Bleaching Resistance and the Role of Algal Endosymbionts

  • K. M. QuigleyEmail author
  • A. C. Baker
  • M. A. Coffroth
  • B. L. Willis
  • M. J. H. van Oppen
Part of the Ecological Studies book series (ECOLSTUD, volume 233)


Coral reefs are among the most diverse and ecologically important biomes on the planet. Most coral species rely on the partnership with dinoflagellates of the genus Symbiodinium for survival due to an obligate nutritional symbiosis. Although this symbiosis has been studied for years, only recently has the taxonomic and functional richness of this genus begun to be explored with the advent of molecular techniques. This chapter reviews the taxonomic, physiological and biogeographic diversity of Symbiodinium and examines how changes in the relative abundance and/or acquisition of different Symbiodinium taxa may or may not provide an avenue for the coral host to acclimate or adapt to changing environmental conditions. Fundamental shifts in our knowledge concerning Symbiodinium diversity and host specificity are also addressed.



This work was funded by NSF grants to A.C.B. (OCE-1358699 and OCE-1447306) and M.A.C. (OCE-04-24996 and OCE-09-26822) and funding through the ARC CoE for Coral Reef Studies to B.L.W. (CE140100020).


  1. Abrego D, Ulstrup KE, Willis BL, van Oppen MJH (2008) Species–specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc B 275:2273–2282. Scholar
  2. Abrego D, van Oppen MJH, Willis BL (2009a) Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Mol Ecol 18:3532–3543. Scholar
  3. Abrego D, van Oppen MJH, Willis BL (2009b) Highly infectious symbiont dominates initial uptake in coral juveniles. Mol Ecol 18:3518–3531. Scholar
  4. Abrego D, Willis BL, van Oppen MJH (2012) Impact of light and temperature on the uptake of algal symbionts by coral juveniles. PLoS One 7.
  5. Andras JP, Kirk NL, Harvell CD (2011) Range-wide population genetic structure of Symbiodinium associated with the Caribbean sea fan coral, Gorgonia ventalina. Mol Ecol 20:2525–2542. Scholar
  6. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105:17442–17446. Scholar
  7. Anthony K, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–550. Scholar
  8. Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC et al (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep 6.
  9. Arif C, Daniels C, Bayer T, Hinestroza E, Barbrook A, Howe CJ et al (2014) Assessing Symbiodinium diversity in scleractinian corals via Next Generation Sequencing based genotyping of the ITS2 rDNA region. Mol Ecol 23:4418–4433. Scholar
  10. Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116. Scholar
  11. Baillie BK, Belda-Baillie CA, Maruyama T (2000a) Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. J Phycol 36:1153–1161. Scholar
  12. Baillie BK, Belda-Baillie CA, Silvestre V, Sison M, Gomez A, Gomez E et al (2000b) Genetic variation in Symbiodinium isolates from giant clams based on random-amplified-polymorphic DNA (RAPD) patterns. Mar Biol 136:829–836. Scholar
  13. Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009a) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20. Scholar
  14. Baird AH, Guest JR, Willis BL (2009b) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571. Scholar
  15. Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766. Scholar
  16. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689. Scholar
  17. Baker AC, Cunning R (2016) Coral “bleaching” as a generalized stress response to environmental disturbance. In: Woodley CM, Downs CA, Bruckner AW, Porter JW, Galloway SB (eds) Diseases of coral. Wiley pp 396–409CrossRefGoogle Scholar
  18. Baker AC, Romanski AM (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: comment on Goulet (2006). Mar Ecol Prog Ser 335:237–242. Scholar
  19. Baker AC, Rowan R (1997) Diversity of symbiotic dinoflagellates (zooxanthellae) in scleractinian corals of the Caribbean and eastern Pacific. In: Proceedings of the 8th international coral reef symposium, Panama, pp 1301–1305Google Scholar
  20. Baker AC, Rowan R, Knowlton N (1997) Symbiosis ecology of two Caribbean acroporid corals. In: Proceedings of the 8th international coral reef symposium, Panama, pp 1295–1300Google Scholar
  21. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004a) Coral reefs: corals’ adaptive response to climate change. Nature 430:741. Scholar
  22. Baker AC, Jones SH, Lee TS, Abuzinada AH, Joubert E, Krupp F (2004b) Symbiont diversity in Arabian corals and its relation to patterns of contemporary and historical environmental stress. In: Abuzinada AH, Jouberte E, Krupp F (eds) Proceedings of the international symposium on the extent and impact of coral bleaching in the Arabian Region. National Commission for Wildlife Conservation and Development, Riyadh, pp 24–36Google Scholar
  23. Banaszak AT, LaJeunesse TC, Trench RK (2000) The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. J Exp Mar Biol Ecol 249:219–233. Scholar
  24. Banaszak AT, Santos MB, LaJeunesse TC, Lesser MP (2006) The distribution of mycosporine-like amino acids (MAAs) and the phylogenetic identity of symbiotic dinoflagellates in cnidarian hosts from the Mexican Caribbean. J Exp Mar Biol Ecol 337:131–146. Scholar
  25. Barbrook AC, Visram S, Douglas AE, Howe CJ (2006) Molecular diversity of dinoflagellate symbionts of Cnidaria: the psbA minicircle of Symbiodinium. Protist 157:159–171. Scholar
  26. Barbrook AC, Voolstra CR, Howe CJ (2014) The chloroplast genome of a Symbiodinium sp. clade C3 isolate. Protist 165:1–13. Scholar
  27. Barneah O, Weis VM, Perez S, Benayahu Y (2004) Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition matters. Mar Ecol Prog Ser 275:89–95. Scholar
  28. Barnes DJ, Chalker BE (1990) Calcification and photosynthesis in reef-building corals and algae. In: Dubinsky Z (ed) Coral Reefs. Ecosystems of the World 25. Elsevier, pp 109–131Google Scholar
  29. 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 U S A 110:1387–1392. Scholar
  30. Baums IB, Devlin-Durante MK, LaJeunesse TC (2014) New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies. Mol Ecol 23:4203–4215. Scholar
  31. Bay LK, Cumbo VR, Abrego D, Kool JT, Ainsworth TD, Willis BL (2011) Infection dynamics vary between Symbiodinium types and cell surface treatments during establishment of endosymbiosis with coral larvae. Diversity 3:356–374. Scholar
  32. Bay LK, Doyle J, Logan M, Berkelmans R (2016) Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral. Roy Soc Open Sci 3. Scholar
  33. Berkelmans R, van 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. Proc R Soc B 273:2305–2312. Scholar
  34. Bhagooli R, Hidaka M (2003) Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species. J Exp Mar Biol Ecol 291:181–197. Scholar
  35. Bieri T, Onishi M, Xiang T, Grossman AR, Pringle JR (2016) Relative contributions of various cellular mechanisms to loss of algae during cnidarian bleaching. PLoS One 11.
