Population structure of Symbiodinium sp. associated with the common sea fan, Gorgonia ventalina, in the Florida Keys across distance, depth, and time

Marine Biology

Volumn 156, Issue 8, 2009, Pages 1609-1623

  Kirk, Nathan L ^a,c   Andras, Jason P ^b   Harvell, C Drew ^b   Santos, Scott R ^c   Coffroth, Mary Alice ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c AUBURN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DINOFLAGELLATE; ENDOSYMBIONT; GENETIC STRUCTURE; GREEN ALGA; POPULATION STRUCTURE; ZOOXANTHELLA;

FLORIDA [UNITED STATES]; FLORIDA KEYS; NORTH AMERICA; UNITED STATES;

DINOPHYCEAE; GORGONIA; GORGONIA VENTALINA; INVERTEBRATA; SYMBIODINIUM; SYMBIODINIUM SP.;

EID: 67349085161     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-009-1196-z     Document Type: Article

References (137)

1. D Abrego KE Ulstrup BL Willis MJH van Oppen 2008 Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress Proc R Soc Lond B Biol Sci 275 2273 2282 10.1098/rspb.2008.0180
2. Andras JP, Kirk NL, Coffroth MA, Harvell CD (2009) Isolation and characterization of microsatellite loci in Symbiodinium B1/B184, the dinoflagellate symbiont of the Caribbean sea fan coral, Gorgonia ventalina. Mol Ecol Res. doi: 10.1111/j.1755-0998.2009.02549.x
3. S Arnaud-Haond K Belkhir 2007 GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization Mol Ecol Notes 7 15 17 10.1111/j.1471-8286.2006.01522.x
4. AC Baker 2001 Reef corals bleach to survive change Nature 411 765 766 10.1038/35081151
5. AC Baker 2003 Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium Annu Rev Ecol Evol Syst 34 661 689 10.1146/annurev.ecolsys.34.011802.132417 (Pubitemid 38171434)
6. F Balloux L Lehmann T de Meeus 2003 The population genetics of clonal and partially clonal diploids Genetics 164 1635 1644 (Pubitemid 37102223)
7. AC Barbrook S Visram AE Douglas CJ Howe 2006 Molecular diversity of dinoflagellate symbionts of cnidaria: the psbA minicircle of Symbiodinium Protist 157 159 171 10.1016/j.protis.2005.12.002
8. Bayer FM (1961) The shallow-water Octocorallia of the West Indian region. Martinus Nijhoff, The Hague
9. R Berkelmans MJH 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 Lond B Biol Sci 273 2305 2312 10.1098/rspb.2006.3567
10. Birkeland C (1974) The effect of wave action on the population dynamics of Gorgonia ventalina Linnaeus. In: Bayer FM (ed) Prostaglandins from Plexaura homomalla: ecology, utilization and conservation of a major medical marine resource. Studies in Tropical Oceanography, pp 115-126
11. RJ Blank 1987 Cell architecture of the dinoflagellate Symbiodinium sp. inhabiting the Hawaiian stony coral Montipora verrucosa Mar Biol (Berl) 94 143 155 10.1007/BF00392906
12. RJ Blank VAR Huss 1989 DNA divergency and speciation in Symbiodinium (Dinophyceae) Plant Syst Evol 163 153 163 10.1007/BF00936511
13. RJ Blank VAR Huss W Kersten 1988 Base composition of DNA from symbiotic dinoflagellates: a tool for phylogenetic classification Arch Microbiol 149 515 520 10.1007/BF00446754
14. J Boenigk K Pfandl T Garstecki H Harms G Novarino A Chatzinotas 2006 Evidence for geographic isolation and signs of endemism within a protistan morphospecies Appl Environ Microbiol 72 5159 5164 10.1128/AEM.00601-06
15. MJ Caley MH Carr MA Hixon TP Hughes GP Jones BA Menge 1996 Recruitment and the local dynamics of open marine populations Annu Rev Ecol Syst 27 477 500 10.1146/annurev.ecolsys.27.1.477
