Long-term changes in Symbiodinium communities in Orbicella annularis in St. John, US Virgin Islands

Marine Ecology Progress Series

Volumn 506, Issue , 2014, Pages 129-144

  Edmunds, Peter J ^a   Pochon, Xavier ^b,c   Levitan, Don R ^d   Yost, Denise M ^b   Belcaid, Mahdi ^b   Putnam, Hollie M ^b   Gates, Ruth D ^b  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c CAWTHRON INSTITUTE   (New Zealand)

^d FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Ecology; Genetics; Long term; Montastraea; Orbicella; Symbiodinium; Virgin Islands

Indexed keywords

CHLOROPLAST; CLADISTICS; CORAL REEF; DINOFLAGELLATE; GENETIC MARKER; GENOTYPE; GROWTH; INTERSPECIFIC INTERACTION; LONG-TERM CHANGE; MICROHABITAT;

LEEWARD ISLANDS [LESSER ANTILLES]; SAINT JOHN [VIRGIN ISLANDS (U.S.)]; VIRGIN ISLANDS; VIRGIN ISLANDS (U.S.);

EID: 84903288670     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps10808     Document Type: Article

References (75)

1. AbramoffMD, Magalhaes PJ, Ram SJ (2004) Image processing with Image J. Biophotonics 11: 36-42
2. 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
3. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of longterm impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80: 435-471
4. Baker DM, Weigt L, Fogel M, Knowlton N (2013) Ancient DNA from coral-hosted Symbiodinium reveal a static mutualism over the last 172 years. PLoS ONE 8: e55057
5. 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 Biol Sci 273: 2305-2312
6. Bruno JF, Edmunds PJ (1997) Clonal variation for phenotypic plasticity in the coral Madracis mirabilis. Ecology 78: 2177-2190
7. Budd AF, Fukami H, Smith ND, Knowlton N (2012) Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozao: Scleractinia). Zool J Linn Soc 166: 465-529
8. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43: 320-326
9. Cantin NE, van Oppen MJH, Willis BL, Mieog JC, Negri AP (2009) Juvenile corals can acquire more carbon from highperformance algal symbionts. Coral Reefs 28: 405-414
10. Connell JH (1973) Population ecology of reef-building corals, Vol 2. In: Jones OA, Endean R (eds) Biology and geology of coral reefs. Academic Press, New York, NY, p 204-245
11. Cooper TF, Berkelmans R, Ulstrup KE, Weeks S, Radford B, Jones AM, Goyle J, Canto M, O'Leary RA, van Oppen MJH (2011) Environmental factors controlling the distribution of Symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef. PLoS ONE 6: e25536
12. Correa AMS, Brandt ME, Smith TB, Thornhill DJ, Baker AC (2009) Symbiodinium associations with diseased and healthy scleractinian corals. Coral Reefs 28: 437-448
13. De'ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA 109: 17995-17999
14. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461
15. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200
16. Edmunds PJ (2013) Decadal-scale changes in the community structure of coral reefs in St. John, US Virgin Islands. Mar Ecol Prog Ser 489: 107-123
17. Edmunds PJ, Elahi R (2007) The demographic of a 15-year decline in cover of the Caribbean reef coral Montastraea annularis. Ecol Monogr 77: 3-18
18. 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 Resour 12: 369-373
19. Garren M, Walsh SM, Caccone A, Knowlton N (2006) Patterns of association between Symbiodinium and members of the Montastraea annularis complex on spatial scales from within colonies to between geographic regions. Coral Reefs 25: 503-512
20. Goreau TF (1959) The ecology of Jamaican coral reefs. I. Species composition and zonation. Ecology 40: 67-90
21. Gosz JR, Waide RB, Magnuson JJ (2010) Twenty-eight years of the US-LTER program: experience, results, and re-search questions. In: Muller F, Baessler C, Schubert H, Klotz S (eds) Long-term ecological research. Springer Sciences + Business Media BV, p 59-74
22. Green EA, Davies SW, Matz MV, Medina M (2013) Nextgeneration sequencing reveals cryptic Symbiodinium diversity within Orbicella faveolata and Orbicella franksi at the Flower Garden Banks, Gulf of Mexico. PeerJ 2:e386
23. Hairston NJ, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8: 1114-1127
24. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98
25. Hoegh-Guldberg O (1999) Coral bleaching, climate change and the future of the world's coral reefs. Mar Freshw Res 50: 839-866
26. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS and others (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742
27. Hughes TP, Jackson JBC (1980) Do corals lie about their age? Some demographic consequences of partial mortality, fission, and fusion. Science 209: 713-715
28. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54: 187-211
29. Huse SM, Dethlefsen L, Huber JA, Mark Welch D and others (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4: e1000255
30. 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 Biol Sci 271: 1757-1763
31. Jablonski D, Sepkoski JJ (1996) Paleobiology, community ecology, and scales of ecological pattern. Ecology 77: 1367-1378
32. Jeong HJ, Yoo YD, Kang NS, Lim AS and others (2012) Hetero trophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc Natl Acad Sci USA 109: 12604-12609
33. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endo-symbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc Biol Sci 275: 1359-1365