  36. Blank RJ, Huss VA (1989) DNA divergency and speciation in Symbiodinium (Dinophyceae). Plant Syst Evol 163:153–163. Scholar
  37. Blank RJ, Trench RK (1985) Speciation and symbiotic dinoflagellates. Science 229:656–659. Scholar
  38. Blank RJ, Trench RK (1986) Nomenclature of endosymbiotic dinoflagellates. Taxon 35:286–294. Scholar
  39. Bo M, Baker AC, Gaino E, Wirshing HH, Scoccia F, Bavestrello G (2011) First description of algal mutualistic endosymbiosis in a black coral (Anthozoa: Antipatharia). Mar Ecol Prog Ser 435:1–11. Scholar
  40. Boldt L, Yellowlees D, Leggat W (2008) Measuring Symbiodinium sp. gene expression patterns with quantitative real-time PCR. Proceedings of the 11th international coral reef symposium, Fort Lauderdale, pp 118–122Google Scholar
  41. Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N et al (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS One 5. Scholar
  42. Bongaerts P, Frade PR, Hay KB, Englebert N, Latijnhouwers KRW, Bak RPM et al (2015a) Deep down on a Caribbean reef: lower mesophotic depths harbor a specialized coral-endosymbiont community. Sci Rep 5.
  43. Bongaerts P, Carmichael M, Hay KB, Tonk L, Frade PR, Hoegh-Guldberg O (2015b) Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. Roy Soc Open Sci 2.
  44. Boulotte NM, Dalton SJ, Carroll AG, Harrison PL, Putnam HM, Peplow LM et al (2016) Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J 10:2693–2701. Scholar
  45. Brazeau DA, Lasker HR (1990) Sexual reproduction and external brooding by the Caribbean gorgonian Briareum asbestinum. Mar Biol 104:465–474. Scholar
  46. Brown BB, Dunne RD, Goodson MG, Douglas AD (2002) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21:119–126. Scholar
  47. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326. Scholar
  48. Buddemeier RW, Smith SV (1999) Coral adaptation and acclimatization: a most ingenious paradox. Am Zool 39:1–9CrossRefGoogle Scholar
  49. Buddemeier RW, Baker AC, Fautin DG, Jacobs JR (2004) The adaptive hypothesis of bleaching. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 427–444CrossRefGoogle Scholar
  50. Burnett WJ (2002) Longitudinal variation in algal symbionts (zooxanthellae) from the Indian Ocean zoanthid Palythoa caesia. Mar Ecol Prog Ser 234:105–109. Scholar
  51. Byler KA, Carmi-Veal M, Fine M, Goulet TL (2013) Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. PLoS One 8. Scholar
  52. Cantin N, van Oppen MJH, Willis B, Mieog J, Negri A (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405–414. Scholar
  53. Carlos AA, Baillie BK, Kawachi M, Maruyama T (1999) Phylogenetic position of Symbiodinium (Dinophyceae) isolates from Tridacnids (Bivalvia), Cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. J Phycol 35:1054–1062. Scholar
  54. Chakravarti LJ, Beltran VH, Oppen MJH (2017) Rapid thermal adaptation in photosymbionts of reef-building corals. Glob Chang Biol 23:4675–4688. Scholar
  55. Chen CA, Lam KK, Nakano Y, Tsai W-S (2003) A stable association of the stress-tolerant zooxanthellae, Symbiodinium clade D, with the low-temperature-tolerant coral, Oulastrea crispata (Scleractinia: Faviidae) in subtropical non-reefal coral communities. Zool Stud 42:540–550Google Scholar
  56. Chen CA, Wang AT, Fang LS, Yang YW (2005) Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Mar Ecol Prog Ser 295:113–121. Scholar
  57. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34. Scholar
  58. Coffroth MA, Santos S, Goulet T (2001) Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Mar Ecol Prog Ser 222:85–96. Scholar
  59. Coffroth MA, Lewis CF, Santos SR, Weaver JL (2006) Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr Biol 16:R985–R987. Scholar
  60. Coffroth MA, Poland DM, Petrou EL, Brazeau DA, Holmberg JC (2010) Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLoS One 5.
  61. Cooper TF, Berkelmans R, Ulstrup KE, Weeks S, Radford B, Jones AM et al (2011) Environmental factors controlling the distribution of Symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef. PLoS One 6.
  62. Correa A, McDonald M, Baker A (2009) Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade symbionts in Caribbean corals. Mar Biol 156:2403–2411. Scholar
  63. Császár NBM, Ralph PJ, Frankham R, Berkelmans R, van Oppen MJH (2010) Estimating the potential for adaptation of corals to climate warming. PLoS One 5.
  64. Cumbo VR, Baird AH, van Oppen MJH (2013) The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32:111–120. Scholar
  65. Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:259–262. Scholar
  66. Cunning R, Gillette P, Capo T, Galvez K, Baker AC (2015a) Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs 34:155–160. Scholar
  67. Cunning R, Silverstein RN, Baker AC (2015b) Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc R Soc B 282.
  68. Cunning R, Yost DM, Guarinello ML, Putnam HM, Gates RD (2015c) Variability of Symbiodinium communities in waters, sediments, and corals of thermally distinct reef pools in American Samoa. PLoS One 10.
  69. Cunning R, Silverstein RN, Baker AC (2017a) Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals. Coral Reefs.
  70. Cunning R, Gates RD, Edmunds PJ (2017b) Using high-throughput sequencing of ITS2 to describe Symbiodinium metacommunities in St. John, US Virgin Islands. PeerJ 5.
