Microbial Ecology

, Volume 75, Issue 4, pp 903–915 | Cite as

Coral Symbiodinium Community Composition Across the Belize Mesoamerican Barrier Reef System is Influenced by Host Species and Thermal Variability

  • J. H. BaumannEmail author
  • S. W. Davies
  • H. E. Aichelman
  • K. D. Castillo
Environmental Microbiology


Reef-building corals maintain a symbiotic relationship with dinoflagellate algae of the genus Symbiodinium, and this symbiosis is vital for the survival of the coral holobiont. Symbiodinium community composition within the coral host has been shown to influence a coral’s ability to resist and recover from stress. A multitude of stressors including ocean warming, ocean acidification, and eutrophication have been linked to global scale decline in coral health and cover in recent decades. Three distinct thermal regimes (highTP, modTP, and lowTP) following an inshore-offshore gradient of declining average temperatures and thermal variation were identified on the Belize Mesoamerican Barrier Reef System (MBRS). Quantitative metabarcoding of the ITS-2 locus was employed to investigate differences and similarities in Symbiodinium genetic diversity of the Caribbean corals Siderastrea siderea, S. radians, and Pseudodiploria strigosa between the three thermal regimes. A total of ten Symbiodinium lineages were identified across the three coral host species. S. siderea was associated with distinct Symbiodinium communities; however, Symbiodinium communities of its congener, S. radians and P. strigosa, were more similar to one another. Thermal regime played a role in defining Symbiodinium communities in S. siderea but not S. radians or P. strigosa. Against expectations, Symbiodinium trenchii, a symbiont known to confer thermal tolerance, was dominant only in S. siderea at one sampled offshore site and was rare inshore, suggesting that coral thermal tolerance in more thermally variable inshore habitats is achieved through alternative mechanisms. Overall, thermal parameters alone were likely not the only primary drivers of Symbiodinium community composition, suggesting that environmental variables unrelated to temperature (i.e., light availability or nutrients) may play key roles in structuring coral-algal communities in Belize and that the relative importance of these environmental variables may vary by coral host species.


Coral Symbiodinium Symbiosis Marine science Environmental variability 



We thank J. Watkins, L. Speare, and A. Knowlton for laboratory assistance and C. Berger for assistance with coding. We also thank NASA JPL and NOAA ERDAAP for access to MUR SST data used in this paper, Belize Fisheries Department for issuing research and collection permits, and Garbutt’s Marine for providing local expert guides and boats for field research.

Funding information

This work was supported by the Rufford Foundation ( Small Grant to JHB (15802-1), the National Science Foundation (Oceanography) ( to KDC (OCE 1459522), and the Department of Defense NDSEG fellowship to JHB.

Compliance with Ethical Standards

Conflicts of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2017_1096_MOESM1_ESM.docx (111 kb)
ESM 1 (DOCX 110 kb)
248_2017_1096_MOESM2_ESM.tif (1.1 mb)
Fig. S1 MUR SST values for each sampling site from June 2014 - December 2014. The black horizontal line indicates the published bleaching threshold of 29.7°C for Belize (TIFF 1.13 mb)
248_2017_1096_Fig5_ESM.gif (182 kb)

High resolution image (GIF 181 kb)


