Symbiodinium spp. associated with high-latitude scleractinian corals from Jeju Island, South Korea

Abstract

Most studies on endosymbiotic dinoflagellate algae (genus Symbiodinium) associated with scleractinian corals focus on tropical and sub-tropical reefs. Their diversity in outlying, non-reef coral communities at high latitudes is still not fully documented. In this study, we analyzed the Symbiodinium diversity associated with five scleractinian species collected at eight sites around Jeju Island (South Korea, 33.4°N) between 5 and 15 m depth. Denaturing gradient gel electrophoresis of amplified internal transcribed spacer region 2 distinguished five Symbiodinium types. We observed a high level of specificity between host genera and Symbiodinium spp. despite existing in an environment with large seasonal oscillations in temperature and light. Psammocora albopicta and Psammocora profundacella were associated with C1 and Montipora millepora with C17. Alveopora japonica was associated exclusively with an unusual F-type, the only known clade F representative functionally important to a scleractinian coral. Oulastrea crispata was associated with Symbiodinium boreum (type D15), occasionally co-occurring with type C3 (in 4 % of specimens). In addition to increasing the knowledge of Symbiodinium diversity in high-latitude coral communities, this study constitutes an important baseline upon which the effects of projected environmental change in the near future can be assessed. A better understanding of high-latitude coral communities is critical for understanding how a warming planet will affect the tempo and mode of shifts in the composition of temperate marine communities.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Baghooli R (2012) Light-induced production of turbeculae on exposed coral surfaces of the coral Montipora capitata. University of Mauritius Research Journal 18:145–165

    Google Scholar 

  2. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571

    Article  Google Scholar 

  3. Baird AH, Sommer B, Madin JS (2012) Poleward range expansion of Acropora spp. along the east coast of Australia. Coral Reefs 31:1063

    Article  Google Scholar 

  4. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  5. Barneah O, Weis VM, Perez ST, Benayahu Y (2004) Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition matters. Mar Ecol Prog Ser 275:89–95

    CAS  Article  Google Scholar 

  6. Beger M, Sommer B, Harrison PL, Smith SDA, Pandolfi JM (2014) Conserving potential coral reef refuges at high latitudes. Divers Distrib 20:245–257

    Article  Google Scholar 

  7. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellate 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 273:2305–2315

    Article  Google Scholar 

  8. Bongaerts P, Sampayo EM, Bridge TCL, Ridgway T, Vermeulen F, Englebert N, Webster JM, Hoegh-Guldberg O (2011) Symbiodinium diversity in mesophotic coral communities on the Great Barrier Reef: a first assessment. Mar Ecol Prog Ser 439:117–126

    Article  Google Scholar 

  9. Bongaerts P, Frade P, Ogier J, Hay K, van Bleijswijk J, Englebert N, Vermeij M, Bak R, Visser P, Hoegh-Guldberg O (2013) Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2–60 m) on a Caribbean reef. BMC Evol Biol 13:205

    PubMed Central  PubMed  Article  Google Scholar 

  10. Budd AF, Pandolfi JM (2010) Evolutionary novelty is concentrated at the edge of coral species distributions. Science 328:1558–1561

    CAS  PubMed  Article  Google Scholar 

  11. 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-reef coral communities. Zool Stud 42:540–550

    Google Scholar 

  12. Cooper TF, Ulstrup KE, Dandan SS, Heyward AJ, Kuhl M, Muirhead A, O’Leary RA, Ziersen BEF, van Oppen MJH (2011) Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types. Proc R Soc Lond B Biol Sci 278:1840–1850

    Article  Google Scholar 

  13. Denis V, Chen CA, Song JI, Woo S (2013) Alveopora japonica beds thriving under kelp. Coral Reefs 32:503

    Article  Google Scholar 

  14. Denis V, Ribas Deulofeu L, De Palmas S, Chen CA (2014) First record of the scleractinian coral Psammocora albopicta from Korean waters. Mar Biodivers 44:157–158

    Google Scholar 

  15. Denis V, Ribas-Deulofeu L, Loubeyres M, De Palmas S, Hwang SJ, Woo S, Song JI, Chen CA (2015) Recruitment of the subtropical coral Alveopora japonica in the temperate waters of Jeju Island, South Korea. Bull Mar Sci 91:85–96