  71. Davies SW, Wham DC, Kanke MR, Matz MV (2016) Ecological factors rather than physical barriers to dispersal shape genetic structure of algal symbionts in horizontally-transmitting corals. bioRxiv.
  72. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261. Scholar
  73. DeBoer TS, Baker AC, Erdmann MV, Ambariyanto, Jones PR, Barber PH (2012) Patterns of Symbiodinium distribution in three giant clam species across the biodiverse Bird’s Head region of Indonesia. Mar Ecol Prog Ser 444:117–132. Scholar
  74. del C Gómez-Cabrera M, Ortiz JC, WKW L, Ward S, Hoegh-Guldberg O (2008) Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus. Coral Reefs 27:219–226. Scholar
  75. Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV (2015) Genomic determinants of coral heat tolerance across latitudes. Science 348:1460–1462. Scholar
  76. Dunn SR, Weis VM (2009) Apoptosis as a post-phagocytic winnowing mechanism in a coral–dinoflagellate mutualism. Environ Microbiol 11:268–276. Scholar
  77. Fabina NS, Putnam HM, Franklin EC, Stat M, Gates RD (2012) Transmission mode predicts specificity and interaction patterns in coral-Symbiodinium networks. PLoS One 7. Scholar
  78. Fabina NS, Putnam HM, Franklin EC, Stat M, Gates RD (2013) Symbiotic specificity, association patterns, and function determine community responses to global changes: defining critical research areas for coral Symbiodinium symbioses. Glob Chang Biol 19:3306–3316. Scholar
  79. Fabricius KE, Klumpp DW (1995) Widespread mixotrophy in reef-inhabiting soft corals: the influence of depth, and colony expansion and contraction on photosynthesis. Mar Ecol Prog Ser 125:195–204. Scholar
  80. Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13:2445–2458. Scholar
  81. Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals. Coral Reefs 2:129–150. Scholar
  82. Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, LaJeunesse TC (2010) The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 60:250–263. Scholar
  83. FitzPatrick SK, Liberatore KL, Garcia JR, Burghardt I, Colman DR, Moquin SA et al (2012) Symbiodinium diversity in the soft coral Heteroxenia sp. and its nudibranch predator Phyllodesmium lizardensis. Coral Reefs 31:895–905. Scholar
  84. Frade PR, De Jongh F, Vermeulen F, van Bleijswijk J, Bak RPM (2008) Variation in symbiont distribution between closely related coral species over large depth ranges. Mol Ecol 17:691–703. Scholar
  85. Frank U, Oren U, Loya Y, Rinkevich B (1997) Alloimmune maturation in the coral Stylophora pistillata is achieved through three distinctive stages, 4 months post–metamorphosis. Proc R Soc B 264:99–104. Scholar
  86. Franklin EC, Stat M, Pochon X, Putnam HM, Gates RD (2012) GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium-host symbioses. Mol Ecol Resour 12:369–373. Scholar
  87. Franzenburg S, Walter J, Künzel S, Wang J, Baines JF, Bosch TCG et al (2013) Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc Natl Acad Sci U S A 110:E3730–E3738. Scholar
  88. Freudenthal H (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J Eukaryot Microbiol 9:45–52. Scholar
  89. Gierz SL, Forêt S, Leggat W (2017) Transcriptomic analysis of thermally stressed Symbiodinium reveals differential expression of stress and metabolism genes. Front Plant Sci 8.
  90. Glynn PW, Maté JL, Baker AC, Calderon MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997-1998 El Niño Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982-1983 event. Bull Mar Sci 69:79–109Google Scholar
  91. Gou W, Sun J, Li X, Zhen Y, Xin Z, Yu Z et al (2003) Phylogenetic analysis of a free-living strain of Symbiodinium isolated from Jiaozhou Bay, P.R. China. J Exp Mar Biol Ecol 296:135–144. Scholar
  92. Goulet TL (2006) Most corals may not change their symbionts. Mar Ecol Prog Ser 321:1–7. Scholar
  93. Goulet TL, Coffroth MA (2003a) Genetic composition of zooxanthellae between and within colonies of the octocoral Plexaura kuna, based on small subunit rDNA and multilocus DNA fingerprinting. Mar Biol 142:233–239. Scholar
  94. Goulet TL, Coffroth MA (2003b) Stability of an octocoral-algal symbiosis over time and space. Mar Ecol Prog Ser 250:117–124. Scholar
  95. Goulet TL, Coffroth MA (2004) The genetic identity of dinoflagellate symbionts in Caribbean octocorals. Coral Reefs 23:465–472. Scholar
  96. Goulet TL, Cook CB, Goulet D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallida/Symbiodinium symbiosis. Limnol Oceanogr 50:1490–1498. Scholar
  97. Goulet TL, Simmons C, Goulet D (2008) Worldwide biogeography of Symbiodinium in tropical octocorals. Mar Ecol Prog Ser 355:45–58. Scholar
  98. Grajales A, Rodriguez E (2014) Morphological revision of the genus Aiptasia and the family Aiptasiidae (Cnidaria, Actiniaria, Metridioidea). Zootaxa 3826:55–100. Scholar
  99. Granados-Cifuentes C, Neigel J, Leberg P, Rodriguez-Lanetty M (2015) Genetic diversity of free-living Symbiodinium in the Caribbean: the importance of habitats and seasons. Coral Reefs 34:927–939. Scholar
  100. 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.
