chandler J, Backman V, Marcelino L. Consensus thermotolerance ranking for 110 Symbiodinium phylotypes: an exemplar utilization of a novel iterative partial-rank aggregation tool with broad application potential. Funct Ecol. 2017;31:172–83.
Gabay Y, Parkinson JE, Wilkinson SP, Weis VM, Davy SK. Inter-partner specificity limits the acquisition of thermotolerant symbionts in a model cnidarian-dinoflagellate symbiosis. ISME J. 2019;13:2489–99.
Poland DM, Coffroth MA. Trans-generational specificity within a cnidarian–algal symbiosis. Coral Reefs. 2017;36:119–29.
Fraune S, Bosch TCG. Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci USA. 2007;104:13146.
Herrera M, Ziegler M, Voolstra CR, Aranda M. Laboratory-cultured strains of the sea anemone exaiptasia reveal distinct bacterial communities. Front Mar Sci. 2017;4:115.
Grajales A, Rodríguez E. Morphological revision of the genus Aiptasia and the family Aiptasiidae (Cnidaria, Actinaria, Metridioidea). Zootaxa. 2014;3826:55–100.
Xiang T, Hambleton EA, DeNofrio JC, Pringle JR, Grossman AR. Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity. J Phycol. 2013;49:447–58.
Bieri T, Onishi M, Xiang T, Grossman AR, Pringle JR. Relative contributions of various cellular mechanisms to loss of algae during cnidarian bleaching. PLoS ONE. 2016;11:e0152693.
Sunagawa S, Wilson EC, Thaler M, Smith ML, Caruso C, Pringle JR, et al. Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics. 2009;10:258.
Cziesielski MJ, Liew YJ, Cui G, Schmidt-Roach S, Campana S, Marondedze C, et al. Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts. Proc Biol Sci. 2018;285:20172654.
Belda-Baillie CA, Baillie BK, Maruyama T. Specificity of a model cnidarian-dinoflagellate symbiosis. Biol Bull. 2002;202:74–85.
Rodriguez-Lanetty M, Chang S-J, Song J-I. Specificity of two temperate dinoflagellate–anthozoan associations from the north-western Pacific Ocean. Mar Biol. 2003;143:1193–9.
Cziesielski MJ, Schmidt-Roach S, Aranda M. The past, present, and future of coral heat stress studies. Ecol Evolution. 2019;9:10055–66.
Lehnert EM, Mouchka ME, Burriesci MS, Gallo ND, Schwarz JA, Pringle JR. Extensive differences in gene expression between symbiotic and aposymbiotic cnidarians. G3 (Bethesda). 2014;4:277–95.
Gegner HM, Ziegler M, Rädecker N, Buitrago-López C, Aranda M, Voolstra CR. High salinity conveys thermotolerance in the coral model Aiptasia. Biol Open. 2017;6:1943.
Cui G, Liew YJ, Li Y, Kharbatia N, Zahran NI, Emwas A-H, et al. Host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia. PLoS Genet. 2019;15:e1008189.
Röthig T, Costa RM, Simona F, Baumgarten S, Torres AF, Radhakrishnan A, et al. Distinct bacterial communities associated with the coral model aiptasia in aposymbiotic and symbiotic states with symbiodinium. Front Mar Sci. 2016;3:234.
Matthews JL, Sproles AE, Oakley CA, Grossman AR, Weis VM, Davy SK. Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones (Aiptasia sp.) for symbiosis investigations. J Exp Biol. 2016;219:306.
Hume BCC, Ziegler M, Poulain J, Pochon X, Romac S, Boissin E, et al. An improved primer set and amplification protocol with increased specificity and sensitivity targeting the Symbiodinium ITS2 region. PeerJ. 2018;6:e4816.
Hume BCC, Smith EG, Ziegler M, Warrington HJM, Burt JA, LaJeunesse TC, et al. SymPortal: a novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol Ecol Resour. 2019;19:1063–80.
R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing; 2018.
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Community Ecology Package. 2019.
Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26:32–46.
Anderson MJ. Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online. American Cancer Society; 2017. p. 1–15.
Anderson MJ, Willis TJ. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology. 2003;84:511–25.
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
IBM SPSS Statistics (Version 22.0). Armonk, NY, USA: IBM Corporation; 2013.
Robison JD, Warner ME. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol. 2006;42:568–79.
McGinty ES, Pieczonka J, Mydlarz LD. Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol. 2012;64:1000–7.
Grégoire V, Schmacka F, Coffroth MA, Karsten U. Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). J Appl Phycol. 2017;29:1893–905.
Lesser MP. Phylogenetic signature of light and thermal stress for the endosymbiotic dinoflagellates of corals (Family Symbiodiniaceae). Limnol Oceanogr. 2019;64:1852–63.
Hambleton EA, Guse A, Pringle JR. Similar specificities of symbiont uptake by adults and larvae in an anemone model system for coral biology. J Exp Biol. 2014;217:1613.