  1. 1.
    Meyer FH (1966) Mycorrhiza and other plant symbioses. Symbiosis 1:171–255Google Scholar
  2. 2.
    Honegger R (1991) Functional aspects of the lichen symbiosis. Annu Rev Plant Biol 42:553–578CrossRefGoogle Scholar
  3. 3.
    Degnan PH, Lazarus AB, Brock CD, Wernegreen JJ (2004) Host–symbiont stability and fast evolutionary rates in an ant–bacterium association: cospeciation of Camponotus species and their endosymbionts, Candidatus Blochmannia. Syst Biol 53:95–110PubMedCrossRefGoogle Scholar
  4. 4.
    Brosi GB, McCulley RL, Bush LP, Nelson JA, Classen AT, Norby RJ (2011) Effects of multiple climate change factors on the tall fescue–fungal endophyte symbiosis: infection frequency and tissue chemistry. New Phytol 189:797–805PubMedCrossRefGoogle Scholar
  5. 5.
    Coles SL, Brown BE (2003) Coral bleaching-capacity for acclimatization and adaptation. Adv Mar Biol 46:183–213PubMedCrossRefGoogle Scholar
  6. 6.
    Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  7. 7.
    Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world 25: coral reefs. Elsevier, New York, pp. 75–87Google Scholar
  8. 8.
    DeSalvo MK, Sunagawa S, Fisher PL, Voolstra CR, IGLESIAS-PRIETO R, Medina M (2010) Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol Ecol 19:1174–1186PubMedCrossRefGoogle Scholar
  9. 9.
    Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plan Cell Environ 19:291–299CrossRefGoogle Scholar
  10. 10.
    Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17CrossRefGoogle Scholar
  11. 11.
    Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377PubMedCrossRefGoogle Scholar
  12. 12.
    Heron SF, Maynard JA, Ruben van Hooidonk C (2016) Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Scientific reports 6Google Scholar
  13. 13.
    Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933PubMedCrossRefGoogle Scholar
  14. 14.
    Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshwater Res 50:839–866CrossRefGoogle Scholar
  15. 15.
    Wild C, Hoegh-Guldberg O, Naumann MS, Colombo-Pallotta MF, Ateweberhan M, Fitt WK, Iglesias-Prieto R, Palmer C, Bythell JC, Ortiz J-C, Loya Y, van Woesik R (2011) Climate change impedes scleractinian corals as primary reef ecosystem engineers. Mar Freshw Res 62:205–215. CrossRefGoogle Scholar
  16. 16.
    Wooldridge S, Done T, Berkelmans R, Jones R, Marshall P (2005) Precursors for resilience in coral communities in a warming climate: a belief network approach. Mar Ecol Prog Ser 295:157–169CrossRefGoogle Scholar
  17. 17.
    Donner SD, Knutson TR, Oppenheimer M (2007) Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc Natl Acad Sci 104:5483–5488PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Donner SD, Skirving WJ, Little CM, Oppenheimer M, Hoegh-Guldberg O (2005) Global assessment of coral bleaching and required rates of adaptation under climate change. Glob Chang Biol 11:2251–2265CrossRefGoogle Scholar
  19. 19.
    Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162CrossRefGoogle Scholar
  20. 20.
    D'Croz L, Mate JL, Oke JE (2001) Responses to elevated seawater temperature and UV radiation in the coral Porites lobata from upwelling and non-upwelling environments on the Pacific coast of Panama. Bull Mar Sci 69:203–214Google Scholar
  21. 21.
    McWilliams JP, Cote IM, Gill JA, Sutherland WJ, Watkinson AR (2005) Accelerating impacts of temperature-induced coral bleaching in the Caribbean. Ecology 86:2055–2060CrossRefGoogle Scholar
  22. 22.
    Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K, Donner S, Hoegh-Guldberg O (2013) Limiting global warming to 2 °C is unlikely to save most coral reefs. Nat Clim Chang 3:165–170CrossRefGoogle Scholar
  23. 23.
    Chollett I, Müller-Karger FE, Heron SF, Skirving W, Mumby PJ (2012) Seasonal and spatial heterogeneity of recent sea surface temperature trends in the Caribbean Sea and southeast Gulf of Mexico. Mar. Pollut. Bull. 64:956–965PubMedCrossRefGoogle Scholar
  24. 24.
    Belkin IM (2009) Rapid warming of large marine ecosystems. Prog Oceanogr 81:207–213CrossRefGoogle Scholar
  25. 25.
    Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960PubMedCrossRefGoogle Scholar
  26. 26.
    Van Hooidonk R, Maynard JA, Liu Y, Lee SK (2015) Downscaled projections of Caribbean coral bleaching that can inform conservation planning. Global Change BiologyGoogle Scholar
  27. 27.
    Barshis DJ (2015) Genomic potential for coral survival of climate change coral reefs in the Anthropocene. Springer, pp. 133–146Google Scholar