  101. Grégoire V, Schmacka F, Coffroth MA, Karsten U (2017) Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). J Appl Phycol 29:1893–1905. Scholar
  102. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189. Scholar
  103. Grupstra CGB, Coma R, Ribes M, Leydet KP, Parkinson JE, McDonald K et al (2017) Evidence for coral range expansion accompanied by reduced diversity of Symbiodinium genotypes. Coral Reefs 36:981–985. Scholar
  104. Gutiérrez-Rodríguez C, Lasker HR (2004) Reproductive biology, development, and planula behavior in the Caribbean gorgonian Pseudopterogorgia elisabethae. Invertebr Biol 123:54–67. Scholar
  105. Hansen G, Daugbjerg N (2009) Symbiodinium natans sp. nov.: a “free-living” dinoflagellate from Tenerife (Northeast-Atlantic Ocean). J Phycol 45:251–263. Scholar
  106. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Coral Reefs. Ecosystems of the World 25. Elsevier, pp 133–207Google Scholar
  107. Harvell D, Jordán-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith G et al (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195. Scholar
  108. Hirose M, Kinzie R, Hidaka M (2001) Timing and process of entry of zooxanthellae into oocytes of hermatypic corals. Coral Reefs 20:273–280. Scholar
  109. Hirose M, Reimer JD, Hidaka M, Suda S (2008) Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa, Japan. Mar Biol 155:105–112. Scholar
  110. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866. Scholar
  111. Hoogenboom MO, Campbell DA, Beraud E, DeZeeuw K, Ferrier-Pagès C (2012) Effects of light, food availability and temperature stress on the function of photosystem II and photosystem I of coral symbionts. PLoS One 7. Scholar
  112. Howells EJ, van Oppen MJH, Willis BL (2009) High genetic differentiation and cross-shelf patterns of genetic diversity among Great Barrier Reef populations of Symbiodinium. Coral Reefs 28:215–225. Scholar
  113. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature. Clim Chang 2:116–120. Scholar
  114. Howells EJ, Willis BL, Bay LK, van Oppen MJH (2013) Spatial and temporal genetic structure of Symbiodinium populations within a common reef-building coral on the Great Barrier Reef. Mol Ecol 22:3693–3708. Scholar
  115. Howells EJ, Willis BL, Bay LK, van Oppen MJH (2016a) Microsatellite allele sizes alone are insufficient to delineate species boundaries in Symbiodinium. Mol Ecol 25:2719–2723. Scholar
  116. Howells EJ, Abrego D, Meyer E, Kirk NL, Burt JA (2016b) Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob Chang Biol 22:2702–2714. Scholar
  117. Huang H, Zhou G, Yang J, Liu S, You F, Lei X (2013) Diversity of free-living and symbiotic Symbiodinium in the coral reefs of Sanya, South China Sea. Mar Biol Res 9:117–128. Scholar
  118. Hume BCC, 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.
  119. Hunter CL, Morden CW, Smith CM (1997) The utility of ITS sequences in assessing relationships among zooxanthellae and corals. In: Proceedings of the 8th international coral reef symposium, Panama, pp 1599–1602Google Scholar
  120. Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 113:163–175. Scholar
  121. Iglesias-Prieto R, Trench RK (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll–protein complexes to different photon-flux densities. Mar Biol 130:23–33. Scholar
  122. Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc B 271:1757–1763. Scholar
  123. Jeong HJ, Lee SY, Kang NS, Yoo YD, Lim AS, Lee MJ et al (2014) Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the sole representative of Symbiodinium clade E. J Eukaryot Microbiol 61:75–94. Scholar
  124. 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.
  125. 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 2011.
  126. Jones A, Berkelmans R (2012) The photokinetics of thermo-tolerance in Symbiodinium. Mar Ecol 33:490–498. Scholar
  127. Jones AM, Berkelmans R, van Oppen MJH, 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 B 275:1359–1365. Scholar
  128. Kamezaki M, Higa M, Hirose M, Suda S, Reimer JD (2013) Different zooxanthellae types in populations of the zoanthid Zoanthus sansibaricus along depth gradients in Okinawa, Japan. Mar Biodivers 43:61–70. Scholar
  129. Karim W, Nakaema S, Hidaka M (2015) Temperature effects on the growth rates and photosynthetic activities of Symbiodinium cells. J Mar Sci Eng 3:368–381. Scholar
  130. Kemp DW, Cook CB, LaJeunesse TC, Brooks WR (2006) A comparison of the thermal bleaching responses of the zoanthid Palythoa caribaeorum from three geographically different regions in south Florida. J Exp Mar Biol Ecol 335:266–276. Scholar
  131. Kemp DW, Fitt WK, Schmidt GW (2008) A microsampling method for genotyping coral symbionts. Coral Reefs 27:289–293. Scholar
  132. Kemp DW, Hernandez-Pech X, Iglesias-Prieto R, Fitt WK, Schmidt GW (2014) Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnol Oceanogr 59:788–797. Scholar
  133. 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 34:535–547. Scholar
  134. Kenkel C, Matz MV (2016) Enhanced gene expression plasticity as a mechanism of adaptation to a variable environment in a reef-building coral. bioRxiv.
  135. Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, Matz MV (2013) Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol 22:4335–4348. Scholar
  136. 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 34:519–531. Scholar
  137. Kennedy EV, Tonk L, Foster NL, Chollett I, Ortiz J-C, Dove S et al (2016) Symbiodinium biogeography tracks environmental patterns rather than host genetics in a key Caribbean reef-builder, Orbicella annularis. Proc R Soc B 283.
  138. Kinzie RA (1974) Experimental infection of aposymbiotic gorgonian polyps with zooxanthellae. J Exp Mar Biol Ecol 15:335–342. Scholar
  139. Kinzie RA, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: experimental tests of critical assumptions. Biol Bull 200:51–58. Scholar
  140. Kirk NL, Andras JP, Harvell CD, Santos SR, Coffroth MA (2009) Population structure of Symbiodinium sp. associated with the common sea fan, Gorgonia ventalina, in the Florida Keys across distance, depth, and time. Mar Biol 156:1609–1623. Scholar
  141. Klueter A, Crandall JB, Archer FI, Teece MA, Coffroth MA (2015) Taxonomic and environmental variation of metabolite profiles in marine dinoflagellates of the genus Symbiodinium. Metabolites 5:74–99. Scholar
  142. Kuniya N, Jimbo M, Tanimoto F, Yamashita H, Koike K, Harii S et al (2015) Possible involvement of Tachylectin-2-like lectin from Acropora tenuis in the process of Symbiodinium acquisition. Fish Sci 81:473–483. Scholar
  143. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiont dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880. Scholar
  144. LaJeunesse TL (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400. Scholar
  145. LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581. Scholar
  146. LaJeunesse TC, Loh WKW, 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 48:2046–2054. Scholar
  147. LaJeunesse T, Bhagooli R, Hidaka M, Devantier L, Done T, Schmidt G et al (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161. Scholar
  148. 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 24:157–159. Scholar
  149. 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 B 276:4139–4148. Scholar
  150. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO et al (2010a) 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 37:785–800. Scholar
  151. LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M et al (2010b) Host-symbiont recombination versus natural selection in response of coral-dinoflagellate symbioses to environmental disturbance. Proc R Soc B 277:2925–2934. Scholar
