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.
References
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
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
Baird AH, Sommer B, Madin JS (2012) Poleward range expansion of Acropora spp. along the east coast of Australia. Coral Reefs 31:1063
Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689
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
Beger M, Sommer B, Harrison PL, Smith SDA, Pandolfi JM (2014) Conserving potential coral reef refuges at high latitudes. Divers Distrib 20:245–257
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
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
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
Budd AF, Pandolfi JM (2010) Evolutionary novelty is concentrated at the edge of coral species distributions. Science 328:1558–1561
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
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
Denis V, Chen CA, Song JI, Woo S (2013) Alveopora japonica beds thriving under kelp. Coral Reefs 32:503
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
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
Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity 81:599–603
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
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
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
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
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
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
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
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
Kawecki TJ (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39:321–342
Kleypas JA, McManus JW, Meñez LAB (1999) Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146–159
LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400
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
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
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
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
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
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
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
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
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
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
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
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
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
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
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
Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497
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
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
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
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
Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742
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
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
Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90
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
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
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)
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
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
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
Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville
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
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
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
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
Yamamura N (1996) Evolution of mutualistic symbiosis: a differential equation model. Popul Ecol 38:211–218
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
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
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.
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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
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DOI: https://doi.org/10.1007/s00338-015-1286-y