16. AA Carlos BK Baillie M Kawachi T Maruyama 1999 Phylogenetic position of Symbiodinium (dinophyceae) isolates from tridacnids (bivalvia), cardids (bivalvia), a sponge (porifera), a soft coral (anthozoa), and a free-living strain J Phycol 35 1054 1062 10.1046/j.1529-8817.1999.3551054.x (Pubitemid 29530809)
17. SS Chang BB Prezelin RK Trench 1983 Mechanisms of photoadaption in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum Mar Biol (Berl) 76 219 229 10.1007/BF00393021
18. MA Coffroth SR Santos 2005 Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium Protist 156 19 34 10.1016/j.protis.2005.02.004
19. MA Coffroth HR Lasker ME Diamond JA Bruenn E Bermingham 1992 DNA fingerprints of a gorgonian coral: a method for detecting clonal structure in a vegetative species Mar Biol (Berl) 114 317 325 10.1007/BF00349534 (Pubitemid 23404985)
20. MA Coffroth SR Santos TL Goulet 2001 Early ontogenetic expression of specificity in a cnidarian-algal symbiosis Mar Ecol Prog Ser 222 85 96 10.3354/meps222085 (Pubitemid 33141576)
21. MA Coffroth CF Lewis SR Santos JL Weaver 2006 Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians Curr Biol 16 R985 R987 10.1016/j.cub.2006.10.049
22. NJ Colley RK Trench 1983 Selectivity in phagocytosis and persistence of symbiotic algae by the scyphistoma stage of the jellyfish Cassiopeia xamachana Proc R Soc Lond B Biol Sci 219 61 82 10.1098/rspb.1983.0059
23. J DeWoody JD Nason VD Hipkins 2006 Mitigating scoring errors in microsatellite data from wild populations Mol Ecol Notes 6 951 957 10.1111/j.1471-8286.2006.01449.x
24. OE Diekmann RPM Bak L Tonk WT Stam JL Olsen 2002 No habitat correlation of zooxanthellae in the coral genus Madracis on a Curacao reef Mar Ecol Prog Ser 227 221 232 10.3354/meps227221 (Pubitemid 34235124)
25. JR Dolan 2005 Biogeography of aquatic microbes Aquat Microb Ecol 41 39 48 10.3354/ame041039
26. JR Dolan 2006 Microbial biogeography? J Biogeogr 33 199 200 10.1111/j.1365-2699.2005.01406.x
27. SD Donner WJ Skirving CM Little M Oppenheimer O Hoegh-Guldberg 2005 Global assessment of coral bleaching and required rates of adaptation under climate change Glob Change Biol 11 2251 2265 10.1111/j.1365-2486.2005.01073.x
28. SD Donner TR Knutson M Oppenheimer 2007 Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event Proc Natl Acad Sci USA 104 5483 5488 10.1073/pnas.0610122104
29. PJ Edmunds JF Bruno DB Carlon 2004 Effects of depth and microhabitat on growth and survivorship of juvenile corals in the Florida Keys Mar Ecol Prog Ser 278 115 124 10.3354/meps278115 (Pubitemid 39379425)
30. H Ellegren 2004 Microsatellites: simple sequences with complex evolution Nat Rev Genet 5 435 445 10.1038/nrg1348
31. G Evanno S Regnaut J Goudet 2005 Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study Mol Ecol 14 2611 2620 10.1111/j.1365-294X.2005.02553.x
32. L Excoffier PE Smouse JM Quattro 1992 Analysis of molecular variation inferred from metric distances among DNA haplotypes: applications to human mitochondrial DNA restriction data Genetics 131 479 491
33. L Excoffier G Laval S Schneider 2005 Arlequin ver. 3.0: an integrated software package for population genetics data analysis Evol Bioinform Online 1 47 50
34. D Falush M Stephens JK Pritchard 2003 Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies Genetics 164 1567 1587 (Pubitemid 37102217)
35. T Fenchel 2001 How dinoflagellates swim Protist 152 329 338 10.1078/1434-4610-00071 (Pubitemid 34085317)
36. T Fenchel BJ Finlay 2004 The ubiquity of small species: patterns of local and global diversity Bioscience 54 777 784 10.1641/0006-3568(2004)054[0777: TUOSSP]2.0.CO;2 (Pubitemid 39073976)
