Marine Biodiversity

, Volume 43, Issue 4, pp 261–272 | Cite as

Ecological and biogeographic implications of Siderastrea symbiotic relationship with Symbiodinium sp. C46 in Sal Island (Cape Verde, East Atlantic Ocean)

  • João G. MonteiroEmail author
  • Cristiane F. Costa
  • Krystyna Gorlach-Lira
  • William K. Fitt
  • Sergio S. Stefanni
  • Roberto Sassi
  • Ricardo S. Santos
  • Todd C. LaJeunesse
Original Paper


The relative abundance of the genus Siderastrea and its relationship with temperature and irradiance was assessed around Sal Island (Cape Verde). In some of the surveyed sites, these corals accounted for 80–90 % of the living cover, making it a biotope-dominant organism. Unlike Siderastrea corals from West Atlantic and Caribbean locations, genetic analyses of the dinoflagellate symbiotic partner revealed high specificity between Siderastrea sp. in Cape Verde and the Symbiodinium type C46. Biotope restriction of the ecological success of Siderastrea in Cape Verde may be explained in part by this host–symbiont partnership, resulting locally in a small optimum ecological niche with specific light intensity regimes. Distinctively, West Atlantic and Caribbean Siderastrea associates with a much broader range of Symbiodinium diversity, suggesting that these symbioses exhibit some flexibility under differing environmental conditions where these corals occupy a wider range of ecological niches. Geographic isolation and/or long-standing environmental conditions are probably responsible for such adaptions and coral–dinoflagellate symbioses. Additional genetic analyses on Clade C Symbiodinium associated with Siderastrea were conducted with the hyper-variable plastid psbA minicircle to resolve phylogeographic patterns that indicate the relative connectivity and/or isolation of these symbionts throughout the tropical Atlantic.


Coral reef Siderastrea Symbiodinium Diversity Biogeography Endosymbiosis 



We wish to thank Cape Verde Diving, Dunas de Sal and Scuba Caribe dive operators who provided help and logistic support to all fieldwork in Cape Verde. We thank the Brazilian students Tatiana P. de Leon Amorim and Carolina da Rocha Simões for help with collections and processing of samples. D. Thornhill provided several psbA sequences from colonies of Siderastrea monitored near Lee Stocking Island, Bahamas. We also thank all reviewers for their comments and contributions. This research was also part of J.M.’s doctoral research program (SFRH/BD/27869/2009), funded by the Portuguese Foundation for Science and Technology (FCT). Funding for this research was also provided by the IOC-UNESCO-World Bank Targeted working group on coral bleaching and Pennsylvania State University. IMAR-DOP/UAz (Research and Development Unit no. 531) and LarSyS-Associated Laboratory are supported by the Portuguese Foundation for Science and Technology (FCT) under a strategic project and DRCTC-GR Azores through a Pluriannual Funding scheme (COMPETE and PRO-Convergência). Exchange of specimens was made possible by a Material Transfer Agreement between Penn State University and the Universidade Federal da Paraiba and by CITES permit 02/2008 issued by Direcção Geral do Ambiente, Cape Verde.


