Coral Reefs

, Volume 26, Issue 1, pp 35–44 | Cite as

Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities

  • Yi-T. Lien
  • Y. Nakano
  • S. Plathong
  • H. Fukami
  • Jih-T. Wang
  • C. A. ChenEmail author


Biogeographic investigations have suggested that coral-symbiont associations can adapt to higher temperatures by hosting a heat-tolerant Symbiodinium, phylotype D. It is hypothesized that phylotype D is absent in high latitudes due to its heat-tolerant characteristics. In this study, this hypothesis was tested by examining the symbiont diversity in a scleractinian coral, Oulastrea crispata, throughout its entire latitudinal distribution range in the West Pacific. Molecular phylotyping of the 5′-end of the nuclear large subunit of ribosomal DNA (lsu rDNA) indicated that phylotype D was the dominant Symbiodinium in O. crispata from the tropical reefs to the marginal non-reefal coral communities. Several colonies of tropical populations were associated with phylotype C, either alone or simultaneously with phylotype D. Analysis of the polymerase chain reaction products using single-strand conformation polymorphism (SSCP) detected relatively low densities of phylotype C in most of the O. crispata colonies surveyed. These results provide evidence for the occurrence of phylotype D in cold-water outlying coral communities. The dominant occurrence of phylotype C in some O. crispata colonies on tropical reefs and the relatively low densities of phylotype C identified by SSCP in subtropical and temperate populations show that the dominant symbiont type can vary in this coral species and that multiple symbionts can co-occur in the same host.


Coral bleaching Symbiodinium Phylotype Heat tolerant PCR-RFLP SSCP 



Many thanks to K. K. Lam, Q.-C. Chen, X.-C. Song, and P. Jarayabhand for hosting our field trips and for their coral collections. Special thanks to the Evolutionary Biology Group, Research Centre for Biodiversity, Academia Sinica (RCBAS), the three anonymous reviewers and Dr. M. van Oppen for the constructive comments. This work was supported by Academia Sinica Thematic grants (2002–2004, 2006–2007) to C.A.C, and by the RCBAS travel funds for field collections at Hainan and Weijhou Islands, China, and Si-Chiang, Bu-Lun and Sa-Tun, Thailand. This is the Evolution and Ecology Group, RCBAS contribution no. 41.