37. BJ Finlay T Fenchel 2004 Cosmopolitan metapopulations of free-living microbial eukaryotes Protist 155 237 244 10.1078/143446104774199619
38. WK Fitt 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 (Berl) 81 9 17 10.1007/BF00397620
39. WK Fitt RK Trench 1983 The relationship of diel patterns of cell division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture New Phytol 94 421 432 10.1111/j.1469-8137.1983.tb03456.x
40. W Foissner 2006 Biogeography and dispersal of micro-organisms: a review emphasizing protists Acta Protozool 45 111 136 (Pubitemid 43772500)
41. PR Frade P Bongaerts AJS Winkelhagen L Tonk RPM Bak 2008 In situ photobiology of corals over large depth ranges: a multivariate analysis on the roles of environment, host, and algal symbiont Limnol Oceanogr 53 2711 2723
42. PR Frade N Englebert J Faria PM Visser RPM Bak 2008 Distribution and photobiology of Symbiodinium types in different light environments for three colour morphs of the coral Madracis pharensis: is there more to it than total irradiance? Coral Reefs 27 913 925 10.1007/s00338-008-0406-3
43. HD Freudenthal 1962 Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology J Protozool 9 45 52
44. PW Glynn 1996 Coral reef bleaching: facts, hypotheses, and implications Glob Change Biol 2 495 509 10.1111/j.1365-2486.1996.tb00063.x (Pubitemid 126670990)
45. TL Goulet MA Coffroth 2003 Stability of an octocoral-algal symbiosis over time and space Mar Ecol Prog Ser 250 117 124 10.3354/meps250117 (Pubitemid 36524322)
46. TL Goulet MA Coffroth 2004 The genetic identity of dinoflagellate symbionts in Caribbean octocorals Coral Reefs 23 465 472 (Pubitemid 40393758)
47. TL Goulet CB Cook D Goulet 2005 Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallida/Symbiodinium symbiosis Limnol Oceanogr 50 1490 1498 (Pubitemid 41356430)
48. J Green BJM Bohannan 2006 Spatial scaling of microbial biodiversity Trends Ecol Evol 21 501 507 10.1016/j.tree.2006.06.012
49. Y Harada S Kawano Iwasa 1997 Probability of clonal identity: inferring the relative success of sexual versus clonal reproduction from spatial genetic patterns J Ecol 85 591 600 10.2307/2960530 (Pubitemid 27447304)
50. H Hillebrand F Watermann R Karez U-G Berninger 2001 Differences in species richness patterns between unicellular and multicellular organisms Oecologia 126 114 124 10.1007/s004420000492
51. O Hoegh-Guldberg 1999 Climate change, coral bleaching and the future of the world's coral reefs Mar Freshw Res 50 839 866 10.1071/MF99078 (Pubitemid 30018479)
52. O Hoegh-Guldberg PJ Mumby AJ Hooten RS Steneck P Greenfield ED Gomez CD Harvell PF Sale AJ Edwards K Caldeira N Knowlton CM Eakin R Iglesias-Prieto N Muthiga RH Bradbury A Dubi ME Hatziolos 2007 Coral reefs under rapid climate change and ocean acidification Science 318 1737 10.1126/science.1152509
53. KE Holsinger RJ Mason-Gamer 1996 Hierarchical analysis of nucleotide diversity in geographically structured populations Genetics 142 629 639 (Pubitemid 26039230)
54. EJ Howells MJH van Oppen BL Willis 2009 High genetic differentiation and cross-shelf patterns of genetic diversity among Great Barrier Reef populations of Symbiodinium Coral Reefs 28 215 225 10.1007/s00338-008-0450-z
55. PL Jokiel 1984 Long distance dispersal of reef corals by rafting Coral Reefs 3 113 116 10.1007/BF00263761
56. RA Kinzie 1973 The zonation of West Indian gorgonians Bull Mar Sci 23 93 155