  1. Acker J, Leptoukh G (2007) Online analysis enhances use of NASA earth science data. Eos Trans Am Geophys Union 88:14–17CrossRefGoogle Scholar
  2. Avise JC, Wollenberg K (1997) Phylogenetics and the origin of species. Proc Natl Acad Sci USA 94:7748–7755PubMedCrossRefGoogle Scholar
  3. Baillie B, Belda-Baillie C, Silvestre V, Sison M, Gomez AV, Gomez ED, Monje V (2000) Genetic variation in Symbiodinium isolates from giant clams based on random-amplified-polymorphic DNA (RAPD) patterns. Mar Biol 136:829–836CrossRefGoogle Scholar
  4. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Coral reefs: corals' adaptive response to climate change. Nature 430:741PubMedCrossRefGoogle Scholar
  5. Barbrook A, Visram S, Douglas A, Howe C (2006) Molecular diversity of dinoflagellate symbionts of cnidaria: the psbA minicircle of Symbiodinium. Protist 157:159–171PubMedCrossRefGoogle Scholar
  6. 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 Lond B 273:2305–2312CrossRefGoogle Scholar
  7. Bohren CF, Huffmann DR (1983) Absorption and scattering of light by small particles. Wiley, New YorkGoogle Scholar
  8. Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic Divergence across Habitats in the Widespread Coral Seriatopora hystrix and Its Associated Symbiodinium. PLoS ONE 5:e10871Google Scholar
  9. Braby H (1913) The Harmattan wind of the Guinea Coast. Q J R Meteorol Soc 39:301–306CrossRefGoogle Scholar
  10. Castillo KD, Ries JB, Weiss JM (2011) Declining coral skeletal extension for forereef colonies of Siderastrea siderea on the Mesoamerican Barrier Reef System, Southern Belize. PLoS ONE 6:e14615PubMedCrossRefGoogle Scholar
  11. Colombo-Pallotta MF, Rodríguez-Román A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907CrossRefGoogle Scholar
  12. Costa CF, Sassi R, Gorlach-Lira K (2008) Zooxanthellae genotypes in the coral Siderastrea stellata from coastal reefs in northeastern Brazil. J Exp Mar Biol Ecol 367:149–152CrossRefGoogle Scholar
  13. Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, LaJeunesse TC (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 60:250–263PubMedCrossRefGoogle Scholar
  14. Fitt W, Brown B, Warner M, Dunne R (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65CrossRefGoogle Scholar
  15. Floeter SR, Rocha LA, Robertson DR, Joyeux JC, Smith-Vaniz WF, Wirtz P, Edwards AJ, Barreiros JP, Ferreira CEL, Gasparini JL, Brito A, Falcón JM, Bowen BW, Bernardi G (2007) Atlantic reef fish biogeography and evolution. J Biogeogr 35:22–47Google Scholar
  16. Foster AB (1980) Environmental variation in skeletal morphology within the Caribbean Reef Corals Montastraea annularis and Siderastrea siderea. Bull Mar Sci 30:678–709Google Scholar
  17. Garrison VH, Shinn EA, Foreman WT, Griffin DW, Holmes CW, Kellogg CA, Majewski MS, Richardson LL, Ritchie KB, Smith GW (2003) African and Asian dust: from desert soils to coral reefs. Bioscience 53:469–480CrossRefGoogle Scholar
  18. Gill JA, Watkinson AR, McWilliams JP, Cote IM (2006) Opposing forces of aerosol cooling and El Nino drive coral bleaching on Caribbean reefs. Proc Natl Acad Sci USA 103:18870–18873PubMedCrossRefGoogle Scholar
  19. Goulet T, LaJeunesse TC, Fabricius K (2008) Symbiont specificity and bleaching susceptibility among soft corals in the 1998 Great Barrier Reef mass coral bleaching event. Mar Biol 154:795–804CrossRefGoogle Scholar
  20. Griffin D, Garrison V, Herman J, Shinn E (2001) African desert dust in the Caribbean atmosphere: microbiology and public health. Aerobiologia 17:203–213CrossRefGoogle Scholar
  21. Hallock P (1981) Algal symbiosis: a mathematical analysis. Mar Biol 62:249–255CrossRefGoogle Scholar
  22. Hoegh-Guldberg O (2004) Coral reefs in a century of rapid environmental change. Symbiosis 37:1–31Google Scholar
  23. Hoeksema BW, Roos PJ, Cadée GC (2012) Trans-Atlantic rafting by the brooding reef coral Favia fragum on man-made flotsam. Mar Ecol Prog Ser 445:209–218CrossRefGoogle Scholar
  24. Iglesias-Prieto R, Trench R (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 113:163–175CrossRefGoogle Scholar
  25. Iglesias-Prieto R, Beltrán VH, LaJeunesse TC, Reyes-Bonilla H, Thomé PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Lond B 271:1757–1763CrossRefGoogle Scholar
