The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: Correlations with host and the history of ocean thermal stress

Ecology and Evolution

Volumn 3, Issue 5, 2013, Pages 1317-1329

  Stat, Michael ^a,b,c   Pochon, Xavier ^d   Franklin, Erik C ^e   Bruno, John F ^f   Casey, Kenneth S ^g   Selig, Elizabeth R ^h   Gates, Ruth D ^e  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c CSIRO   (Australia)

^d CAWTHRON INSTITUTE   (New Zealand)

^e UNIVERSITY OF HAWAII   (United States)

^f UNIVERSITY OF NORTH CAROLINA   (United States)

^g NOAA EARTH SYSTEM RESEARCH LABORATORY   (United States)

^h Conservation International   (United States)

Author keywords

Climate change; Coral; ITS2; Symbiodinium; Symbiosis

Indexed keywords

EID: 84886311113     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.556     Document Type: Article

References (77)

1. Abrego, D., K. E. Ulstrup, B. L. Willis, and M. J. H. van Oppen 2008. Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc. R. Soc. B Biol. Sci. 275:2273-2282.
2. Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26:32-46.
3. Anderson, M. J. 2005. PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand.
4. Apprill, A. M., and R. D. Gates 2007. Recognizing diversity in coral symbiotic dinoflagellate communities. Mol. Ecol. 16:1127-1134.
5. Baker, A. C. 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34:661-689.
6. Baker, A., C. Starger, T. McClanahan, and P. Glynn 2004. Corals' adaptive response to climate change. Nature 430:741.
7. Barshis, D. J., J. H. Stillman, R. D. Gates, R. J. Toonen, L. W. Smith, and C. Birkeland 2010. Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Mol. Ecol. 19:1705-1720.
8. Berkelmans, R., and M. J. H. van Oppen 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 Biol. Sci. 273:2305-2312.
9. Bjorbækmo, M. F. M., T. Carlsen, A. Brysting, T. Vrålstad, K. Høiland, K. I. Ugland, et al. 2010. High diversity of root associated fungi in both alpine and arctic Dryas octopetala. BMC Plant Biol. 10:244.
10. Blaalid, R., T. Carlsen, S. Kumar, R. Halvorsen, K. I. Ugland, G. Fontana, et al. 2012. Changes in the root-associated fungal communities along a primary succession gradient analysed by 454 pyrosequencing. Mol. Ecol. 21:1897-1908.
11. Brazelton, W. J., K. A. Ludwig, M. L. Sogin, E. N. Andreishcheva, D. S. Kelley, C. C. Shen, et al. 2010. Archaea and bacteria with surprising microdiversity show shifts in dominance over 1, 000-year time scales in hydrothermal chimneys. Proc. Natl. Acad. Sci. USA 107:1612-1617.
12. Cantin, N. E., M. J. H. van Oppen, B. L. Willis, J. C. Mieog, and A. P. Negri 2009. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405-414.
13. Carpenter, K. E., M. Abrar, G. Aeby, R. B. Aronson, S. Banks, A. Bruckner, et al. 2008. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560-563.
14. Casey, K. S., T. B. Brandon, P. Cornillon, and R. Evans 2010. The past, present, and future of the AVHRR Pathfinder SST program. Springer, New York.
15. Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18:117-143.
16. Clarke, K. R., and R. N. Gorley 2006. PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth.
17. Clement, M., D. Posada, and K. A. Crandall 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:1657-1659.
18. Cooper, T. F., R. Berkelmans, K. E. Ulstrup, S. Weeks, B. Radford, A. M. Jones, et al. 2011. Environmental factors controlling the distribution of Symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef. PLoS ONE 6:e25536.
19. Correa, A. M. S., and A. C. Baker 2009. Understanding diversity in coral-algal symbiosis: a cluster-based approach to interpreting fine-scale genetic variation in the genus Symbiodinium. Coral Reefs 28:81-93.
20. Costa, C. F., R. Sassi, and K. Gorlach-Lira 2008. Zooxanthellae genotypes in the coral Siderastrea stellata from coastal reefs in northeastern Brazil. J. Exp. Mar. Biol. Ecol. 367:149-152.
21. Fabricius, K. E., J. C. Mieog, P. L. Colin, D. Idip, and M. J. H. van Oppen 2004. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol. Ecol. 13:2445-2458.
22. Fenner, D. 2005. Corals of Hawai'i. Mutual Publishing, Honolulu, HI.