57. RA Kinzie 1974 Experimental infection of aposymbiotic gorgonian polyps with zooxanthellae J Exp Mar Biol Ecol 15 335 345 10.1016/0022-0981(74)90054-9
58. RA Kinzie G Chee 1979 The effect of different zooxanthellae on the growth of experimentally reinfected hosts Biol Bull 156 315 327 10.2307/1540920
59. NL Kirk JR Ward MA Coffroth 2005 Stable Symbiodinium composition in the sea fan Gorgonia ventalina during temperature and disease stress Biol Bull 209 227 234 10.2307/3593112 (Pubitemid 43068448)
60. B Kuguru NE Chadwick Y Achituv K Zandbank D Tchernov 2008 Mechanisms of habitat segregation between corallimorpharians: photosynthetic parameters and Symbiodinium types Mar Ecol Prog Ser 369 115 129 10.3354/meps07651
61. TC LaJeunesse 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 37 866 880 10.1046/j.1529-8817.2001.01031.x
62. TC LaJeunesse 2002 Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs Mar Biol (Berl) 141 387 400 10.1007/s00227-002-0829-2
63. S Lampert-Karako N Stambler DJ Katcoff Y Achituv Z Dubinsky N Simon-Blecher 2008 Effects of depth and eutrophication on the zooxanthella clades of Stylophora pistillata from the Gulf of Eilat (Red Sea) Aquat Conserv Mar Freshw Ecosyst 18 1039 1045 10.1002/aqc.927
64. HR Lasker MA Coffroth 1983 Octocoral distributions at Carrie Bow Cay, Belize Mar Ecol Prog Ser 13 21 28 10.3354/meps013021
65. TN Lee N Smith 2002 Volume transport variability through the Florida Keys tidal channels Cont Shelf Res 22 1361 1377 10.1016/S0278-4343(02)00003-1
66. TN Lee E Williams 1999 Mean distribution and seasonal variability of coastal currents and temperature in the Florida Keys with implications for larval recruitment Bull Mar Sci 64 35 56 (Pubitemid 34067375)
67. TN Lee C Rooth E Williams M McGowan AM Szmant ME Clarke 1992 Influence of Florida Current, gyres and wind-driven circulation on transport of larvae and recruitment in the Florida Keys coral reefs Cont Shelf Res 12 971 1002 10.1016/0278-4343(92)90055-O (Pubitemid 23401179)
68. JJ Leichter SR Wing SL Miller MW Denny 1996 Pulsed delivery of subthermocline water to Conch Reef (Florida Keys) by internal tidal bores Limnol Oceanogr 41 1490 1501 (Pubitemid 126447244)
69. JJ Leichter G Shellenbarger SJ Genovese SR Wing 1998 Breaking internal waves on a Florida (USA) coral reef: a plankton pump at work? Mar Ecol Prog Ser 166 83 97 10.3354/meps166083 (Pubitemid 28286437)
70. JJ Leichter HL Stewart SL Miller 2003 Episodic nutrient transport to Florida coral reefs Limnol Oceanogr 48 1394 1407 (Pubitemid 36964760)
71. RA Littman MJH van Oppen BL Willis 2008 Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef) J Exp Mar Biol Ecol 364 48 53 10.1016/j.jembe.2008. 06.034
72. H Magalon E Baudry A Huste M Adjeroud M Veuille 2006 High genetic diversity of the symbiotic dinoflagellates in the coral Pocillopora meandrina from the South Pacific Mar Biol (Berl) 148 913 922 10.1007/s00227-005-0133-z
73. MM Manning RD Gates 2008 Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef Limnol Oceanogr 53 1853 1861
74. N Mantel 1967 The detection of disease clustering and a generalized regression approach Cancer Res 27 209 220
75. JBH Martiny BJM Bohannan JH Brown RK Colwell JA Fuhrman JL Green MC Horner-Devine M Kane JA Krumins CR Kuske PJ Morin S Naeem L Ovreas AL Reysenbach VH Smith JT Staley 2006 Microbial biogeography: putting microorganisms on the map Nat Rev Microbiol 4 102 112 10.1038/nrmicro1341