  26. Kemp D, Cook C, LaJeunesse TC, Brooks W (2006) A comparison of the thermal bleaching responses of the zoanthid Palythoa caribaeorum from three geographically different regions in south Florida. J Exp Mar Biol Ecol 335:266–276CrossRefGoogle Scholar
  27. Kohler K, Gill S (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 32:1259–1269CrossRefGoogle Scholar
  28. Laborel J (1974) West African Reef Corals, an hypothesis on their origin. Proc 2nd Int Coral Reef Symp 1:425–443Google Scholar
  29. LaJeunesse TC (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 37:866–880CrossRefGoogle Scholar
  30. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400CrossRefGoogle Scholar
  31. LaJeunesse TC (2005) “‘Species’” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581PubMedCrossRefGoogle Scholar
  32. 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:e29013PubMedCrossRefGoogle Scholar
  33. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O (2003) Low symbiont diversity in Southern Great Barrier Reef Corals, relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054CrossRefGoogle Scholar
  34. LaJeunesse TC, Bhagooli R, Hidaka M, de Vantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004a) 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
  35. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW (2004b) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603Google Scholar
  36. LaJeunesse TC, Pettay D, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (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 37:785–800CrossRefGoogle Scholar
  37. Lewis J (1989) Spherical growth in the Caribbean coral Siderastrea radians (Pallas) and its survival in disturbed habitats. Coral Reefs 7:161–167CrossRefGoogle Scholar
  38. Li X, Maring H, Savoie D, Voss K (1996) Dominance of mineral dust in aerosol light-scattering in the North Atlantic trade winds. Nature 380:416–419CrossRefGoogle Scholar
  39. Lirman D, Manzello D (2009) Patterns of resistance and resilience of the stress-tolerant coral Siderastrea radians (Pallas) to sub-optimal salinity and sediment burial. J Exp Mar Biol Ecol 369:72–77CrossRefGoogle Scholar
  40. Lirman D, Manzello D, Maciá S (2002) Back from the dead: the resilience of Siderastrea radians to severe stress. Coral Reefs 21:291–292Google Scholar
  41. Littman RA, van Oppen MJH, Willis BL (2008) Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). J Exp Mar Biol Ecol 364:48–53CrossRefGoogle Scholar
  42. Monteiro P, Ribeiro D, Silva JA, Bispo J, Gonçalves J (2008) Ichthyofauna assemblages from two unexplored Atlantic seamounts: Northwest Bank and João Valente Bank (Cape Verde Archipelago). Sci Mar 72:133–143CrossRefGoogle Scholar
  43. Monteiro J, Almeida C, Freitas R, Delgado A, Porteiro F, Santos RSS (2009) Coral assemblages of Cape Verde: preliminary assessment and description. Proc 11th Int Coral Reef Symp 2:1416–1419Google Scholar
  44. Moore RB, Ferguson KM, Loh WKW, Hoegh-Guldberg O, Carter D (2003) Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium. Int J Syst Evol Microbiol 53:1725–1734PubMedCrossRefGoogle Scholar
  45. Morri C, Bianchi C (1995) Cnidarian Zonation at Ilha do Sal (Arquipélago de Cape Verde). Beitr Paläontol 20:41–49Google Scholar
  46. Moses C, Helmle K, Swart P, Dodge E, Merino SE (2003) Pavements of Siderastrea radians on Cape Verde reefs. Coral Reefs 22:506. doi: 10.1007/s00338-003-0346-x
  47. Muller-Parker G, D'Elia C (1997) Interactions between corals and their symbiotic algae. In: Birkeland C (ed) Life and death of coral reefs. Chapman and Hall, New York, pp 96–113CrossRefGoogle Scholar
  48. Muscatine L, McCloskey L, Marian R (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611CrossRefGoogle Scholar
  49. Neves E, Andrade S, Silveira F, Solferini V (2008) Genetic variation and population structuring in two brooding coral species (Siderastrea stellata and Siderastrea radians) from Brazil. Genetica 132:243–254PubMedCrossRefGoogle Scholar
  50. Nunes F, Norris RD, Knowlton D (2011) long distance dispersal and connectivity in Amphi-Atlantic Corals at regional and basin scales. PLoS ONE 6:e22298PubMedCrossRefGoogle Scholar
  51. Oigman-Pszczol S, Creed J (2004) Size structure and spatial distribution of the corals Mussismilia hispida and Siderastrea stellata (Scleractinia) at Armação dos Búzios, Brazil. Bull Mar Sci 74:433–448Google Scholar