  28. 28.
    Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211:1050–1056. PubMedCrossRefGoogle Scholar
  29. 29.
    Castillo KD, Helmuth BST (2005) Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure. Mar Biol 148:261–270CrossRefGoogle Scholar
  30. 30.
    Pineda J, Starczak V, Tarrant A, Blythe J, Davis K, Farrar T, Berumen M, da Silva JC (2013) Two spatial scales in a bleaching event: corals from the mildest and the most extreme thermal environments escape mortality. Limnol Oceanogr 58:1531–1545CrossRefGoogle Scholar
  31. 31.
    Castillo KD, Ries JB, Weiss JM, Lima FP (2012) Decline of forereef corals in response to recent warming linked to history of thermal exposure. Nat Clim Chang 2:756–760CrossRefGoogle Scholar
  32. 32.
    Oliver T, Palumbi S (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440CrossRefGoogle Scholar
  33. 33.
    Soto IM, Muller Karger FE, Hallock P, Hu C (2011) Sea surface temperature variability in the Florida keys and its relationship to coral cover. J Mar Biol 2011:10. CrossRefGoogle Scholar
  34. 34.
    Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV (2015) Genomic determinants of coral heat tolerance across latitudes. Science 348:1460–1462PubMedCrossRefGoogle Scholar
  35. 35.
    Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20PubMedCrossRefGoogle Scholar
  36. 36.
    Kenkel C, Meyer E, Matz M (2013) Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. Mol Ecol 22:4322–4334PubMedCrossRefGoogle Scholar
  37. 37.
    Kenkel C, Goodbody-Gringley G, Caillaud D, Davies S, Bartels E, Matz M (2013) Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol 22:4335–4348PubMedCrossRefGoogle Scholar
  38. 38.
    Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci 110:1387–1392PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269PubMedCrossRefGoogle Scholar
  40. 40.
    LaJeunesse TC, Smith R, Walthe M, Pinzon J, Pettay DT, McGinley M, Aschaffenfurg M, Medina-Rosas P, Cupul-Magana AL, Perez AL, Reyes-Bonilla H, and ME Warner (2010) Host-symbiont recombination vs. natural selection in response of coral-dinoflagellate symbioses to environmental disturbance. Proceedings of the Royal Society BGoogle Scholar
  41. 41.
    Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689CrossRefGoogle Scholar
  42. 42.
    Silverstein RN, Cunning R, Baker AC (2015) Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob Chang Biol 21:236–249PubMedCrossRefGoogle Scholar
  43. 43.
    Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR (2017) Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun 8:14213PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34PubMedCrossRefGoogle Scholar
  45. 45.
    LaJeunesse TC (2001) Investigating biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a ‘species’ level marker. J Phycol 37:866–880CrossRefGoogle Scholar
  46. 46.
    LaJeunesse T, Trench R (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134PubMedCrossRefGoogle Scholar
  47. 47.
    Silverstein RN, Cunning R, Baker AC (2017) Tenacious D: Symbiodinium in clade D remain in reef corals at both high and low temperature extremes despite impairment. J Exp Biol.
  48. 48.
    Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 430:741PubMedCrossRefGoogle Scholar
  49. 49.
    Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742PubMedCrossRefGoogle Scholar
  50. 50.
    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 101:13531–13535PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Berkelmans R, Van Oppen MJ (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc Lond B Biol Sci 273:2305–2312CrossRefGoogle Scholar
  52. 52.
    Hume BC, D'Angelo C, Smith EG, Stevens JR, Burt J, Wiedenmann J (2015) Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf. Sci Rep 5:8562PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Thornhill D, Howells E, Wham D, Steury T, Santos S (2017) Population genetics of reef coral endosymbionts (Symbiodinium, Dinophyceae). Molecular EcologyGoogle Scholar
  54. 54.
    Little AF, Van Oppen MJ, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494PubMedCrossRefGoogle Scholar
  55. 55.
    Thornhill DJ, Kemp DW, Bruns BU, Fitt WK, Schmidt GW (2008) Correspondence between cold tolerance and temperate biogeography in a Western Atlantic Symbiodinium (Dinophyta) Lineage. J Phycol 44:1126–1135PubMedCrossRefGoogle Scholar
  56. 56.