    Article  Google Scholar 

  16. Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity 81:599–603

    Article  Google Scholar 

  17. Dove S, Ortiz JC, Enriquez S, Fine M, Fisher P, Iglesias-Prieto R, Thornhill D, Hoegh-Guldberg O (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol Oceanogr 51:1149–1158

    Article  Google Scholar 

  18. Frade PR, Bongaerts P, Winkelhagen AJS, Tonk L, Bak RPM (2008) In situ photobiology of corals over large depth ranges: a multivariate analysis on the roles of environment, host, and algal symbiont. Limnol Oceanogr 53:2711–2723

    Article  Google Scholar 

  19. 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 Res 12:369–373

    Article  Google Scholar 

  20. Harii S, Omori M, Yamakawa H, Koike Y (2001) Sexual reproduction and larval settlement of the zooxanthellate coral Alveopora japonica Eguchi at high latitude. Coral Reefs 20:19–23

    Article  Google Scholar 

  21. Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195

    Article  Google Scholar 

  22. 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 318:1737–1742

    CAS  PubMed  Article  Google Scholar 

  23. Jeong HJ, Lee SY, Kang NS, Yoo YD, Lim AS, Lee MJ, Kim HS, Yih W, Yamashita H, LaJeunesse TC (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

    CAS  PubMed  Article  Google Scholar 

  24. Kang DH, Song JI, Choi KS (2005) Image analysis of typhoon impacts on soft coral community at Munseom in Jeju, Korea. Ocean Polar Rese 27:25–34

    CAS  Article  Google Scholar 

  25. Kawecki TJ (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39:321–342

    Article  Google Scholar 

  26. Kleypas JA, McManus JW, Meñez LAB (1999) Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146–159

    Google Scholar 

  27. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Article  Google Scholar 

  28. LaJeunesse TC, Thornhill DJ (2011) Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS One 6:e29013

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  29. 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 48:1380–1391

    Article  Google Scholar 

  30. 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

    Article  Google Scholar 

  31. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW (2004) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603

    Google Scholar 

  32. LaJeunesse TC, Reyes Bonilla H, Warner ME, Wills M, Schmidt GW, Fitt WK (2008) Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnol Oceanogr 53:719–727

    Article  Google Scholar 

  33. LaJeunesse TC, Wham DC, Pettay DT, Parkinso 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

    Article  Google Scholar 

  34. 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 37:785–800

    Article  Google Scholar 

  35. Lesser MP, Slattery M, Stat M, Ojimi M, Gates RD, Grottoli A (2010) Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: light, food, and genetics. Ecology 91:990–1003

    PubMed  Article  Google Scholar 

  36. Levas SJ, Grottoli AG, Hughes A, Osburn CL, Matsui Y (2013) Physiological and biochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: Implications for resilience in mounding corals. PLoS One 8:e63267

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  37. Lien YT, Fukami H, Yamashita Y (2012) Symbiodinium clade C dominates zooxanthellates corals (Scleractinia) in the temperate region of Japan. Zoolog Sci 29:173–180

    PubMed  Article  Google Scholar 

  38. Lien YT, Nakano Y, Plathong S, Fukami H, Wang JT, Chen CA (2007) Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26:35–44

    Article  Google Scholar 

  39. Lien YT, Keshavmurthy S, Nakano Y, Plathong S, Huang H, Hsu CM, Fukami H, Yamashita Y, Hsieh HJ, Wang JT, Chen CA (2013) Host genetics and Symbiodinium D diversity in a stress-tolerant scleractinian coral, Oulastrea crispata, in the West Pacific. Mar Ecol Prog Ser 473:163–177

    Article  Google Scholar 

  40. Loh W, 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

    Article  Google Scholar 

  41. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  42. Park SH, Lee YP, Kim YH, Lee IK (1994) Qualitative and quantitative analyses of intertidal benthic algal community in Cheju Island. 1. Species composition and distributional patterns. Algae 9:193–203

    Google Scholar 

  43. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497

    CAS  PubMed  Article  Google Scholar 

  44. 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 139:1069–1078

    Article  Google Scholar 

  45. Pochon X, Garcia-Cuetos L, Baker AC, Castella E, Pawlowski J (2007) One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera. Coral Reefs 26:867–882

    Article  Google Scholar 

  46. Rodriguez-Lanetty M, Cha HR, Song JI (2000) Genetic diversity of symbiotic dinoflagellates associated with anthozoans from Korean waters. Proc 9th Int Coral Reef Symp 1:63–66