  152. Lajeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria. J Phycol:1380–1391.
  153. 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 53:305–319. Scholar
  154. Lasker HR (2003) Zooxanthella densities within a Caribbean octocoral during bleaching and non-bleaching years. Coral Reefs 22:23–26. Scholar
  155. Lasker HR, Peters EC, Coffroth MA (1984) Bleaching of reef coelenterates in the San Blas Islands, Panama. Coral Reefs 3:183–190. Scholar
  156. Lee SY, Jeong HJ, Kang NS, Jang TY, Jang SH, Lim AS (2014) Morphological characterization of Symbiodinium minutum and S. psygmophilum belonging to clade B. Algae 29:299–310. Scholar
  157. Lee SY, Jeong HJ, Kang NS, Jang TY, Jang SH, Lajeunesse TC (2015) Symbiodinium tridacnidorum sp. nov., a dinoflagellate common to Indo-Pacific giant clams, and a revised morphological description of Symbiodinium microadriaticum Freudenthal, emended Trench & Blank. Eur J Phycol 50:155–172. Scholar
  158. Lee MJ, Jeong HJ, Jang SH, Lee SY, Kang NS, Lee KH et al (2016) Most low-abundance “background” Symbiodinium spp. are transitory and have minimal functional significance for symbiotic corals. Microb Ecol 71:771–783. Scholar
  159. Lenz EA, Bramanti L, Lasker HR, Edmunds PJ (2015) Long-term variation of octocoral populations in St. John, US Virgin Islands. Coral Reefs 34:1099–1109. Scholar
  160. Levin RA, Beltran VH, Hill R, Kjelleberg S, McDougald D, Steinberg PD et al (2016) Sex, scavengers, and chaperones: transcriptome secrets of divergent Symbiodinium thermal tolerances. Mol Biol Evol 33:2201–2215. Scholar
  161. Levin RA, Voolstra CR, Weynberg KD, van Oppen MJH (2017a) Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts. ISME J 11:808–812. Scholar
  162. Levin RA, Voolstra CR, Agrawal S, Steinberg PD, Suggett DJ, van Oppen MJH (2017b) Engineering strategies to decode and enhance the genomes of coral symbionts. Front Microbiol 8.
  163. Lewis CL, Coffroth MA (2004) The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304:1490–1492. Scholar
  164. Lin S, Cheng S, Song B, Zhong X, Lin X, Li W et al (2015) The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350:691–694. Scholar
  165. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494. Scholar
  166. Littman RA, Willis BL, Bourne DG (2009) Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol Prog Ser 389:45–59. Scholar
  167. Loh W, Loi T, Carter D, Hoegh-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. Mar Ecol Prog Ser 222:97–107. Scholar
  168. Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 5:346–351. Scholar
  169. Lohr J, Munn CB, Wilson WH (2007) Characterization of a latent virus-like infection of symbiotic zooxanthellae. Appl Environ Microbiol 73:2976–2981. Scholar
  170. Loram JE, Boonham N, O’Toole P, Trapido-Rosenthal HG, Douglas AE (2007) Molecular quantification of symbiotic dinoflagellate algae of the genus Symbiodinium. Biol Bull 212:259–268. Scholar
  171. Lucas MQ, Stat M, Smith MC, Weil E, Schizas NV (2016) Symbiodinium (internal transcribed spacer 2) diversity in the coral host Agaricia lamarcki (Cnidaria: Scleractinia) between shallow and mesophotic reefs in the Northern Caribbean (20–70 m). Mar Ecol 37:1079–1087. Scholar
  172. Magalon H, Baudry E, Husté A, Adjeroud M, Veuille M (2006) High genetic diversity of the symbiotic dinoflagellates in the coral Pocillopora meandrina from the South Pacific. Mar Biol 148:913–922. Scholar
  173. Manning MM, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53:1853–1861. Scholar
  174. Marhaver KL, Edwards RA, Rohwer F (2008) Viral communities associated with healthy and bleaching corals. Environ Microbiol 10:2277–2286. Scholar
  175. McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, Warner ME (2012) Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar Ecol Prog Ser 462:1–7. Scholar
  176. McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol 64:1000–1007. Scholar
  177. McIlroy SE, Coffroth MA (2017) Coral ontogeny affects early symbiont acquisition in laboratory-reared recruits. Coral Reefs 36:927–932. Scholar
  178. McIlroy SE, Gillette P, Cunning R, Klueter A, Capo T, Baker AC et al (2016) The effects of Symbiodinium (Pyrrhophyta) identity on growth, survivorship, and thermal tolerance of newly settled coral recruits. J Phycol 52:1114–1124. Scholar
  179. Meyer JR, Ellner SP, Hairston NG, Jones LE, Yoshida T (2006) Prey evolution on the time scale of predator–prey dynamics revealed by allele-specific quantitative PCR. Proc Natl Acad Sci U S A 103:10690–10695. Scholar
  180. Mieog JC, van Oppen MJH, Cantin NE, Stam WT, Olsen JL (2007) Real-time PCR reveals a high incidence of Symbiodinium; clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26:449–457. Scholar
  181. Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS One 4.