    Jones AM, Berkelmans R, van Oppen MJ, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc Lond B Biol Sci 275:1359–1365CrossRefGoogle Scholar
  57. 57.
    LaJeunesse TC, Smith RT, Finney J, Oxenford H (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. Proc R Soc Lond B Biol Sci 276:4139–4148CrossRefGoogle Scholar
  58. 58.
    Jones AM, Berkelmans R (2011) Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant Symbiodinium type-D. J Mar Biol 2011Google Scholar
  59. 59.
    Cunning R, Gillette P, Capo T, Galvez K, Baker AC (2015) Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs 34:155–160. CrossRefGoogle Scholar
  60. 60.
    Cantin NE, van Oppen MJ, Willis BL, Mieog JC, Negri AP (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405CrossRefGoogle Scholar
  61. 61.
    Kennedy EV, Foster NL, Mumby PJ, Stevens JR (2015) Widespread prevalence of cryptic Symbiodinium D in the key Caribbean reef builder, Orbicella annularis. Coral Reefs 34:519–531CrossRefGoogle Scholar
  62. 62.
    Diekmann O, Bak R, Tonk L, Stam W, Olsen J (2002) No habitat correlation of zooxanthellae in the coral genus Madracis on a Curacao reef. Mar Ecol Prog Ser 227:221–232CrossRefGoogle Scholar
  63. 63.
    Baker AC, Rowan R, Knowlton N (1997) Symbiosis ecology of two Caribbean Acroporid corals. In: Lessios, HA, Macintyre, IG (eds.) Proceedings of the 8th International Coral Reef Symposium, vol. 2, Panama, pp. 1296–1300Google Scholar
  64. 64.
    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 Biol Sci 279:2609–2618. CrossRefGoogle Scholar
  65. 65.
    Quigley KM, Davies SW, Kenkel CD, Willis BL, Matz MV, Bay LK (2014) Deep-sequencing method for quantifying background abundances of Symbiodinium types: exploring the rare Symbiodinium biosphere in reef-building corals. PLoS One 9:e94297PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Jones A, Berkelmans R (2010) Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS One 5:e10437. PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Correa AMS, McDonald MD, Baker AC (2009) Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Mar Biol 156:2403–2411. CrossRefGoogle Scholar
  69. 69.
    Lee MJ, Jeong HJ, Jang SH, Lee SY, Kang NS, Lee KH, Kim HS, Wham DC, LaJeunesse TC (2016) Most low-abundance “background” Symbiodinium spp. are transitory and have minimal functional significance for symbiotic corals. Microbial Ecology: 1–13Google Scholar
  70. 70.
    Garren M, Walsh SM, Caccone A, Knowlton N (2006) Patterns of association between Symbiodinium and members of the Montastraea annularis species complex on spatial scales ranging from within colonies to between geographic regions. Coral Reefs 25:503–512CrossRefGoogle Scholar
  71. 71.
    Kemp DW, Thornhill DJ, Rotjan RD, Iglesias-Prieto R, Fitt WK, Schmidt GW (2015) Spatially distinct and regionally endemic Symbiodinium assemblages in the threatened Caribbean reef-building coral Orbicella faveolata. Coral Reefs 34:535–547CrossRefGoogle Scholar
  72. 72.
    Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnol Oceanogr 51:1887–1897CrossRefGoogle Scholar
  73. 73.
    Green EA, Davies SW, Matz MV, Medina M (2014) Quantifying cryptic Symbiodinium diversity within Orbicella faveolata and Orbicella franksi at the Flower Garden Banks, Gulf of Mexico. PeerJ 2:e386PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Pettay DT, Wham DC, Smith RT, Iglesias-Prieto R, LaJeunesse TC (2015) Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc Natl Acad Sci 112:7513–7518PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Kennedy EV, Tonk L, Foster NL, Chollett I, Ortiz J-C, Dove S, Hoegh-Guldberg O, Mumby PJ, Stevens JR (2016) Symbiodinium biogeography tracks environmental patterns rather than host genetics in a key Caribbean reef-builder, Orbicella annularis. Proc R Soc B, vol. 283. The Royal Society, pp. 20161938Google Scholar
  76. 76.
    Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan K, Patterson M, Witcher B (2009) Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28:925CrossRefGoogle Scholar
  77. 77.
    Lirman D, Manzello D (2009) Patterns of resistance and resilience of the stress-tolerant coral Siderastrea radians (Pallas) to sub-optimal salinity and sediment burial. J Exp Mar Biol Ecol 369:72–77CrossRefGoogle Scholar
  78. 78.
    Lirman D, Fong P (2007) Is proximity to land-based sources of coral stressors an appropriate measure of risk to coral reefs? An example from the Florida Reef Tract. Mar Pollut Bull 54:779–791PubMedCrossRefGoogle Scholar