23. Finney, J. C., D. T. Pettay, E. M. Sampayo, M. E. Warner, H. A. Oxenford, and T. C. LaJeunesse 2010. The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb. Ecol. 60:250-263.
24. Franklin, E. C., M. Stat, X. Pochon, H. M. Putnam, and R. D. Gates 2012. GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium-host symbioses. Mol. Ecol. Resour. 12:369-373.
25. Goulet, T. 2006. Most corals may not change their symbionts. Mar. Ecol. Prog. Ser. 321:1-7.
26. Granados, C., C. Camargo, S. Zea, and J. A. Sánchez 2008. Phylogenetic relationships among zooxanthellae (Symbiodinium) associated to excavating sponges (Cliona spp.) reveal an unexpected lineage in the Caribbean. Mol. Phylogenet. Evol. 49:554-560.
27. Grottoli, A. G., L. J. Rodrigues, and J. E. Palardy 2006. Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186-1189.
28. Hill, M., A. Allenby, B. Ramsby, C. Schönberg, and A. Hill 2011. Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Mol. Phylogenet. Evol. 59:81-88.
29. Hoegh-Guldberg, O. 1999. Climate change, coral bleaching, and the future of the world's coral reefs. Mar. Freshw. Res. 50:839-866.
30. Hoegh-Guldberg, O., and J. F. Bruno 2010. The impact of climate change on the world's marine ecosystems. Science 328:1523-1528.
31. Hoegh-Guldberg, O., and J. G. Smith 1989. The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J. Exp. Mar. Biol. Ecol. 129:279-303.
32. Horner-Devine, M. C., M. Lage, J. Hughes, and J. Bohannan 2004. A taxa-area relationship for bacteria. Nature 432:750-753.
33. Hunter, C. L., M. D. Stephenson, R. S. Tjeerdema, D. G. Crosby, G. S. Ichikawa, J. D. Goetzl, et al. 1995. Contaminants in oysters in Kaneohe Bay, Hawaii. Mar. Pollut. Bull. 30:646-654.
34. Jones, A., and R. Berkelmans 2010. Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS ONE 5:e10437.
35. Jones, A. M., R. Berkelmans, M. J. H. van Oppen, J. C. Mieog, and W. Sinclair 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 Biol. Sci. 275:1359-1365.
36. LaJeunesse, T. C. 2005. "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol. Biol. Evol. 22:570-581.
37. LaJeunesse, T., W. Loh, R. van Woesik, O. Hoegh-Guldberg, G. Schmidt, and W. Fitt 2003. Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol. Oceanogr. 48:2046-2054.
38. LaJeunesse, T., D. Thornhill, E. Cox, F. Stanton, W. Fitt, and G. Schmidt 2004a. High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596-603.
39. LaJeunesse, T. C., R. Bhagooli, M. Hidaka, L. De Vantier, T. Done, G. W. Schmidt, et al. 2004b. Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar. Ecol. Prog. Ser. 284:147-161.
40. LaJeunesse, T. C., H. Reyes-Bonilla, and M. E. Warner 2007. Spring "bleaching" among Pocillopora in the Sea of Cortez, Eastern Pacific. Coral Reefs 26:265-270.
41. LaJeunesse, T. C., W. K. W. Loh, and R. K. Tench 2008. Do introduced endosymbiotic dinoflagellates 'take' to new hosts? Biol. Invasions 11:995-1003.
42. LaJeunesse, T., R. Smith, J. Finney, and H. Oxenford 2009. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral "bleaching" event. Proc. R. Soc. B Biol. Sci. 276:4139-4148.
43. LaJeunesse, T. C., D. T. Pettay, E. M. Sampayo, N. Phongsuwan, B. Brown, D. O. Obura, et al. 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.
44. Landeweert, R., P. Leeflang, T. Kuyper, E. Hoffland, A. Rosling, K. Wernars, et al. 2003. Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl. Environ. Microbiol. 69:327-333.
45. Little, A., M. van Oppen, and B. Willis 2004. Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492-1494.
46. McArdle, B. H., and M. J. Anderson 2001. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290-297.
47. McGinley, M. P., M. D. Aschaffenburg, D. T. Pettay, R. T. Smith, T. C. LaJeunesse, and M. E. Warner 2012. Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar. Ecol. Prog. Ser. 462:1-7.
48. Mieog, J. C., M. J. H. van Oppen, N. E. Cantin, W. T. Stam, and J. L. Olsen 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 26:449-457.
49. Mieog, J. C., J. L. Olsen, R. Berkelmans, S. A. Bleuler-Martinez, B. L. Willis, and M. J. H. van Oppen 2009. The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4:e6364.