  182. Moore RB, Ferguson KM, Loh WKW, Hoegh-Guldberg O, Carter DA (2003) Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium. Int J Syst Evol Microbiol 53:1725–1734. Scholar
  183. Moya A, Tambutté S, Tambutté E, Zoccola D, Caminiti N, Allemand D (2006) Study of calcification during a daily cycle of the coral Stylophora pistillata: implications for ‘light-enhanced calcification’. J Exp Biol 209:3413–3419. Scholar
  184. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460. Scholar
  185. Nozawa Y, Loya Y (2005) Genetic relationship and maturity state of the allorecognition system affect contact reactions in juvenile Seriatopora corals. Mar Ecol Prog Ser 286:115–123. Scholar
  186. Oliver TA, Palumbi SR (2009) Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Mar Ecol Prog Ser 378:93–103. Scholar
  187. Oliver T, Palumbi S (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440. Scholar
  188. Ortiz JC, González-Rivero M, Mumby PJ (2013) Can a thermally tolerant symbiont improve the future of Caribbean coral reefs? Glob Chang Biol 19:273–281. Scholar
  189. Padilla-Gamiño JL, Pochon X, Bird C, Concepcion GT, Gates RD (2012) From parent to gamete: vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata. PLoS One 7. Scholar
  190. Parkinson JE, Baums IB (2014) The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front Microbiol 5.
  191. Parkinson JE, Banaszak AT, Altman NS, LaJeunesse TC, Baums IB (2015a) Intraspecific diversity among partners drives functional variation in coral symbioses. Sci Rep 5.
  192. Parkinson JE, Coffroth MA, LaJeunesse TC (2015b) New species of Clade B Symbiodinium (Dinophyceae) from the greater Caribbean belong to different functional guilds: S. aenigmaticum sp. nov., S. antillogorgium sp. nov., S. endomadracis sp. nov., and S. pseudominutum sp. nov. J Phycol 51:850–858. Scholar
  193. Parkinson J, Baumgarten S, Michell CT, Baums IB, LaJeunesse TC, Voolstra CR (2016) Gene expression variation resolves species and individual strains among coral-associated dinoflagellates within the genus Symbiodinium. Genome Biol Evol 8:665–680. Scholar
  194. Pettay DT, Lajeunesse TC (2009) Microsatellite loci for assessing genetic diversity, dispersal and clonality of coral symbionts in “stress-tolerant” clade D Symbiodinium. Mol Ecol Resour 9:1022–1025. Scholar
  195. Pettay DT, Wham DC, Pinzón JH, Lajeunesse TC (2011) Genotypic diversity and spatial–temporal distribution of Symbiodinium clones in an abundant reef coral. Mol Ecol 20:5197–5212. Scholar
  196. Pinzón JH, LaJeunesse TC (2011) Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Mol Ecol 20:311–325. Scholar
  197. Pinzón J, Devlin-Durante M, Weber M, Baums I, LaJeunesse T (2011) Microsatellite loci for Symbiodinium A3 (S. fitti) a common algal symbiont among Caribbean Acropora (stony corals) and Indo-Pacific giant clams (Tridacna). Conserv Genet Resour 3:45–47. Scholar
  198. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497. Scholar
  199. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30. Scholar
  200. Pochon X, Stat M, Takabayashi M, Chasqui L, Chauka LJ, Logan DDK et al (2010) Comparison of endosymbiotic and free-living Symbiodinium (Dinophyceae) diversity in a Hawaiian reef environment. J Phycol 46:53–65. Scholar
  201. Pochon X, Putnam HM, Burki F, Gates RD (2012) Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLoS One 7. Scholar
  202. Pochon X, Gates RD, Vik D, Edmunds PJ (2014) Molecular characterization of symbiotic algae (Symbiodinium spp.) in soritid foraminifera (Sorites orbiculus) and a scleractinian coral (Orbicella annularis) from St John, US Virgin Islands. Mar Biol 161:2307–2318. Scholar
  203. Poland DM, Coffroth MA (2017) Trans-generational specificity within a cnidarian–algal symbiosis. Coral Reefs 36:119–129. Scholar
  204. Poland DM, Mansfield JM, Hannes AR, Lewis CLF, Shearer TL, Connelly SJ et al (2013) Variation in Symbiodinium communities in juvenile Briareum asbestinum (Cnidaria: Octocorallia) over temporal and spatial scales. Mar Ecol Prog Ser 476:23–37. Scholar
  205. Porto I, Granados C, Restrepo JC, Sanchez JA (2008) Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS One 3.
  206. Prada C, McIlroy SE, Beltrán DM, Valint DJ, Ford SA, Hellberg ME et al (2014) Cryptic diversity hides host and habitat specialization in a gorgonian-algal symbiosis. Mol Ecol 23:3330–3340. Scholar
  207. Puill-Stephan E, Willis BL, van Herwerden L, van Oppen MJH (2009) Chimerism in wild adult populations of the broadcast spawning coral Acropora millepora on the Great Barrier Reef. PLoS One 4.
  208. Puill-Stephan E, Willis BL, Abrego D, Raina JB, van Oppen MJH (2012) Allorecognition maturation in the broadcast-spawning coral Acropora millepora. Coral Reefs 31:1019–1028. Scholar
  209. Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc Roy Soc Biol 279:4352–4361. Scholar
  210. 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.
  211. Quigley KM, Willis BL, Bay LK (2016) Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis. Roy Soc Open Sci 3.
  212. Quigley KM, Willis BL, Bay LK (2017a) Heritability of the Symbiodinium community in vertically- and horizontally-transmitting broadcast spawning corals. Sci Rep 7.
  213. Quigley KM, Bay LK, Willis BL (2017b) 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.
  214. Quigley KM, Warner PA, Bay LK, Willis BL (2018) Unexpected mixed-mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral. Heredity.
  215. Ralph PJ, Gademann R, Larkum AWD (2001) Zooxanthellae expelled from bleached corals at 33oC are photosynthetically competent. Mar Ecol Prog Ser 220:163–168. Scholar
  216. Reich HG, Robertson DL, Goodbody-Gringley G (2017) Do the shuffle: changes in Symbiodinium consortia throughout juvenile coral development. PLoS One 12.