  52. Oliver TA, Palumbi SR (2010) Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30:241–250CrossRefGoogle Scholar
  53. Pearse VB, Muscatine L (1971) Role of symbiotic algae (Zooxanthellae) in coral calcification. Biol Bull 141:350–363CrossRefGoogle Scholar
  54. Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27CrossRefGoogle Scholar
  55. Pochon X, Stat M, Takabayashi M, Chasqui L, Chauka LJ, Logan DDK, Gates RD (2010) Comparison of endosymbiotic and free-living Symbiodinium (dinophyceae) diversity in a Hawaiian reef environment. J Phycol 46:53–65CrossRefGoogle Scholar
  56. Rocha LA, Rocha CR, Robertson DR, Bowen BW (2008) Comparative phylogeography of Atlantic reef fishes indicates both origin and accumulation of diversity in the Caribbean. BMC Evol Biol 8:157–173PubMedCrossRefGoogle Scholar
  57. Rodriguez-Lanetty M, Krupp DA, Weis VM (2004) Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Mar Ecol Prog Ser 275:97–102CrossRefGoogle Scholar
  58. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269PubMedCrossRefGoogle Scholar
  59. Sampayo E, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16:3721–3733PubMedCrossRefGoogle Scholar
  60. Sampayo E, Dove S, LaJeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519PubMedCrossRefGoogle Scholar
  61. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90CrossRefGoogle Scholar
  62. Shinn E, Smith G, Prospero J, Betzer P (2000) African dust and the demise of Caribbean Coral Reefs. Geophys Res Lett 27:3029–3032CrossRefGoogle Scholar
  63. Stanley GD Jr (2006) Photosymbiosis and the evolution of modern coral reefs. Science 312:857–858PubMedCrossRefGoogle Scholar
  64. Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts - Symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43CrossRefGoogle Scholar
  65. Swofford D (2000) PAUP*, Phylogenetic analysis using parsimony (*and other methods). Sinauer, SunderlandGoogle Scholar
  66. Thornhill DJ, Fitt WK, Schmidt GW (2006a) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25:515–519CrossRefGoogle Scholar
  67. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006b) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722CrossRefGoogle Scholar
  68. Trench R (1993) Microalgal-invertebrate symbioses-a review. Endocytob Cell Res 9:135–175Google Scholar
  69. Veron JEN, Stafford-Smith M (2000) Corals of the world. 1:490. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  70. Veron JEN, Stafford-Smith M (2002) Coral ID (CD-Rom, first release). Australian Institute of Marine Science, TownsvilleGoogle Scholar
  71. Wallenstein FFMM, Neto AI, Álvaro NV, Tittley I (2008) Subtidal rocky shore communities of the Azores: developing a biotope survey method. J Coast Res 24:244–249CrossRefGoogle Scholar
  72. 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 52:1887–1897CrossRefGoogle Scholar
  73. Wilke B, Duke B, Jimoh W (1984) Mineralogy and chemistry of Harmattan dust in northern Nigeria. Catena 11:91–96CrossRefGoogle Scholar
  74. Zazo C, Goy J, Dabrio CJ, Soler V, Hillaire-Marcel C, Ghaleb B, González-Delgado JA, Bardají T, Cabero A (2007) Quaternary marine terraces on Sal Island (Cape Verde archipelago). Quat Sci Rev 26:876–893CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • João G. Monteiro
    • 1
    • 3
    Email author
  • Cristiane F. Costa
    • 4
  • Krystyna Gorlach-Lira
    • 5
  • William K. Fitt
    • 6
  • Sergio S. Stefanni
    • 2
  • Roberto Sassi
    • 4
  • Ricardo S. Santos
    • 2
    • 3
  • Todd C. LaJeunesse
    • 7
  1. 1.Centre of IMAR of the University of the Azores and LARSyS Associated LaboratoryHortaPortugal
  2. 2.Centre of IMAR of the University of the Azores and LARSyS Associated LaboratoryHortaPortugal
  3. 3.Departament of Oceanography and Fisheries of the University of the AzoresHortaPortugal
  4. 4.Universidade Federal da Paraíba. Departamento de Sistemática e Ecologia, Laboratório de Ambientes Recifais e Biotecnologia com Microalgas (UFPB/DSE/LARBIM)ParaíbaBrazil
  5. 5.Universidade Federal da Paraíba, Departamento de Biologia Molecular, Laboratório de Biologia Molecular e Ecologia (UFPB/DBM/LABIME)ParaíbaBrazil
  6. 6.Odum School of EcologyUniversity of GeorgiaAthensUSA
  7. 7.Depatment of Biology, Mueller LaboratoryPennsylvania State UniversityUniversity ParkUSA

Personalised recommendations