Marine Biology

, Volume 143, Issue 6, pp 1193–1199 | Cite as

Specificity of two temperate dinoflagellate–anthozoan associations from the north-western Pacific Ocean

  • M. Rodriguez-Lanetty
  • Soo-Jung Chang
  • Jun-Im SongEmail author
Research Article


Whilst many studies of symbiotic dinoflagellate diversity have focused on tropical reef environments, only a few have explored the degree and pattern of divergence of these endosymbionts at high latitudes. In this study, the genetic diversity and specificity of symbiotic dinoflagellates associated with two common anthozoan hosts in the north-western Pacific Ocean was studied in four different seasons during a period of 1 year. Partial nucleotide sequences of 28S and complete ITS1 ribosomal DNA regions were used to identify, genetically, the endosymbionts extracted from the scleractinian Alveopora japonica and the actinarian Heteractis sp. A. japonica harbours symbionts belonging to Symbiodinium of clade F, while Heteractis sp. associates with Symbiodinium of clade C. Moreover, no seasonal changes in the endosymbiont community were detected in these two associations during this study. This is the first evidence that these two temperate cnidarian–microalgae symbioses are stable. Furthermore, we tested the apparent specificity of the Heteractis sp.– Symbiodinium sp. clade C association, by performing alga-infection experiments with aposymbiotic hosts, and monitoring the uptake and persistence of homologous and heterologous symbionts. The findings confirm the association patterns detected in the field and show that Heteractis sp. only establishes a successful association with Symbiodinium cells of clade C, at least among the heterologous symbionts occurring in the study area. Our results are consistent with the idea that selective pressures in highly fluctuating temperate environments might have granted symbiosis-specificity an adaptive value.


Dinoflagellate Scleractinian Coral ITS1 rDNA Symbiotic Dinoflagellate Bleaching Procedure 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are grateful to H. Cha and Y. Lee for assistance in the collection of samples, and S. Hwang for helping in the maintenance of the aquarium systems. We also want to thank to Dr. G. Muller-Parker and Dr. S. Davy for their comments on a first draft of our manuscript. This work was supported by a grant No. R04-2000-0001P from the Korean Science and Engineering Foundation (to J.I.S.).