  217. Reimer JD, Todd PA (2009) Preliminary molecular examination of zooxanthellate zoanthids (Hexacorallia: Zoantharia) and associated zooxanthellae (Symbiodinium spp.) diversity in Singapore. Raffles Bull Zool 22:103–120Google Scholar
  218. Reimer JD, Shah MMR, Sinniger F, Yanagi K, Suda S (2010) Preliminary analyses of cultured Symbiodinium isolated from sand in the oceanic Ogasawara Islands, Japan. Mar Biodivers 40:237–247. Scholar
  219. Reimer JD, Herrera M, Gatins R, Roberts MB, Parkinson JE, Berumen ML (2016) Latitudinal variation in the symbiotic dinoflagellate Symbiodinium of the common reef zoantharian Palythoa tuberculosa on the Saudi Arabian coast of the Red Sea. J Biogeogr 44:661–673. Scholar
  220. Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42:568–579. Scholar
  221. Rodriguez-Lanetty M, Krupp DA, Weis VM (2004) Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Mar Ecol Prog Ser 275:97–102. Scholar
  222. Rodriguez-Lanetty M, Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM (2006) Temporal and spatial infection dynamics indicate recognition events in the early hours of a dinoflagellate/coral symbiosis. Mar Biol 149:713–719. Scholar
  223. Rowan R (2004) Coral bleaching: Thermal adaptation in reef coral symbionts. Nature 430:742. Scholar
  224. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci U S A 92:2850–2853. Scholar
  225. Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1351. Scholar
  226. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269. Scholar
  227. Ruzicka RR, Colella MA, Porter JW, Morrison JM, Kidney JA, Brinkhuis V et al (2013) Temporal changes in benthic assemblages on Florida Keys reefs 11 years after the 1997/1998 El Niño. Mar Ecol Prog Ser 489:125–141. Scholar
  228. Sampayo EM, Dove S, Lajeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519. Scholar
  229. Santos SR, Taylor DJ, Coffroth MA (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagelaltes: implications for extrapolating to the intact symbiosis. J Phycol 37:900–912. Scholar
  230. Santos SR, Taylor DJ, Kinzie RA, Sakai K, Coffroth MA (2002) Evolution of length variation and heteroplasmy in the chloroplast rDNA of symbiotic dinoflagellates (Symbiodinium, Dinophyta) and a novel insertion in the universal core region of the large subunit rDNA. Phycologia 41:311–318. Scholar
  231. Santos SR, Gutierrez-Rodriguez C, Coffroth MA (2003) Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23S)-ribosomal DNA sequences. Mar Biotechnol 5:130–140. Scholar
  232. Santos SR, Shearer TL, Hannes AR, Coffroth MA (2004) Fine-scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean. Mol Ecol 13:459–469. Scholar
  233. Savage AM, Trapido-Rosenthal H, Douglas AE (2002) On the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance. Mar Ecol Prog Ser 244:27–37. Scholar
  234. Sawall Y, Al-Sofyani A, Banguera-Hinestroza E, Voolstra CR (2014) Spatio-temporal analyses of Symbiodinium physiology of the coral Pocillopora verrucosa along large-scale nutrient and temperature gradients in the Red Sea. PLoS One 9. Scholar
  235. Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (= Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum. Proc R Soc B 207:405–427. Scholar
  236. Serrano X, Baums IB, O’Reilly K, Smith TB, Jones RJ, Shearer TL et al (2014) Geographic differences in vertical connectivity in the Caribbean coral Montastraea cavernosa despite high levels of horizontal connectivity at shallow depths. Mol Ecol 23:4226–4240. Scholar
  237. Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R et al (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23:1399–1408. Scholar
  238. Shoguchi E, Shinzato C, Hisata K, Satoh N, Mungpakdee S (2015) The large mitochondrial genome of Symbiodinium minutum reveals conserved noncoding sequences between dinoflagellates and apicomplexans. Genome Biol Evol 7:2237–2244. Scholar
  239. Silverstein RN, Correa AMS, LaJeunesse TC, Baker AC (2011) Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar Ecol Prog Ser 422:63–75. Scholar
  240. 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 (1738):2609–2618. Scholar
  241. 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 21:236–249. Scholar
  242. 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 220:1192–1196. Scholar
  243. Smith EG, Ketchum RN, Burt JA (2017) Host specificity of Symbiodinium variants revealed by an ITS2 metahaplotype approach. ISME J 11:1500–1503. Scholar
  244. Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts—symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43. Scholar
  245. Stat M, Morris E, Gates RD (2008) Functional diversity in the coral-dinoflagellate symbiosis. Proc Natl Acad Sci U S A 105:9256–9261. Scholar
  246. Stat M, Pochon X, Cowie RO, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386:83–96. Scholar
  247. Stat M, Yost D, Gates R (2015) Geographic structure and host specificity shape the community composition of symbiotic dinoflagellates in corals from the Northwestern Hawaiian Islands. Coral Reefs 34:1075–1086. Scholar
  248. Suggett DJ, Goyen S, Evenhuis C, Szabó M, Pettay DT, Warner ME et al (2015) Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208:370–381. Scholar
  249. Swain TD, Chandler J, Backman V, Marcelino L (2016) Consensus thermotolerance ranking for 110 Symbiodinium phylotypes: an exemplar utilization of a novel iterative partial rank aggregation tool with broad application potential. Funct Ecol 31:172–183. Scholar
  250. Sweet MJ (2013) Symbiodinium diversity within Acropora muricata and the surrounding environment. Mar Ecol 35:343–353. Scholar
  251. Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 40:160–164. Scholar
  252. Takabayashi M, Adams LM, Pochon X, Gates RD (2012) Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai’i and Florida. Coral Reefs 31:157–167. Scholar
  253. Taylor DL (1974) Symbiotic marine algae: taxonomy and biological fitness. In: Vernberg WB (ed) Symbiosis in the Sea. University of South Carolina Press, Columbia, pp 245–262Google Scholar
  254. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M et al (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci U S A 101:13531–13535. Scholar
  255. Thomas L, Kendrick GA, Kennington WJ, Richards ZT, Stat M (2014) Exploring Symbiodinium diversity and host specificity in Acropora corals from geographical extremes of Western Australia with 454 amplicon pyrosequencing. Mol Ecol 23:3113–3126. Scholar
  256. Thornhill DJ, Fitt WK, Schmidt GW (2006a) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25:515–519. Scholar
  257. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006b) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722. Scholar
  258. 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 16:5326–5340. Scholar
  259. 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 44:1126–1135. Scholar
  260. 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.