  79. 79.
    Lirman D, Manzello D, Maciá S (2002) Back from the dead: the resilience of Siderastrea radians to severe stress. Coral Reefs 21:291–292CrossRefGoogle Scholar
  80. 80.
    Castillo KD, Ries JB, Weiss JM (2011) Declining coral skeletal extension for forereef colonies of Siderastrea siderea on the Mesoamerican Barrier Reef System, Southern Belize. PLoS One 6:e14615PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Guzman HM, Tudhope AW (1998) Seasonal variation in skeletal extension rate and stable isotopic (13C/12C and 18O/16O) composition in response to several environmental variables in the Caribbean reef coral Siderastrea siderea. Mar Ecol Prog Ser 166:109–118CrossRefGoogle Scholar
  82. 82.
    Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Côté IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386PubMedCrossRefGoogle Scholar
  83. 83.
    Baumann JH, Townsend JE, Courtney TA, Aichelman HE, Davies SW, Lima FP, Castillo KD (2016) Temperature regimes impact coral assemblages along environmental gradients on lagoonal reefs in Belize. PLoS One 11:e0162098. PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Simons R (2011) ERDDAP—the Envionmental Research Division’s Data Access ProgramGoogle Scholar
  85. 85.
    Gleeson M, Strong A (1995) Applying MCSST to coral reef bleaching. Adv Space Res 16:151–154CrossRefGoogle Scholar
  86. 86.
    Aronson RB, Precht WF, Toscano MA, Koltes KH (2002) The 1998 bleaching event and its aftermath on a coral reef in Belize. Marine Biology xxxGoogle Scholar
  87. 87.
    Davies SW, Rahman M, Meyer E, Green EA, Buschiazzo E, Medina M, Matz MV (2013) Novel polymorphic microsatellite markers for population genetics of the endangered Caribbean star coral, Montastraea faveolata. Mar Biodivers 43:167–172CrossRefGoogle Scholar
  88. 88.
    Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction: twenty-something years on. Nat Protoc 1:581–585PubMedCrossRefGoogle Scholar
  89. 89.
    Stat M, Loh WKH, 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
  90. 90.
    Klepac CN, Beal J, Kenkel CD, Sproles A, Polinski JM, Williams MA, Matz MV, Voss JD (2015) Seasonal stability of coral-Symbiodinium associations in the subtropical coral habitat of St. Lucie Reef, Florida. Mar Ecol Prog Ser 532:137–151CrossRefGoogle Scholar
  91. 91.
    Li W, Fu L, Niu B, Wu S, Wooley J (2012) Ultrafast clustering algorithms for metagenomic sequence analysis. Briefings in bioinformatics: bbs035Google Scholar
  92. 92.
    Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  93. 93.
    Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321PubMedCrossRefGoogle Scholar
  94. 94.
    Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J-F, Guindon S, Lefort V, Lescot M (2008) robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465–W469PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Dereeper A, Audic S, Claverie J-M, Blanc G (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol. Biol. 10:8PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Chevenet F, Brun C, Bañuls A-L, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC bioinformatics 7:439PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Team RC (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  100. 100.
    Thornhill DJ, LaJeunesse TC, Santos SR (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16:5326–5340PubMedCrossRefGoogle Scholar
  101. 101.
    Matz MV, Wright RM, Scott JG (2013) No control genes required: Bayesian analysis of qRT-PCR data. PLoS One 8:e71448PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, Simpson GL, Solymos P, Stevens M, Wagner H (2013) Package ‘vegan’. R Packag ver 254:20–28Google Scholar
  103. 103.
    Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA and La Jeunesse TC (2010) On the relative significance of host-habitat, irradiance, and dispersal in the ecological distribution and speciation of coral endosymbionts. Microbial Ecology In PressGoogle Scholar
  104. 104.
    LaJeunesse TC, Loh WK, Van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054CrossRefGoogle Scholar
  105. 105.
    Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722CrossRefGoogle Scholar
  106. 106.
    Thornhill DJ, Xiang Y, Fitt WK, Santos SR (2009) Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS One 4:e6262PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Van Oppen M, Mieog J, Sanchez C, Fabricius K (2005) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14:2403–2417PubMedCrossRefGoogle Scholar