  1. Baillie BK, Belda-Baillie CA, Maruyama T (2000) Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. J Phycol 36:1153–1161Google Scholar
  2. Baker AC (1999) The symbiosis ecology of reef-building corals. PhD thesis. Rosenstiel School of Marine and Atmospheric Science. University of Miami, MiamiGoogle Scholar
  3. Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766PubMedGoogle Scholar
  4. Baker AC, Rowan R (1997) Diversity of symbiotic dinoflagellates (zooxanthellae) in scleractinian corals of the Caribbean and eastern Pacific. Proc 8th Int Coral Reef Symp 2:1301–1306Google Scholar
  5. Belda-Baillie CA, Baillie BK, Maruyama T (2002) Specificity of a model cnidarian–dinoflagellate symbiosis. Biol Bull 202:74–85Google Scholar
  6. Berner T, Baghdasarian G, Muscatine L (1993) Repopulation of a sea anemone with symbiotic dinoflagellates: analysis by in vivo fluorescence. J Exp Mar Biol Ecol 170:145–158Google Scholar
  7. Bui B, Hoegh-Guldberg O, Loh W, Carter D (2000) Analysing the diversity of symbiotic dinoflagellates (zooxanthellae) using molecular approach. The Australian Society for Microbiology Conference, Poster no. P1.22Google Scholar
  8. Bythell JC, Douglas AE, Sharp VA, Searle JB, Brown BE (1997) Algal genotype and photoacclimatory responses of the symbiotic algae Symbiodinium in natural populations of the sea anemone Anemionia viridis. Proc R Soc London Ser B 264:1277–1282Google Scholar
  9. Chang SS, Prezelin BB, Trench RK (1983) Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar Biol 76:219–229Google Scholar
  10. Coffroth MA, Goulet TL, Santos SR (2001) Early ontogenic expression of specificity in a cnidarian–algal symbiosis. Mar Ecol Prog Ser 222:85–96Google Scholar
  11. Colley NJ, Trench RK (1983) Cellular events in the reestablishment of a symbiosis between a marine dinoflagellate and a coelenterate. Cell Tissue Res 239:93–103Google Scholar
  12. Darius HT, Dauga C, Grimont PAD, Chungue E, Martin PV (1998) Diversity in symbiotic dinoflagellates (Pyrrophyta) from seven scleractinian coral species: Restriction enzyme analysis of small subunit ribosomal RNA genes. J Eukaryot Microbiol 45:619–627Google Scholar
  13. Davy SK, Lucas IAN, Turner JR (1997a) Uptake and persistence of homologous and heterologous zooxanthellae in the temperate sea anemone Cereus pedunculatus (Pennat). Biol Bull 192:208–216Google Scholar
  14. Davy SK, Lucas IAN, Turner JR (1997b) The nature of temperate anthozoan–dinoflagellate symbioses. Proc 8th Int Coral Reef Symp 2:1307–1312Google Scholar
  15. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
  16. Fitt WK (1984) The role of chemosensory behavior of Symbiodinium microadriaticum, intermediate hosts, and host behavior in the infection of coelenterates and molluscs with zooxanthellae. Mar Biol 81:9–17Google Scholar
  17. Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J Protozool 9:45–52Google Scholar
  18. 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 113:163–175Google Scholar
  19. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a species level marker. J Phycol 37:866–880Google Scholar
  20. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134PubMedGoogle Scholar
  21. Loh W, Carter D, Hoegh-Guldberg O (1998) Diversity of zooxanthellae from scleractinian corals of One Tree Island (The Great Barrier Reef). ACRS 75th Annu Conf 1:141–149Google Scholar
  22. Loi T (1998) Molecular diversity of the predominant clade C zooxanthellae from scleractinian corals of the Great Barrier Reef. Honours thesis, Department of Microbiology, University of Sydney, SydneyGoogle Scholar
  23. Muller-Parker G, Davy SK (2001) Temperate and tropical algal–sea anemone symbioses. Invertebr Biol 120:104–123Google Scholar
  24. Muller-Parker G, D'Elia C (1997) Interactions between corals and their symbiotic algae. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, New YorkGoogle Scholar
  25. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world. Coral Reef. Elsevier, AmsterdamGoogle Scholar
  26. Muscatine LE, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27:454–460Google Scholar
  27. Pawlowski J, Holzmann M, Fahrni JF, Pochon X, Lee JJ (2001) Molecular identification of algal endosymbionts in large miliolid foraminifera. 2. Dinoflagellates. J Eukaryot Microbiol 48:368–373PubMedGoogle Scholar
  28. 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 139:1069–78CrossRefGoogle Scholar
  29. Porter JW, Muscatine L, Dubinsky Z, Falkowski P (1984) Primary production and photoadaptation in light- and shade-adapted colonies of the symbiotic coral, Stylophora pistillata. Proc R Soc London Ser B 222:161–180Google Scholar
  30. Rodriguez-Lanetty M (2003) Evolving lineages of Symbiodinium -like dinoflagellates based on ITS1 rDNA. Mol Phylogenet Evol 28:152–168Google Scholar
  31. Rodriguez-Lanetty M, Loh W, Carter D, Hoegh-Guldberg O (2001) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Mar Biol 138:1175–1181Google Scholar
  32. Rodriguez-Lanetty M, Cha HR, Song JI (2003) Genetic diversity of symbiotic dinoflagellates associated to anthozoans from Korean waters. Proc 8th Int Coral Reef Symp 1:163–166Google Scholar
  33. Rowan R (1998) Diversity and ecology of zooxanthallae on coral reefs. J Phycol 34:407–417CrossRefGoogle Scholar
  34. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral–algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853Google Scholar
  35. Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal–algal symbioses. Science 251:1348–1350Google Scholar
  36. Rowan R, Knowlton N, Baker AC (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269PubMedGoogle Scholar
  37. 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 Ecol Prog Ser 244:17–26Google Scholar
  38. Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (= Gymnodinium) microadriaticum Freudenthal and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of S. microadriaticum. Proc R Soc London Ser B 207:445–460Google Scholar
  39. Schwarz JA, Weis VM, Potts DC (2002) Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantisima. Mar Biol 140:471–478Google Scholar
  40. Seavy BE, Muller-Parker G (2002) Chemosensory and feeding responses of the nudibranch Aeolidia papillosa to the symbiotic sea anemone Anthopleura elegantissima. Invertebr Biol 121:115–125Google Scholar
  41. Song JI (1991) A systematic study on the Korean Anthozoa. 12. Order Scleractinia. Korean J Syst Zool 7:127–150Google Scholar
  42. Song JI, Lim HS (2001) Taxonomy of symbiotic dinoflagellates associated with Korean anthozoans. Korean J Biol Sci 5:281–289Google Scholar
  43. Swofford DL (1998) PAUP. Phylogenetic analysis using parsimony. Sinauer, Sunderland, Mass.Google Scholar
  44. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensivity of progressive multiple sequence alignment through sequences weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedGoogle Scholar
  45. Toller WW, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull 201:360–373PubMedGoogle Scholar
  46. Trench RK (1997) Diversity of symbiotic dinoflagellates and the evolution of microalgal–invertebrate symbioses. Proc 8th Int Coral Reef Symp 2:1275–1286Google Scholar
  47. Van Oppen MJH, Palstra EP, Piquet AMT, Miller D (2001) Patterns of coral–dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host–symbiont selectivity. Proc R Soc London Ser B 268:1759–1767Google Scholar
  48. Weis MV, Reynolds WS, Boer MD de, 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 20:301–308CrossRefGoogle Scholar
  49. Wilcox TP (1998) Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: morphology does not recapitulate phylogeny. Mol Phylogenet Evol 10:436–448PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • M. Rodriguez-Lanetty
    • 1
    • 2
  • Soo-Jung Chang
    • 1
  • Jun-Im Song
    • 1
    Email author
  1. 1.Department of Life SciencesEwha Women's UniversitySeoulKorea
  2. 2.Department of ZoologyOregon State UniversityCorvallisUSA

Personalised recommendations