Host-Specific Interactions with Environmental Factors Shape the Distribution of Symbiodinium across the Great Barrier Reef

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Tonk, Linda ^a   Sampayo, Eugenia M ^a   Weeks, Scarla ^a   Magno Canto, Marites ^a   Hoegh Guldberg, Ove ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACROPORIDAE MILLEPORA; ACROPORIDAE TENUIS; ARTICLE; COMMUNITY STRUCTURE; CONTROLLED STUDY; CORAL REEF; DINOFLAGELLATE; ENVIRONMENTAL FACTOR; ENVIRONMENTAL IMPACT; GEOGRAPHICAL VARIATION (SPECIES); NONHUMAN; POCILLOPORIDAE DAMICORNIS; POCILLOPORIDAE PISTILLATA; POPULATION RESEARCH; SEA SURFACE TEMPERATURE; SPECIES DISTRIBUTION; SPECIES DIVERSITY; SPECIES IDENTIFICATION; SYMBIODINIUM; SYMBIODINIUM HYSTRIX; SYMBIODINIUM PISTILLATA; SYMBIONT; TAXONOMY; TURBINARIA RENIFORMIS;

ANIMALS; BIODIVERSITY; CORAL REEFS; DINOFLAGELLIDA; ECOSYSTEM; ENVIRONMENT; HOST SPECIFICITY; OCEANOGRAPHY; SYMBIOSIS;

ANTHOZOA; DINOPHYCEAE; INVERTEBRATA; SYMBIODINIUM;

EID: 84879747899     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068533     Document Type: Article

References (78)