  1. Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766CrossRefGoogle Scholar
  2. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Syst 34:661–689CrossRefGoogle Scholar
  3. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 403:741CrossRefGoogle Scholar
  4. 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
  5. Brown BE (1997a) Adaptations of reef corals to physical environmental stress. Adv Mar Biol 31:222–299Google Scholar
  6. Brown BE (1997b) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138CrossRefGoogle Scholar
  7. Carlos AA, Baillie BK, Brett K, Kawaguchi 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 35:1054–1062CrossRefGoogle Scholar
  8. Chen CA, Lam KK, Nakano Y, Tsai WS (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
  9. Chen CA, Wang JT, Fang LS, Yang YW (2005a) Fluctuating algal symbiont communities in Acropora palifera (Cnidaria; Scleractinia) from Taiwan. Mar Ecol Prog Ser 295:343–347Google Scholar
  10. Chen CA, Yang YW, Wei NV, Tsai WS, Fang LS (2005b) Symbiont diversity in the scleractinian corals from tropical reefs and non-reefal communities in Taiwan. Coral Reefs 24:11–22CrossRefGoogle Scholar
  11. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34CrossRefGoogle Scholar
  12. Coles SL, Brown BE (2003) Coral bleaching—capacity for acclimatization and adaptation. Adv Mar Biol 46:183–223CrossRefGoogle Scholar
  13. Douglas AE (2003) Coral bleaching—how and why? Mar Pollut Bull 46:385–392CrossRefGoogle Scholar
  14. 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 13:2445–2458CrossRefGoogle Scholar
  15. Garcia L, Pochon X, Pawlowski J (2006) Molecular evidence for host-symbiont specificity in soritid foraminifera. Protist 156: 399–412Google Scholar
  16. Gilbert DC (1994) SeqApp 1.9. A biological sequence editor and analysis program for Macintosh computers. Available from ftp.indiana.eduGoogle Scholar
  17. 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
  18. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  19. Hoegh-Guldberg O, Jones RJ, Ward S, Loh WK (2002) Is coral bleaching really adaptive? Nature 415:601–602CrossRefGoogle Scholar
  20. 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, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefGoogle Scholar
  21. 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 Lond B Biol Sci 271:1757–1763CrossRefGoogle Scholar
  22. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schimdt 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
  23. LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Don T, Schimdt GW, Fitt WK, Hoegh-Guldberg O (2004a) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161Google Scholar
  24. LaJeunesse TC, Thornhill DJ, Cox FF, Stanton FG, Fitt WK, Schmidt GW (2004b) High diversity and host-specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603Google Scholar
  25. Lam KK (2000) Sexual reproduction of a low-temperature tolerant coral Oulastrea crispata (Scleractinia, Faviidae) in Hong Kong, China. Mar Ecol Prog Ser 205:101–111Google Scholar
  26. Loh W, Hidaka M, Hirose M, Titlyanov EA (2002) Genotypic diversity of symbiotic dinoflagellates associated with hermatypic corals from a fringing reef at Sesoko Island, Okinawa. Galaxea 4:1–9Google Scholar
  27. Nakano Y, Yamazato K (1992) Ecological study of reproduction of Oulastrea crispata in Okinawa. Zool Sci 9:1292Google Scholar
  28. Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T (1989a) Detection of polymorphism of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proc Natl Acad Sci USA 86:2766–2770CrossRefGoogle Scholar
  29. Orita M, Suzuki Y, Sekiya T, Hayashi K (1989b) A rapid and sensitive detection of point mutations and genetic polymorphisms using polymerase chain reaction. Genomics 5:874–879CrossRefGoogle Scholar
  30. Pochon X, Montoya-Burgos JI, Stadeklmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30CrossRefGoogle Scholar
  31. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808CrossRefGoogle Scholar
  32. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefGoogle Scholar
  33. Ronquist F, Huelsenbeck JP (2003) MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  34. Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34:407–417CrossRefGoogle Scholar
  35. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742CrossRefGoogle Scholar
  36. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 28:2850–2853CrossRefGoogle Scholar
  37. Rowan R, Powers D (1991a) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73Google Scholar
  38. Rowan R, Powers DA (1991b) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1351CrossRefGoogle Scholar
  39. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269CrossRefGoogle Scholar
  40. Schoenberg CHL, Loh WKW (2005) Molecular identity of the unique symbiotic dinoflagellates found in the bioeroding demosponge Cliona orientalis. Mar Ecol Prog Ser 299:157–166Google Scholar
  41. Sotka EE, Thacker RW (2005) Do some corals like it hot? Trends Ecol Evol 20:59–62CrossRefGoogle Scholar
  42. Swofford DL (2002) PAUP 4.10b: phylogenetic analysis using parsimony (and other methods). Sinauer Associates, SunderlandGoogle Scholar
  43. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipid of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535CrossRefGoogle Scholar
  44. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL X: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position-specific gap penalties and weight matrix choice. Nuclei Acids Res 22:4673–4680CrossRefGoogle Scholar
  45. 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 201:348–359CrossRefGoogle Scholar
  46. 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 201:360–373CrossRefGoogle Scholar
  47. van Oppen MJH, Mieog JC, Sánchez CA, Fabricius KE (2005) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14:2403–2417CrossRefGoogle Scholar
  48. van Oppen MJH, Palstra FP, Piquet AMT, 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 Lond Ser B 268:1759–1767CrossRefGoogle Scholar
  49. Veron JEN (1995) Corals in Space and Time. University of New South Wales Press, SydneyGoogle Scholar
  50. Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  51. Yajima T, Sano O, Okamoto T, Yoshohiro S, Thutomu S, Masahiro M (1986) Ecological distribution of the reef coral, Oulastrea crispata (Lamarck) at the shore region in the vicinity of Tukumo Bay. Bull Jpn Sea Res Inst Kanazawa Univ 18:21–36Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Yi-T. Lien
    • 1
    • 2
  • Y. Nakano
    • 2
  • S. Plathong
    • 3
  • H. Fukami
    • 4
  • Jih-T. Wang
    • 5
  • C. A. Chen
    • 1
    Email author
  1. 1.Research Center for BiodiversityAcademia SinicaTaipeiTaiwan
  2. 2.Sesoko Station, Tropical Biosphere Research CenterUniversity of RyukyusOkinawaJapan
  3. 3.Department of BiologyPrince of Songkla UniversitySongklaThailand
  4. 4.Seto Marine Biological StationThe Kyoto UniversityShirayamaJapan
  5. 5.Department of BiotechnologyTajen University of Science and TechnologyYanpu, PingtungTaiwan

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