    Google Scholar 

  47. Rodriguez-Lanetty M, Chang SJ, Song JI (2003) Specificity of two temperate dinoflagellates-anthozoan associations from the North-western Pacific Ocean. Mar Biol 143:1193–1199

    Article  Google Scholar 

  48. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742

    CAS  PubMed  Article  Google Scholar 

  49. Sampayo EM, Ridgeway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci USA 105:10444–10449

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  50. Savage AM, Goodson MS, Visram S, Trapido-Rosenthal H, Wiedenmann J, Douglas AE (2002) Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and sea anemones. Mar Eco Prog Ser 244:17–26

    Article  Google Scholar 

  51. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    CAS  Article  Google Scholar 

  52. Silverstein RN, Correa AM, LaJeunesse TC, Baker AC (2011) Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar Ecol Prog Ser 422:63–75

    Article  Google Scholar 

  53. Sugihara K, Yamano H, Choi KS, Hyeong K (2014) Zooxanthellate scleractinian corals of Jeju Island, Republic of Korea. In: Nakashizuka T (ed) Nakano S, Y Tetsukazu. Integrative Observations and Assessments. Springer, Japan, pp 111–130

    Google Scholar 

  54. Takatsuki Y, Kuraga N, Shiga T, Bunki N, Inoue H, Fujiwara H, Ariyoshi M (2007) Long-term trends in sea surface temperature adjacent to Japan. Sokko Jiho 74:S33–S87 (In Japanese)

    Google Scholar 

  55. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  56. 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 148:711–722

    Article  Google Scholar 

  57. Vergés A, Steinberg PD, Hay ME, Poore AG, Campbell AH, Ballesteros E, Heck KL, Booth D, Coleman MA, Feary D, Figueira W, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, van Sebille E, Sen Gupta A, Smale DA, Tomas F, Wernberg T, Wilson SK (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc Biol Sci 281:20140846

    PubMed Central  PubMed  Article  Google Scholar 

  58. Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville

    Google Scholar 

  59. Veron JEN (2011) Global ocean circulation and coral reefs. In: Hopley D (ed) Encyclopedia of modern coral reefs. Encyclopedia of Earth Science Series, Springer, Heidelberg, pp 497–503

    Google Scholar 

  60. 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

    Article  Google Scholar 

  61. 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

    Article  Google Scholar 

  62. Wicks LC, Sampayo E, Gardner JPA, Davy SK (2010) Local endemicity and high diversity characterise high-latitude coral–Symbiodinium partnerships. Coral Reefs 29:989–1003

    Article  Google Scholar 

  63. Yamamura N (1996) Evolution of mutualistic symbiosis: a differential equation model. Popul Ecol 38:211–218

    Article  Google Scholar 

  64. Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys Res Lett. doi:10.1029/2010GL046474

    Google Scholar 

  65. Yamashita H, Koike K (2012) Genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol Res 61:68–80

    Article  Google Scholar 

Download references

Acknowledgments

Coral collection was supported by the Korean Coral Resources Bank (KCRB). Thanks are given to the members of the Coral Reef Evolutionary Ecology and Genetics (CREEG) laboratory, Biodiversity Research Center, Academia Sinica (BRCAS). This study was supported by Academia Sinica Thematic program grants (2011–2013), the National Science Council of Taiwan (NSC, Grant 100-2923-B-001-005-MY2) to CAC and National Research Foundation of Korea (NRF, Grant 2011-0030568) to JIS. VD was supported by a NSC postdoctoral fellowship, ML by the International Internship Program of the Taiwan International Graduate Program (TIGP-IIP) and SW by PE99202, Korea. The authors would like to thank the anonymous reviewers for their valuable comments and suggestions to improve the quality of the manuscript. This is CREEG-BRCAS contribution no. 113.

Author information

Affiliations

Authors

Corresponding author

Correspondence to C. A. Chen.

Additional information

Communicated by Biology Editor Dr. Anastazia Banaszak

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

De Palmas, S., Denis, V., Ribas-Deulofeu, L. et al. Symbiodinium spp. associated with high-latitude scleractinian corals from Jeju Island, South Korea. Coral Reefs 34, 919–925 (2015). https://doi.org/10.1007/s00338-015-1286-y

Download citation

Keywords

  • Zooxanthellae
  • Outlying coral communities
  • Marginal areas
  • Coral reefs
  • Tropicalization
  • ITS2–DGGE