1. Hoegh-Guldberg O, (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshw Res 50: 839-866.
2. Teneva L, Karnauskas M, Logan CA, Bianucci L, Currie JC, et al. (2012) Predicting coral bleaching hotspots: the role of regional variability in thermal stress and potential adaptation rates. Coral Reefs 31: 1-12.
3. van Woesik, Franklin EC, O'Leary J, McClanahan TR, Klaus JS, et al. (2012) Hosts of the Plio-Pleistocene past reflect modern-day coral vulnerability. Proc Roy Soc Lond B 279: 2448-2456.
4. Frade PR, De Jongh F, Vermeulen F, Van Bleijswijk J, Bak RPM, (2008) Variation in symbiont distribution between closely related coral species over large depth ranges. Mol Ecol 17: 691-703.
5. LaJeunesse TC, Bhagooli R, Hidaka M, DeVantier L, Done T, et al. (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: 147-161.
6. Rowan R, Knowlton N, (1995) Intraspecific diversity and ecological zonation in coral algal symbiosis. Proc Natl Acad Sci U S A 92: 2850-2853.
7. Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S, (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16: 3721-3733.
8. Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, et al. (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.
9. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, 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.
10. 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 Roy Soc Lond B 273: 2305-2312.
11. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, et al. (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanog 48: 2046-2054.
12. van Oppen MJH, Mahiny AJ, Done TJ, (2005) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24: 482-487.
13. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.
14. Pochon X, Gates RD, (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol Phylogenet Evol 56: 492-497.
15. Rowan R, Powers DA, (1991) A molecular genetic cassification of zooxanthellae and the evolution of animal-algal symbioses. Science 251: 1348-1351.
16. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, et al. (2004) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23: 596-603.
17. 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.
18. van Oppen MJH, Palstra FP, Piquet AMT, Miller DJ, (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity (vol 268, pg 1759, 2001). Proc Roy Soc Lond B 268: 2617-2617.
19. LaJeunesse TC, Thornhill DJ, (2011) Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolutionary history through psbA non-coding region genotyping. PLoS ONE 6: e29013.
20. Sampayo EM, Dove S, Lajeunesse TC, (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18: 500-519.
21. 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.
22. Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE, (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc Roy Soc Lond B 271: 1757-1763.
23. LaJeunesse TC, Lambert G, Andersen RA, Coffroth MA, Galbraith DW, (2005b) Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. J Phycol 41: 880-886.
24. 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 Oceanog 53: 2711-2723.
25. 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 Roy Soc Lond B 275: 1359-1365.
26. Sampayo EM, Ridgway 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 U S A 105: 10444-10449.
27. 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 Oceanog 51: 1887-1897.
28. LaJeunesse TC, Smith R, Walther M, Pinzon J, Pettay DT, et al. (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc Roy Soc Lond B 277: 2925-2934.
29. Diekmann OE, Bak RPM, Tonk L, Stam WT, Olsen JL, (2002) No habitat correlation of zooxanthellae in the coral genus Madracis on a Curacao reef. Mar Ecol Prog Ser 227: 221-232.
30. Diekmann OE, Olsen JL, Stam WT, Bak RPM, (2003) Genetic variation within Symbiodinium clade B from the coral genus Madracis in the Caribbean (Netherlands Antilles). Coral Reefs 22: 29-33.
31. Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, et al. (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS ONE 5: e0871.
32. 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: 449-457.
33. 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.
34. Stat M, Loh WKW, Hoegh-Guldberg O, Carter DA, (2008) Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs 27: 763-772.
35. Wicks LC, Gardner JPA, Davy SK, (2010) Spatial patterns and regional affinities of coral communities at the Kermadec Islands Marine Reserve, New Zealand-a marginal high-latitude site. Mar Ecol Prog Ser 400: 101-113.
36. Cooper TF, Berkelmans R, Ulstrup KE, Weeks S, Radford B, 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.
37. Spalding MD, Fox HE, Halpern BS, McManus MA, Molnar J, et al. (2007) Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. BioScience 57: 573-583.
38. Loh WKW, Loi T, 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.
39. Rodriguez-Lanetty M, Chang SJ, Song JI, (2003) Specificity of two temperate dinoflagellate-anthozoan associations from the north-western Pacific Ocean. Mar Biol 143: 1193-1199.
40. Ulstrup KE, Berkelmans R, Ralph PJ, van Oppen MJH, (2006) Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae. Mar Ecol Prog Ser 314: 135-148.
41. Ulstrup KE, Hill R, van Oppen MJH, Larkum AWD, Ralph PJ, (2008) Seasonal variation in the photo-physiology of homogeneous and heterogeneous Symbiodinium consortia in two scleractinian corals. Mar Ecol Prog Ser 361: 139-150.
42. Ulstrup KE, Van Oppen MJH, (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12: 3477-3484.