76. Y Michalakis L Excoffier 1996 A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci Genetics 142 1061 1064 (Pubitemid 26162549)
77. Miller MP (1997) Tools for population genetic analyses (TFPGA) 1.3
78. M Montresor S Sgrosso G Procaccini WHCF Kooistra 2003 Intraspecific diversity in Scrippsiella trochoidea (Dinophyceae): evidence for cryptic species Phycologia 41 56 70 (Pubitemid 36333443)
79. RB Moore KM Ferguson WKW Loh O Hoegh-Guldberg D Carter 2003 Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium Int J Syst Evol Microbiol 53 1725 1734 10.1099/ijs.0.02594-0
80. G Muller-Parker 1984 Dispersal of zooxanthellae on coral reefs by predators on cnidarians Biol Bull 167 159 10.2307/1541344
81. C Mundy R Babcock 2000 Are vertical distribution patterns of scleractinian corals maintained by pre- of post-settlement processes? A case study of three contrasting species Mar Ecol Prog Ser 198 109 119 10.3354/meps198109 (Pubitemid 30411277)
82. S Nagai C Lian S Yamaguchi M Hamaguchi Y Matsuyama S Itakura H Shimada S Kaga H Yamauchi Y Sonda T Nishikawa C-H Kim T Hogetsu 2007 Microsatellite markers reveal population genetic structure of the toxic dinoflagellate Alexandrium tamarense (Dinophyceae) in Japanese coastal waters J Phycol 43 43 54 10.1111/j.1529-8817.2006.00304.x
83. I Nagelkerken K Buchan GW Smith K Bonair P Bush J Garzon-Ferreira L Botero P Gayle CD Harvell C Heberer K Kim C Petrovic L Pors P Yoshioka 1997 Widespread disease in Caribbean sea fans: II. Patterns of infection and tissue loss Mar Ecol Prog Ser 160 255 263 10.3354/meps160255 (Pubitemid 28069546)
84. M Nei 1972 Genetic distance between populations Am Nat 106 283 292 10.1086/282771
85. M Nei 1978 Estimation of average heterozygosity and genetic distance from a small number of individuals Genetics 89 583 590 (Pubitemid 8396073)
86. DM Opresko 1973 Abundance and distribution of shallow-water gorgonians in the area of Miami, Florida Bull Mar Sci 23 535 558
87. SR Palumbi 1992 Marine speciation on a small planet Trends Ecol Evol 7 114 118 10.1016/0169-5347(92)90144-Z (Pubitemid 23395167)
88. RT Papke DM Ward 2004 The importance of physical isolation to microbial diversification FEMS Microbiol Ecol 48 293 303 10.1016/j.femsec.2004.03.013
89. SF Perez CB Cook WR Brooks 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 14 10.1016/S0022-0981(00)00282-3
90. J Pineda 1994 Internal tidal bores in the nearshore: warm-water fronts, seaward gravity currents and the onshore transport of neustonic larvae J Mar Res 52 427 458 10.1357/0022240943077046
91. PA Pitts 1994 An investigation of Near-bottom flow patterns along and across Hawk Channel, Florida Keys Bull Mar Sci 54 610 620
92. X Pochon JI Montoya-Burgos B Stadelmann J Pawlowski 2006 Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium Mol Phylogenet Evol 38 20 30 10.1016/j.ympev.2005.04.028
93. T Pommier B Canback L Riemann KH Bostrom K Simu P Lundberg A Tunlid A Hagstrom 2007 Global patterns of diversity and community structure in marine bacterioplankton Mol Ecol 16 867 880 10.1111/j.1365-294X.2006.03189.x
94. I Porto C Granados JC Restrepo JA Sanchez 2008 Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs PLoS ONE 3 e2160 10.1371/journal.pone.0002160
95. JK Pritchard M Stephens P Donnelly 2000 Inference of population structure using multilocus genotype data Genetics 155 945 959 (Pubitemid 30397141)
96. CM Roberts 1997 Connectivity and management of Caribbean coral reefs Science 278 1454 10.1126/science.278.5342.1454