  261. Thornhill DJ, Kemp DW, Sampayo EM, Schmidt GW (2010) Comparative analyses of amplicon migration behavior in differing denaturing gradient gel electrophoresis (DGGE) systems. Coral Reefs 29:83–91. Scholar
  262. Thornhill DJ, Lewis AM, Wham DC, LaJeunesse TC (2014) Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68:352–367. Scholar
  263. Thornhill DJ, Howells EJ, Wham DC, Steury TD, Santos SR (2017) Population genetics of reef coral endosymbionts (Symbiodinium, Dinophyceae). Mol Ecol 26:2640–2659. Scholar
  264. Toller WW, Rowan R, Knowlton N (2001a) Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol Bull 201:348–359. Scholar
  265. Toller WW, Rowan R, Knowlton N (2001b) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull 201:360–373. Scholar
  266. Tonk L, Bongaerts P, Sampayo EM, Hoegh-Guldberg O (2013) SymbioGBR: a web-based database of Symbiodinium associated with cnidarian hosts on the Great Barrier Reef. BMC Ecol 13. Scholar
  267. Tonk L, Sampayo EM, LaJeunesse TC, Schrameyer V, Hoegh-Guldberg O (2014) Symbiodinium (Dinophyceae) diversity in reef-invertebrates along an offshore to inshore reef gradient near Lizard Island, Great Barrier Reef. J Phycol 50:552–563. Scholar
  268. Tonk L, Sampayo EM, Chai A, Schrameyer V, Hoegh-Guldberg O (2017) Symbiodinium (Dinophyceae) community patterns in invertebrate hosts from inshore marginal reefs of the southern Great Barrier Reef, Australia. J Phycol 26:2640–2659. Scholar
  269. Trench RK, Blank RJ (1987) Symbiodinium microadriaticum Freudenthal, S. goreauii sp. nov., S. kawagutii sp. nov. and S. pilosum sp. nov.: Gymnodinioid Dinoflagellate symbionts of marine invertebrates. J Phycol 23:469–481. Scholar
  270. Ulstrup KE, van Oppen MJH (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12:3477–3484. Scholar
  271. Ulstrup KE, Berkelmans R, Ralph PJ, van Oppen MJH (2006) Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae. Mar Ecol Prog Ser 314:135–148. Scholar
  272. van Hooidonk R, Maynard J, Tamelander J, Gove J, Ahmadia G, Raymundo L et al (2016) Local-scale projections of coral reef futures and implications of the Paris Agreement. Sci Rep 6.
  273. van Oppen MJH, Palstra FP, Piquet AM-T, Miller DJ (2001) Patterns of coral–dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host–symbiont selectivity. Proc R Soc B 268:1759–1767. Scholar
  274. van Oppen MJH, Mahiny A, Done T (2005a) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24:482–487. Scholar
  275. van Oppen MJH, Mieog JC, Sanchez CA, Fabricius KE (2005b) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14:2403–2417. Scholar
  276. van Oppen MJH, Leong J-A, Gates RD (2009) Coral-virus interactions: a double-edged sword? Symbiosis 47:1–8. Scholar
  277. van Oppen MJH, Souter P, Howells EJ, Heyward A, Berkelmans R (2011) Novel genetic diversity through somatic mutations: fuel for adaptation of reef corals? Diversity 3:405–423. Scholar
  278. Venera-Ponton DE, Diaz-Pulido G, Rodriguez-Lanetty M, Hoegh-Guldberg O (2010) Presence of Symbiodinium spp. in macroalgal microhabitats from the southern Great Barrier Reef. Coral Reefs 29:1049–1060. Scholar
  279. Ware JR, Fautin DG, Buddemeier RW (1996) Patterns of coral bleaching: modeling the adaptive bleaching hypothesis. Ecol Model 84:199–214. Scholar
  280. 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 51:1887–1897. Scholar
  281. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066. Scholar
  282. Weis VM, Reynolds WS, deBoer MD, Krupp DA (2001) Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20:301–308. Scholar
  283. Weynberg KD, Neave M, Clode PL, Voolstra CR, Brownlee C, Laffy P et al (2017) Prevalent and persistent viral infection in cultures of the coral algal endosymbiont Symbiodinium. Coral Reefs 36:773–784. Scholar
  284. Wham DC, LaJeunesse TC (2016) Symbiodinium population genetics: testing for species boundaries and analysing samples with mixed genotypes. Mol Ecol 25:2699–2712. Scholar
  285. Wham DC, Pettay DT, LaJeunesse TC (2011) Microsatellite loci for the host-generalist “zooxanthella” & Symbiodinium trenchi and other Clade D Symbiodinium. Conserv Genet Resour 3:541–544. Scholar
  286. Wilkinson SP, Fisher PL, van Oppen MJH, Davy SK (2015) Intra-genomic variation in symbiotic dinoflagellates: recent divergence or recombination between lineages? BMC Evol Biol 15.
  287. Wirshing HH, Baker A (2016) On the difficulty of recognizing distinct Symbiodinium species in mixed communities of algal symbionts. Mol Ecol 25:2724–2726. Scholar
  288. Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8:1985–1993. Scholar
  289. Yamashita H, Koike K (2013) Genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol Res 61:68–80. Scholar
  290. Yamashita H, Suzuki G, Hayashibara T, Koike K (2013) Acropora recruits harbor “rare” Symbiodinium in the environmental pool. Coral Reefs 32:355–366. Scholar
  291. Ziegler M, Roder CM, Büchel C, Voolstra CR (2014) Limits to physiological plasticity of the coral Pocillopora verrucosa from the central Red Sea. Coral Reefs 33:1115–1129. Scholar
  292. Ziegler M, Arif C, Burt JA, Dobretsov S, Roder C, LaJeunesse TC et al (2017) Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. J Biogeogr 44:674–686. Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • K. M. Quigley
    • 1
    • 2
    Email author
  • A. C. Baker
    • 3
  • M. A. Coffroth
    • 4
  • B. L. Willis
    • 2
  • M. J. H. van Oppen
    • 1
    • 5
  1. 1.Australian Institute of Marine ScienceTownsvilleAustralia
  2. 2.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  3. 3.Department of Marine Biology and EcologyRosenstiel School of Marine and Atmospheric Science, University of MiamiMiamiUSA
  4. 4.Department of Biological SciencesState University of New York at BuffaloBuffaloUSA
  5. 5.School of BioSciences, The University of MelbourneParkvilleAustralia

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