43. Van Oppen MJH, Mieog JC, Sanchez CA, Fabricius KE, (2005) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14: 2403-2417.
44. van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF, (2011) The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol 20: 1647-1660.
45. van Oppen MJH, (2004) Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Mar Biol 144: 1-7.
46. Ulstrup KE, Kuehl M, van Oppen MJH, Cooper TF, Ralph PJ, (2011) Variation in photosynthesis and respiration in geographically distinct populations of two reef-building coral species. Aquat Biol 12: 241-248.
47. Rodriguez-Lanetty M, Hoegh-Guldberg O, (2003) Symbiont diversity within the widespread scleractinian coral Plesiastrea versipora, across the northwestern Pacific. Mar Biol 143: 501-509.
48. Fabricius KE, Mieog JC, Colin PL, Idip D, Van Oppen MJH, (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13: 2445-2458.
49. Goulet TL, LaJeunesse TC, Fabricius KE, (2008) Symbiont specificity and bleaching susceptibility among soft corals in the 1998 Great Barrier Reef mass coral bleaching event. Mar Biol 154: 795-804.
50. Goulet TL, Simmons C, Goulet D, (2008) Worldwide biogeography of Symbiodinium in tropical octocorals. Mar Ecol Prog Ser 355: 45-58.
51. Howells EJ, van Oppen MJH, Willis BL, (2009) High genetic differentiation and cross-shelf patterns of genetic diversity among Great Barrier Reef populations of Symbiodinium. Coral Reefs 28: 215-225.
52. Jones A, Berkelmans R, (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.
53. Bongaerts P, Riginos C, Hay KB, van Oppen MJH, Hoegh-Guldberg O, et al. (2011) Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats. BMC Evol Biol 11: 303.
54. Hill M, Allenby A, Ramsby B, Schoenberg C, Hill A, (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.
55. Tonk L, Bongaerts P, Sampayo EM, Hoegh-Guldberg O, (2013) SymbioGBR: a web-based database of Symbiodinium associated with cnidarian hosts on the Great Barrier Reef. BMC ecol 13: 7-7.
56. Mieog JC, Van Oppen MJH, Berkelmans R, Stam WT, Olsen JL, (2009) Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol Ecol Res 9: 74-82.
57. LaJeunesse TC, Bonilla HR, Warner ME, Wills M, Schmidt GW, et al. (2008) Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnol Oceanog 53: 719-727.
58. Lee Z, Weidemann A, Kindle J, Arnone R, Carder KL, et al. (2007) Euphotic zone depth: Its derivation and implication to ocean-color remote sensing. J Geophys Res 112: C03009.
59. Weeks S, Werdell PJ, Schaffelke B, Canto M, Lee ZP, et al. (2012) Satellite-derived photic depth on the great barrier reef: spatio-temporal patterns of water clarity. Remote Sens 4: 3781-3795.
60. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods: PRIMER-E Ltd.
61. Oliver TA, Palumbi SR, (2009) Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Mar Ecol Prog Ser 378: 93-103.
62. Dove SG, Lovell C, Fine M, Deckenback J, Hoegh-Guldberg O, et al. (2008) Host pigments: potential facilitators of photosynthesis in coral symbioses. Plant Cell Environ 31: 1523-1533.
63. Enriquez S, Mendez ER, Iglesias-Prieto R, (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanog 50: 1025-1032.
64. Weeks SJ, Bakun A, Steinberg CR, Brinkman R, Hoegh-Guldberg O, (2010) The Capricorn Eddy: a prominent driver of the ecology and future of the southern Great Barrier Reef. Coral Reefs 29: 975-985.
65. Middlebrook R, Hoegh-Guldberg O, Leggat W, (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211: 1050-1056.
66. Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, et al. (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE 7: e33353.
67. 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-reefal coral communities. Zool Stud 42: 540-550.
68. Lien Y-T, Nakano Y, Plathong S, Fukami H, Wang J-T, et al. (2007) Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26: 35-44.
69. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, et al. (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Clim Change 2: 116-120.
70. Silverstein RN, Correa AMS, LaJeunesse TC, Baker AC, (2011) Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar Ecol Prog Ser 422: 63-75.
71. Chen CA, Yang YW, Wei NV, Tsai WS, Fang LS, (2005) Symbiont diversity in scleractinian corals from tropical reefs and subtropical non-reef communities in Taiwan. Coral Reefs 24: 11-22.
72. Lien Y-T, Fukami H, Yamashita Y, (2012) Symbiodinium clade C dominates zooxanthellate corals (Scleractinia) in the temperate region of Japan. Zool Sci 29: 173-180.
73. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, et al. (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci U S A 101: 13531-13535.
74. LaJeunesse TC, Smith RT, Finney J, Oxenford H, (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proc Roy Soc Lond B 276: 4139-4148.
75. Venn AA, Loram JE, Trapido-Rosenthal HG, Joyce DA, Douglas AE, (2008) Importance of time and place: patterns in abundance of Symbiodinium clades A and B in the tropical sea anemone Condylactis gigantea. Biol Bull 215: 243-252.
76. Alongi DM, Trott LA, Mohl M, (2011) Strong tidal currents and labile organic matter stimulate benthic decomposition and carbonate fluxes on the southern Great Barrier Reef shelf. Cont Shelf Res 31: 1384-1395.
77. McGinley M, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, et al. (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.
78. Stat M, Loh WKW, LaJeunesse TC, Hoegh-Guldberg O, Carter DA, (2009) Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28: 709-713.