97. NA Rosenberg 2004 DISTRUCT: a program for the graphical display of population structure Mol Ecol Notes 4 137 138 10.1046/j.1471-8286.2003.00566.x
98. F Rousset 1997 Genetic differentiation and estimation of gene flow from F statistics under isolation by distance Genetics 145 1219 1228 (Pubitemid 27149123)
99. F Rousset 2008 GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux Mol Ecol Res 8 103 106 10.1111/j.1471-8286.2007. 01931.x
100. R Rowan 2004 Thermal adaptations in reef coral symbionts Nature 430 742 10.1038/430742a
101. R Rowan N Knowlton 1995 Intraspecific diversity and ecological zonation in coral-algal symbiosis Proc Natl Acad Sci USA 92 2850 2853 10.1073/pnas.92.7.2850
102. R Rowan DA Powers 1991 Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae) Mar Ecol Prog Ser 71 65 73 10.3354/meps071065
103. EM Sampayo L Franceschinis O Hoegh-Guldberg S Dove 2007 Niche partitioning of closely related symbiotic dinoflagellates Mol Ecol 16 3721 3733 10.1111/j.1365-294X.2007.03403.x
104. JA Sanchez S Zea JM Diaz 1998 Patterns of octocoral and black coral distribution in the oceanic barrier reef-complex of Providencia Island, Southwestern Caribbean Caribb J Sci 34 250 264 (Pubitemid 29294406)
105. SR Santos MA Coffroth 2003 Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium Freudenthal are haploid Biol Bull 204 10 20 10.2307/1543491 (Pubitemid 36234313)
106. SR Santos DJ Taylor RA Kinzie M Hidaka K Sakai MA Coffroth 2002 Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences Mol Phylogenet Evol 23 97 111 10.1016/S1055- 7903(02)00010-6
107. SR Santos C Gutierrez-Rodriguez MA Coffroth 2003 Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23 s)-ribosomal DNA sequences Mar Biotechnol 5 130 140 (Pubitemid 36619160)
108. SR Santos C Gutierrez-Rodriguez HR Lasker MA Coffroth 2003 Symbiodinium sp. associations in the gorgonian Pseudopterogorgia elisabethae in the Bahamas: high levels of genetic variability and population structure in symbiotic dinoflagellates Mar Biol (Berl) 143 111 120 10.1007/s00227-003-1065-0
109. SR Santos TL Shearer AR Hannes MA Coffroth 2004 Fine-scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean Mol Ecol 13 459 469 10.1046/j.1365-294X.2003.02058.x
110. DA Schoenberg RK Trench 1980 Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum Proc R Soc Lond B Biol Sci 207 405 427 10.1098/rspb.1980.0031 (Pubitemid 10076088)
111. DA Schoenberg RK Trench 1980 Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. II. Morphological variation in Symbiodinium microadriaticum Proc R Soc Lond B Biol Sci 207 429 444 10.1098/rspb.1980.0032 (Pubitemid 10076089)
112. DA Schoenberg RK Trench 1980 Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of Symbiodinium microadriaticum Proc R Soc Lond B Biol Sci 207 445 460 10.1098/rspb.1980.0033 (Pubitemid 10076090)
113. G Seutin BN White PT Boag 1991 Preservation of avian blood and tissue samples for DNA analyses Can J Zool 69 82 90 10.1139/z91-013
114. AL Seyfert MEA Cristescu L Frisse S Schaack WK Thomas M Lynch 2008 The rate and spectrum of microsatellite mutation in Caenorhabditis elegans and Daphnia pulex Genetics 178 2113 2121 10.1534/genetics.107.081927
115. TL Shearer MA Coffroth 2006 Genetic identification of Caribbean scleractinian coral recruits at the Flower Garden Banks and the Florida Keys Mar Ecol Prog Ser 306 133 142 10.3354/meps306133 (Pubitemid 43241568)
116. M Slatkin 1995 A measure of population subdivision based on microsatellite allele frequencies Genetics 139 457 462