34. Keitt TH (2008) Coherent ecological dynamics induced by large-scale disturbance. Nature 454: 331-334
35. Kemp DW, Fitt WK, Schmidt GW (2008) A microsampling method for genotyping coral symbionts. Coral Reefs 27: 289-293
36. Knowlton N, Weil E, Leigt LA, Guzman HM (1992) Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255: 330-333
37. Kohler KE, Gill SM (2006) Coral point count with excel extensions (CPCe): a visual basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32: 1259-1269
38. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and physiology of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a 'species' level marker. J Phycol 37: 866-880
39. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141: 387-400
40. 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
41. Lindenmayer DB, Likens GE (2010) The science and application of ecological monitoring. Biol Conserv 143: 1317-1328
42. Little AF, van Oppen NJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304: 1492-1494
43. Loya Y (1972) Community structure and species diversity of hermatypic corals at Eilat, Red Sea. Mar Biol 13: 100-123
44. Maniatis T, Fritsch E, Sambrook J (1989) Molecular cloning; a laboratory manual. Cold Spring Harbor Press, Princeton, NJ
45. McWilliams JP, Cote IM, Gill JA, Sutherland WJ, Watkinson AR (2005) Accelerating impacts of temperature induced corals bleaching in the Caribbean. Ecology 86: 2055-2060
46. Miller J, Muller E, Rogers C, Waara R and others (2009) Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28: 925-937
47. Nichols JD, Williams BK (2006) Monitoring for conservation. Trends Ecol Evol 21: 668-673
48. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol Phylogenet Evol 56: 492-497
49. 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
50. Pochon X, Garcia-Cuetes L, Baker AC, Castella E, Pawlowski J (2007) One-year survey of a single Micronesian reef reveals extraordinary rich diversity of Symbiodinium types in soritid foraminifera. Coral Reefs 26: 867-882
51. Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associated with environmental sensitivity in scleractinian corals. Proc Biol Sci 279: 4352-4361
52. Rowan R (2004) Thermal adaptations in reef coral symbionts. Nature 430: 742 (Pubitemid 39071338
53. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92: 2850-2853
54. Rowan R, Powers DA (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71: 65-73
55. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388: 265-269
56. Sampayo EM, Dove S, LaJeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18: 500-519
57. Severance EG, Szmant AM, Karl SA (2004) Single-copy gene markers isolated from the Caribbean coral Montastraea annularis. Mol Ecol Notes 4: 167-169
58. Sogin ML, Morrison HG, Huber JA, Welch DM and others (2006) Microbial diversity in the deep sea and the underexplored 'rare biosphere'. Proc Natl Acad Sci USA 103: 12115-12120
59. Stat M, Morris E, Gates RD (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA 105: 9256-9261
60. Stat M, Pochon X, Cowie ROM, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386: 83-96
61. Stat M, Bird CE, Pochon X, Chasqui L and others (2011) Variation in Symbiodinium ITS2 sequence assemblages among coral colonies. PLoS ONE 6: e15854
62. Takabayashi M, Adams L, Pochon X, Gates RD (2012) Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai'i and Florida. Coral Reefs 31: 157-167
63. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or postbleaching reversion. Mar Biol 148: 711-722
64. Thornhill DJ, Xiang Y, Fitt WK, Santos SR (2009) Reef endemism, host specificity and temporal stability in pop ulations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS ONE 4: e6262
65. Thornhill DJ, Rotjan RD, Todd BD, Chilcoat GC and others (2011) A connection between colony biomass and death in Caribbean reef-building corals. PLoS ONE 6: e29535
66. Toller WW, Rowan R, Knowlton N (2001a) Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol Bull 201: 348-359
67. Toller WW, Rowan R, Knowlton N (2001b) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull 201: 360-373
68. Tonk L, Sampayo EM, Weeks S, Magno-Canto M, Hoegh-Guldberg O (2013) Host-specific interactions with environmental factors shape the distribution of Symbiodi-nium across the Great Barrier Reef. PLoS ONE 8: e68533
69. Valiere N (2002) GIMLET: a computer program for analyzing genetic individual identification data. Mol Ecol Notes 2: 377-379
70. van Hooidonk R, Maynard JA, Manzello D, Planes S (2014) Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs. Glob Change Biol 20: 103-112
71. van Oosterhout C, Hutchinson W, Wills D, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535-538
72. van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15: 3863-3883
73. 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
74. Weil E, Knowlton N (1994) A multi-character analysis of the Caribbean coral Montastraea annularis (Ellis and Solander, 1786) and its two sibling species, M. faveolata (Ellis and Solander, 1786) and M. franksi (Gregory, 1895). Bull Mar Sci 55: 151-175
75. Woodley JD, Chornesky EA, Clifford PA, Jackson JBC and others (1981) Hurricane Allen's impact on Jamaican coral reefs. Science 214: 749-755