50. Mostafavi, P. G., S. M. R. Fatemi, M. H. Shahhosseiny, O. Hoegh-Guldberg, and W. K. W. Loh 2007. Predominance of clade D Symbiodinium in shallow-water reef-building corals off Kish and Larak Islands (Persian Gulf, Iran). Mar. Biol. 153:25-34.
51. NOAA National Weather Service. Available at http://www.prh.noaa.gov/hnl/pages/climate_summary.php
52. Oliver, T., and S. Palumbi 2009. Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Mar. Ecol. Prog. Ser. 378:93-103.
53. van Oppen, M. J. H., J. C. Mieog, C. A. Sanchez, and K. E. Fabricius 2005. Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol. Ecol. 14:2403-2417.
54. Ortiz, J. C., M. Gonzalez-Rivero, and P. J. Mumby 2013. Can a thermally tolerant symbiont improve the future of Caribbean coral reefs? Global Change Biol. 19:273-281.
55. Perry, A., P. Low, J. Ellis, and J. Reynolds 2005. Climate change and distribution shifts in marine fishes. Science 308:1912-1915.
56. Pochon, X., and R. D. Gates 2010. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawaii. Mol. Phylogenet. Evol. 56:492-497.
57. Pochon, X., L. Garcia-Cuetos, A. C. Baker, E. Castella, and J. Pawlowski 2007. One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera. Coral Reefs 26:867-882.
58. Pochon, X., M. Stat, M. Takabayashi, L. Chasqui, L. J. Chauka, D. D. K. Logan, et al. 2010. Comparison of endosymbiotic and free-living Symbiodinium (Dinophyceae) diversity in a Hawaiian reef environment. J. Phycol. 46:53-65.
59. R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
60. Rodrigues, L. J., and A. G. Grottoli 2007. Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol. Oceanogr. 52:1874-1882.
61. Rowan, R. 2004. Thermal adaptations in reef coral symbionts. Nature 430:742.
62. Sammarco, P. W., and M. J. Risk 1990. Large-scale patterns in internal bioerosion of Porites: cross continental shelf trends on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 59:145-156.
63. Schloss, P. D., S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
64. Selig, E. R., K. S. Casey, and J. F. Bruno 2010. New insights into global patterns of ocean temperature anomolies: implications for coral reef health and management. Global Ecol. Biogeogr. 19:397-411.
65. Silverstein, R. N., A. M. S. Correa, and A. C. Baker 2012. Specificity is rarely absolute in coral-algal symbiosis: implications for coral response to climate change. Proc. R. Soc. B Biol. Sci. 279:2609-2618.
66. Stat, M., and R. D. Gates 2011. Clade D Symbiodinium in scleractinian corals: a "nugget" of hope, a selfish opportunist, an ominous sign, or all of the above? J. Mar. Biol 2011:730715.
67. Stat, M., D. Carter, and O. Hoegh-Guldberg 2006. The evolutionary history of Symbiodinium and scleractinian hosts - symbiosis, diversity, and the effect of climate change. Perspect. Plant Ecol. 8:23-43.
68. Stat, M., E. Morris, and R. D. Gates 2008a. Functional diversity in coral-dinoflagellate symbiosis. Proc. Natl. Acad. Sci. USA 105:9256-9261.
69. Stat, M., W. K. W. Loh, O. Hoegh-Guldberg, and D. A. Carter 2008b. Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs 27:763-772.
70. Stat, M., W. K. W. Loh, T. C. LaJeunesse, O. Hoegh-Guldberg, and D. A. Carter 2009a. Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709-713.
71. Stat, M., X. Pochon, R. Cowie, and R. Gates 2009b. Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar. Ecol. Prog. Ser. 386:83-96.
72. Stat, M., C. E. Bird, X. Pochon, L. Chasqui, L. J. Chauka, G. T. Concepcion, et al. 2011. Variation in Symbiodinium ITS2 sequence assemblages among coral colonies. PLoS ONE 6:e15854.
73. Thornhill, D. J., T. C. LaJeunesse, D. W. Kemp, W. K. Fitt, and G. W. Schmidt 2005. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148:711-722.
74. Thornhill, D. J., W. K. Fitt, and G. W. Schmidt 2006. Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25:515-519.
75. Thornhill, D., T. LaJeunesse, and S. Santos 2007. Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol. Ecol. 16:5326-5340.
76. Walther, G. R., E. Post, P. Convey, A. Menzel, C. Parmesan, T. Beebee, et al. 2002. Ecological responses to recent climate change. Nature 416:389-395.
77. Wicks, L. C., E. Sampayo, J. P. A. Gardner, and S. K. Davy 2010. Local endemicity and high diversity characterise high-latitude coral-Symbiodinium partnerships. Coral Reefs 29:989-1003.