117. NP Smith 1994 Long-term Gulf-to-Atlantic transport through tidal currents in the Florida Keys Bull Mar Sci 54 602 609
118. N Smith 1998 Tidal and long-term exchanges through channels in the Middle and Upper Florida Keys Bull Mar Sci 62 199 211
119. JE Smith CM Smith PS Vroom KL Beach S Miller 2004 Nutrient and growth dynamics of Halimeda tuna on Conch Reef, Florida Keys: possible influence of internal tides on nutrient status and physiology Limnol Oceanogr 49 1923 1936 (Pubitemid 39547871)
120. PE Smouse JC Long RR Sokal 1986 Multiple regression and correlation extensions of the Mantel test of matrix correspondence Syst Zool 4 627 632 10.2307/2413122
121. S Sponaugle TN Lee V Kourafalou D Pinkard 2005 Florida Current frontal eddies and the settlement of coral reef fishes Limnol Oceanogr 50 1033 1048 (Pubitemid 41033828)
122. M Stat RD Gates 2008 Vectored introductions of marine endosymbiotic dinoflagellates into Hawaii Biol Invasions 10 579 583 10.1007/s10530-007-9167-0
123. M Takabayashi SR Santos CB Cook 2004 Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, dinophyta) J Phycol 40 160 164 (Pubitemid 38241647)
124. K Takishita M Ishikura K Koike T Maruyama 2003 Comparison of phylogenies based on nuclear-encoded SSU rDNA and plastid-encoded psbA in the symbiotic dinoflagellate genus Symbiodinium Phycologia 42 285 291 (Pubitemid 36774983)
125. Taylor DL (1974) Symbiotic marine algae: taxonomy and biological fitness. In: Vernberg WB (ed) Symbiosis in the Sea. University of South Carolina Press, Columbia, pp 245-262
126. Taylor FJR (1987) The biology of dinoflagellates. Blackwell, Oxford
127. WW Toller R Rowan N Knowlton 2001 Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths Biol Bull 201 348 359 10.2307/1543613 (Pubitemid 34057131)
128. KE Ulstrup R Berkelmans PJ Ralph MJH van Oppen 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 10.3354/meps314135 (Pubitemid 43989684)
129. KE Ulstrup R Hill MJH van Oppen AWD Larkum PJ Ralph 2008 Seasonal variation in the photo-physiology of homogeneous and heterogeneous Symbiodinium consortia in two scleractinian corals Mar Ecol Prog Ser 361 139 150 10.3354/meps07360
130. MJH van Oppen JC Mieog CA Sanchez KE Fabricius 2005 Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships Mol Ecol 14 2403 2417 10.1111/j.1365-294X.2005.02545.x
131. SA Wainwright JR Dillon 1969 On the orientation of sea fans (genus Gorgonia) Biol Bull 136 130 139 10.2307/1539674
132. ME Warner TC LaJeunesse JD Robison RM Thur 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 (Pubitemid 44185739)
133. TP Wilcox 1998 Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: morphology does not recapitulate phylogeny Mol Phylogenet Evol 10 436 448 10.1006/mpev.1998.0546
134. JF Willemsen 2005 Ocean circulation and impacts on plankton near the Florida Keys Physica A 357 36 43 10.1016/j.physa.2005.05.069
135. T Yacobovitch Y Benayahu VM Weis 2004 Motility of zooxanthellae isolated from the Red Sea soft coral Heteroxenia fuscescens (Cnidaria) J Exp Mar Biol Ecol 298 35 48 10.1016/j.jembe.2003.08.003
136. C Yeung TN Lee 2002 Larval transport and retention of the spiny lobster, Panulirus argus, in the coastal zone of the Florida Keys, USA Fish Oceanogr 11 286 309 10.1046/j.1365-2419.2002.00209.x
137. C Yeung DJ Jones MM Criales TL Jackson WJ Richards 2001 Influence of coastal eddies and counter-currents on the influx of spiny lobster, Panuliris argus, postlarvae into Florida Bay Mar Freshw Res 52 1217 1232 10.1071/MF01110