Advertisement

Marine Biology

, Volume 158, Issue 1, pp 87–100 | Cite as

Do corals select zooxanthellae by alternative discharge?

  • Hiroshi Yamashita
  • Go Suzuki
  • Takeshi Hayashibara
  • Kazuhiko KoikeEmail author
Original Paper

Abstract

Loss of zooxanthellae (dinoflagellate Symbiodinium) from corals will sometimes lead to mass mortality of corals. To detect and quantify Symbiodinium released from corals, we developed a zooxanthellae “trap” and a quantitative PCR (qPCR) system with Symbiodinium clades A–F-specific primer sets. The trap was attached to a branch or the surface of several wild stony corals, and the water samples within the traps, including released Symbiodinium, were subjected to qPCR. All tested corals released clade C Symbiodinium at estimates of ~5,900 cells h−1 cm−2 of coral surface. Although all tested Pocillopora eydouxi harboured both clades C and D, some of these colonies released only clade C or released a lesser amount of clade D than that in the tissues. Our Symbiodinium quantification system revealed that wild hermatypic corals constantly release Symbiodinium to the environment. Our result suggests that some corals may discharge certain clades of Symbiodinium alternatively.

Keywords

Methylene Blue Coral Bleaching qPCR System Symbiodinium Cell Trap Setting 
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.

Notes

Acknowledgments

This work was supported by a Grant-in-Aid (No. 21310011) for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan to KK. The authors express their sincere thanks to Akiko Yura, Tomo Matsuoka, and Yohei Takaya, Faculty of Applied Biological Science, Hiroshima University, for their support during this investigation. Thanks are also given to Dr. Lawrence M. Liao, Hiroshima University, for editing the manuscript.

References

  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 Evol Syst 34:661–689CrossRefGoogle Scholar
  3. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 430:741CrossRefGoogle Scholar
  4. 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 273:2305–2312CrossRefGoogle Scholar
  5. Bhagooli R, Hidaka M (2004) Release of zooxanthellae with intact photosynthetic activity by the coral Galaxea fascicularis in response to high temperature stress. Mar Biol 145:329–337CrossRefGoogle Scholar
  6. Bowers HA, Tengs T, Glasgow HB, Burkholder JM, Rublee PA, Oldach DW (2000) Development of real-time PCR assays for rapid detection of Pfiesteria piscicida and related dinoflagellates. Appl Environ Microbiol 66:4641–4648CrossRefGoogle Scholar
  7. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138CrossRefGoogle Scholar
  8. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326CrossRefGoogle Scholar
  9. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34CrossRefGoogle Scholar
  10. Correa AMS, McDonald MD, Baker AC (2009) Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Mar Biol 156:2403–2411CrossRefGoogle Scholar
  11. Dyhrman ST, Erdner D, La Du J, Galac M, Anderson DM (2006) Molecular quantification of toxic Alexandrium fundyense in the Gulf of Maine using real-time PCR. Harmful Algae 5:242–250CrossRefGoogle Scholar
  12. Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845CrossRefGoogle Scholar
  13. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685CrossRefGoogle Scholar
  14. Galluzzi L, Penna A, Bertozzini E, Vila M, Garcés E, Magnani M (2004) Development of a real-time PCR assay for rapid detection and quantification of Alexandrium minutum (a dinoflagellate). Appl Environ Microbiol 70:1199–1206CrossRefGoogle Scholar
  15. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960CrossRefGoogle Scholar
  16. Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol Bull 182:324–332CrossRefGoogle Scholar
  17. Glynn PW, Maté JL, Baker AC, Calderón 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
  18. Hoegh-Guldberg O (1988) A method for determining the surface area of corals. Coral Reefs 7:113–116CrossRefGoogle Scholar
  19. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  20. Hosoi-Tanabe S, Sako Y (2005) Species-specific detection and quantification of toxic marine dinoflagellates Alexandrium tamarense and A. catenella by real-time PCR assay. Mar Biotechnol 7:506–514CrossRefGoogle Scholar
  21. Jones RJ (1997) Zooxanthellae loss as a bioassay for assessing stress in corals. Mar Ecol Prog Ser 149:163–171CrossRefGoogle Scholar
  22. 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 275:1359–1365CrossRefGoogle Scholar
  23. Kamikawa R, Asai J, Miyahara T, Murata K, Oyama K, Yoshimatsu S, Yoshida T, Sako Y (2006) Application of a real-time PCR assay to a comprehensive method of monitoring harmful algae. Microbes Environ 21:163–173CrossRefGoogle Scholar
  24. Kinzie RA III, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: experimental tests of critical assumptions. Biol Bull 200:51–58CrossRefGoogle Scholar
  25. Koike K, Yamashita H, Oh-Uchi A, Tamaki M, Hayashibara T (2007) A quantitative real-time PCR method for monitoring Symbiodinium in the water column. Galaxea 9:1–12CrossRefGoogle Scholar
  26. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400CrossRefGoogle Scholar
  27. 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 48:2046–2054CrossRefGoogle Scholar
  28. LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161CrossRefGoogle Scholar
  29. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefGoogle Scholar
  30. Lewis CL, Coffroth MA (2004) The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304:1490–1492CrossRefGoogle Scholar
  31. Lien Yi-T, Nakano Y, Plathong S, Fukami H, Wang Jih-T, Chen CA (2007) Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26:35–44CrossRefGoogle Scholar
  32. 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 212:259–268CrossRefGoogle Scholar
  33. Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263CrossRefGoogle Scholar
  34. 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 26:449–457CrossRefGoogle Scholar
  35. Perez SF, Cook CB, Brooks WR (2001) The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. J Exp Mar Biol Ecol 256:1–14CrossRefGoogle Scholar
  36. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogent Evol 56:492–497CrossRefGoogle Scholar
  37. 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 38:20–30CrossRefGoogle Scholar
  38. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742CrossRefGoogle Scholar
  39. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853CrossRefGoogle Scholar
  40. 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
  41. Stimson J, Kinzie RA III (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153:63–74CrossRefGoogle Scholar
  42. Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 40:160–164CrossRefGoogle Scholar
  43. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535CrossRefGoogle Scholar
  44. 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 148:711–722CrossRefGoogle Scholar
  45. Titlyanov EA, Titlyanova TV, Leletkin VA, Tsukahara J, van Woesik R, Yamazato K (1996) Degradation of zooxanthellae and regulation of their density in hermatypic corals. Mar Ecol Prog Ser 139:167–178CrossRefGoogle Scholar
  46. Toller WW, Rowan R, Knowlton N (2001) 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
  47. Wilcox TP (1998) Large-subunit ribosomal RNA systematics of symbiotic Dinoflagellates: morphology does not recapitulate phylogeny. Mol Phylogenet Evol 10:436–448CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Hiroshi Yamashita
    • 1
    • 2
  • Go Suzuki
    • 2
  • Takeshi Hayashibara
    • 2
  • Kazuhiko Koike
    • 1
    Email author
  1. 1.Graduate School of Biosphere Science, Hiroshima UniversityHigashi-HiroshimaJapan
  2. 2.Ishigaki Tropical Station Seikai National Fisheries Research InstituteFisheries Research Agency, Fukai-OhtaIshigakiJapan

Personalised recommendations