Wolfowicz I, Baumgarten S, Voss PA, Hambleton EA, Voolstra CR, Hatta M, et al. Aiptasia sp. larvae as a model to reveal mechanisms of symbiont selection in cnidarians. Sci Rep. 2016;6:32366.
Thornhill DJ, Xiang Y, Pettay DT, Zhong M, Santos SR. Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol. 2013;22:4499–515.
Little AF, van Oppen MJH, Willis BL. Flexibility in algal endosymbioses shapes growth in reef corals. Science. 2004;304:1492.
Pettay DT, Wham DC, Smith RT, Iglesias-Prieto R, LaJeunesse TC. Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc Natl Acad Sci USA. 2015;112:7513.
Baums IB, Devlin-Durante MK, LaJeunesse TC. New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies. Mol Ecol. 2014;23:4203–15.
Nyamukondiwa C, Terblanche JS. Thermal tolerance in adult Mediterranean and Natal fruit flies (Ceratitis capitata and Ceratitis rosa): effects of age, gender and feeding status. J Therm Biol. 2009;34:406–14.
Dowd WW, King FA, Denny MW. Thermal variation, thermal extremes and the physiological performance of individuals. J Exp Biol. 2015;218:1956.
Chidawanyika F, Nyamukondiwa C, Strathie L, Fischer K. Effects of thermal regimes, starvation and age on heat tolerance of the Parthenium Beetle Zygogramma bicolorata (Coleoptera: Chrysomelidae) following dynamic and static protocols. PLoS ONE. 2017;12:e0169371.
Hoadley KD, Lewis AM, Wham DC, Pettay DT, Grasso C, Smith R, et al. Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Sci Rep. 2019;9:9985.
Rädecker N, Raina J-B, Pernice M, Perna G, Guagliardo P, Kilburn MR, et al. Using aiptasia as a model to study metabolic interactions in cnidarian-symbiodinium symbioses. Front Physiol. 2018;9:214–214.
Osman EO, Smith DJ, Ziegler M, Kürten B, Conrad C, El-Haddad KM, et al. Thermal refugia against coral bleaching throughout the northern Red Sea. Glob Change Biol. 2018;24:e474–84.
Berumen ML, Voolstra CR, Daffonchio D, Agusti S, Aranda M, Irigoien X, et al. The Red Sea: environmental gradients shape a natural laboratory in a nascent ocean. In: Voolstra CR, Berumen ML, editors. Coral Reefs of the Red Sea. Cham: Springer International Publishing; 2019. p. 1–10.
Hawkins TD, Hagemeyer JCG, Hoadley KD, Marsh AG, Warner ME. Partitioning of respiration in an animal-algal symbiosis: implications for different aerobic capacity between Symbiodinium spp. Front Physiol. 2016;7:128.
Hoadley KD, Rollison D, Pettay DT, Warner ME. Differential carbon utilization and asexual reproduction under elevated pCO2 conditions in the model anemone, Exaiptasia pallida, hosting different symbionts. Limnol Oceanogr. 2015;60:2108–20.
Borell EM, Yuliantri AR, Bischof K, Richter C. The effect of heterotrophy on photosynthesis and tissue composition of two scleractinian corals under elevated temperature. J Exp Mar Biol Ecol. 2008;364:116–23.
Ferrier-Pagès C, Rottier C, Beraud E, Levy O. Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: effect on the rates of photosynthesis. J Exp Mar Biol Ecol. 2010;390:118–24.
Connolly SR, Lopez-Yglesias MA, Anthony KRN. Food availability promotes rapid recovery from thermal stress in a scleractinian coral. Coral Reefs. 2012;31:951–60.
Lyndby NH, Holm JB, Wangpraseurt D, Grover R, Rottier C, Kühl M, et al. Effect of feeding and thermal stress on photosynthesis, respiration and the carbon budget of the scleractinian coral Pocillopora damicornis. bioRxiv. 2018:378059.
Borell EM, Bischof K. Feeding sustains photosynthetic quantum yield of a scleractinian coral during thermal stress. Oecologia. 2008;157:593.
Weng L-C, Pasaribu B, Ping Lin I, Tsai C-H, Chen C-S, Jiang P-L. Nitrogen deprivation induces lipid droplet accumulation and alters fatty acid metabolism in symbiotic dinoflagellates isolated from aiptasia pulchella. Sci Rep. 2014;4:5777.
Fitt W, Cook C. The effects of feeding or addition of dissolved inorganic nutrients in maintaining the symbiosis between dinoflagellates and a tropical marine cnidarian. Mar Biol. 2001;139:507–17.
Ferrier-Pagès C, Witting J, Tambutté E, Sebens KP. Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs. 2003;22:229–40.
van der Merwe R, Röthig T, Voolstra CR, Ochsenkühn MA, Lattemann S, Amy GL. High salinity tolerance of the Red Sea coral Fungia granulosa under desalination concentrate discharge conditions: an in situ photophysiology experiment. Front Mar Sci. 2014;1:58.
Source: Ecology - nature.com