  108. 108.
    Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078CrossRefGoogle Scholar
  109. 109.
    Stat M, Yost DM, Gates RD (2015) Geographic structure and host specificity shape the community composition of symbiotic dinoflagellates in corals from the Northwestern Hawaiian Islands. Coral Reefs 34:1075–1086CrossRefGoogle Scholar
  110. 110.
    LaJeunesse TC, Lee S, Bush S, Bruno JF (2005) Persistence of non-Caribbean algal symbionts in Indo-Pacific mushroom corals released to Jamaica 35 years ago. Coral Reefs 24:157–159CrossRefGoogle Scholar
  111. 111.
    Santos S, Shearer T, Hannes A, Coffroth M (2004) Fine-scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean. Mol Ecol 13:459–469PubMedCrossRefGoogle Scholar
  112. 112.
    Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJ, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS One 5:e10871PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Tong H, Cai L, Zhou G, Yuan T, Zhang W, Tian R, Huang H, Qian P-Y (2017) Temperature shapes coral-algal symbiosis in the South China Sea. Sci Rep 7:40118. PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326CrossRefGoogle Scholar
  115. 115.
    Glynn PW, Mate JL, Baker AC, Calderon MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997-1998 El Nino Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982-1983 event. Bull Mar Sci 69:79–109Google Scholar
  116. 116.
    Frade P, Englebert N, Faria J, Visser P, Bak R (2008) 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 27:913–925CrossRefGoogle Scholar
  117. 117.
    Ulstrup KE, Ralph PJ, Larkum AWD, Kuhl M (2006) Intra-colonial variability in light acclimation of zooxanthellae in coral tissues of Pocillopora damicornis. Mar Biol 149:1325–1335CrossRefGoogle Scholar
  118. 118.
    Ulstrup KE, Van Oppen M (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12:3477–3484PubMedCrossRefGoogle Scholar
  119. 119.
    Toller WW, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull 201:360–373PubMedCrossRefGoogle Scholar
  120. 120.
    Hennige SJ, Smith DJ, Walsh S-J, McGinley MP, Warner ME, Suggett DJ (2010) Acclimation and adaptation of scleractinian coral communities along environmental gradients within an Indonesian reef system. J Exp Mar Biol Ecol 391:143–152. CrossRefGoogle Scholar
  121. 121.
    Abrego D, Van Oppen MJ, Willis BL (2009) Highly infectious symbiont dominates initial uptake in coral juveniles. Mol Ecol 18:3518–3531PubMedCrossRefGoogle Scholar
  122. 122.
    Fabricius K, Mieog J, Colin P, Idip D, H VAN OPPEN M (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13:2445–2458PubMedCrossRefGoogle Scholar
  123. 123.
    LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800CrossRefGoogle Scholar
  124. 124.
    Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766PubMedCrossRefGoogle Scholar
  125. 125.
    LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia 53:305–319CrossRefGoogle Scholar
  126. 126.
    Carilli JE, Norris RD, Black BA, Walsh SM, McField M (2009) Local stressors reduce coral resilience to bleaching. PLoS One 4:e6324PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Paris CB, Cherubin LM (2008) River-reef connectivity in the Meso-American region. Coral Reefs 27:773–781CrossRefGoogle Scholar
  128. 128.
    Carilli JE, Prouty NG, Hughen KA, Norris RD (2009) Century-scale records of land-based activities recorded in Mesoamerican coral cores. Mar Pollut Bull 58:1835–1842PubMedCrossRefGoogle Scholar
  129. 129.
    Howells EJ, Berkelmans R, van Oppen MJ, Willis BL, Bay LK (2013) Historical thermal regimes define limits to coral acclimatization. Ecology 94:1078–1088PubMedCrossRefGoogle Scholar
  130. 130.
    Howells E, Beltran V, Larsen N, Bay L, Willis B, Van Oppen M (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120CrossRefGoogle Scholar
  131. 131.
    Hume BC, Voolstra CR, Arif C, D’Angelo C, Burt JA, Eyal G, Loya Y, Wiedenmann J (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc Natl Acad Sci 113:4416–4421PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Department of Marine SciencesUniversity of North Carolina at Chapel HillChapel HillUSA
  2. 2.Department of BiologyBoston UniversityBostonUSA
  3. 3.Department of Biological SciencesOld Dominion UniversityNorfolkUSA

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