Advertisement

General Ecological Aspects of Anthozoan-Symbiodinium Interactions in the Mediterranean Sea

  • Pilar Casado-AmezúaEmail author
  • Alejandro Terrón-Sigler
  • Jorge H. Pinzón
  • Paola Furla
  • Didier Forcioli
  • Denis Allemand
  • Marta Ribes
  • Rafel Coma
Chapter

Abstract

The aim of this chapter is to provide a general overview of the main ecological aspects of Anthozoan-Symbiodinium mutualisms in the Mediterranean Sea. There are reports of at least twelve species of symbiotic anthozans in the basin. These anthozoans establish symbiotic relations with Symbiodinium Temperate A and B2 (Symbiodinium psygmophilum), corresponding to the only two species of Symbiodinium described in the region. A synthesis of the trophic and biochemical aspects of the interaction between Symbiodinum and their cnidarian hosts is given to contribute to the understanding of the mechanisms that maintain this special association. Finally, current knowledge about the ecological importance of this interaction in engineering species is examined. This review is framed to highlight the ecological importance of this symbiotic relationship in ecosystem construction and maintenance on an enclosed, temperate marine basin.

Keywords

Symbiodinium sp. Anthozoans Mutualism Engineer species Mediterranean Sea 

Notes

Acknowledgements

We would like to thank H. Zibrowius, TC. LaJeunesse, and MA. Coffroth for their suggestions during the initial development of ideas for this manuscript. P. Peñalver, D. León-Muez and A. Ibáñez helped in the field with the pictures. E. Lynne did help us to improve the English grammar and edition. Financial support to R. Coma and M. Ribes was provided by the Spanish Government under the CSI-Coral grant (CGL2013-43106-R).

References

  1. Ainsworth TD, Fine M, Roff G, Hoegh-Guldberg O (2008) Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica. ISME J 2:67–79CrossRefPubMedGoogle Scholar
  2. Antoniadou C, Chintiroglou C (2010) Biodiversity of zoobenthos associated with a Cladocora caespitosa bank in the north Aegean Sea. Rapp Commun Int Mer Méditerr 39:432Google Scholar
  3. Armorza-Zvuloni R, Segal R, Kramarsky-Winter E, Loya Y (2011) Repeated bleaching events may result in high tolerance and notable gametogenesis in stony corals: Oculina patagonica as a model. Mar Ecol Prog Ser 426:149–159CrossRefGoogle Scholar
  4. Baird A, Maynard JA (2008) Coral adaptation in the face of climate change. Science 320:15–316CrossRefGoogle Scholar
  5. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689CrossRefGoogle Scholar
  6. Baker AC, Rowan R (1997) Diversity of symbiotic dinoflagellates (zooxanthellae) in scleractinian corals of the Caribbean and eastern Pacific. In: Lessios HA, Macintyre IG (eds) Proceedings of the 8th international coral reef symposium, PanamaGoogle Scholar
  7. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol 44:123–195Google Scholar
  8. Barbrook AC, Visram S, Douglas AE, Christopher JH (2006) Molecular diversity of dinoflagellate symbionts of Cnidaria: the psbA minicircle of Symbiodinium. Protist 157:159–171CrossRefPubMedGoogle Scholar
  9. Blanc PL (2002) The opening of the Plio-Quaternary Gibraltar Strait: assessing the size of a cataclysm. Geodin Acta 15:303–317CrossRefGoogle Scholar
  10. Boudouresque CF (2004) Marine biodiversity in the Mediterranean: status of species, populations and communities. Sci Rep Port-Cros Nat Park Fr 20:97–146Google Scholar
  11. Calvo E, Simo R, Coma R, Ribes M, Pascual J, Sabates A, Gili JM, Pelejero C (2011) Effects of climate change on Mediterranean marine ecosystems: the case of the Catalan Sea. Climate Res 50:1–29CrossRefGoogle Scholar
  12. Carvalho S, Cúrdia J, Pereira F, Guerra-García JM, Santos MN, Cunha M (2014) Biodiversity patterns of epifaunal assemblages associated with the gorgonians Eunicella gazella and Leptogorgia lusitanica in response to host, space and time. J Sea Res 85:37–47CrossRefGoogle Scholar
  13. Casado-Amezúa P, Machordom A, Bernardo J, González-Wangüemert M (2014) New insights into the genetic diversity of Mediterranean zooxanthellae. Symbiosis 63:41–46CrossRefGoogle Scholar
  14. Cocito S, Ferrier-Pagès C, Cupido R, Rottier C, Meier-Augenstein W, Kemp H, Reynaud S, Peirano A (2013) Nutrient acquisition in four Mediterranean gorgonian species. Mar Ecol Prog Ser 473:179–188CrossRefGoogle Scholar
  15. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34CrossRefPubMedGoogle Scholar
  16. Coll M, Piroddi C, Steenbeek J, Kaschner K et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns and threats. PLoS One 5:e11842CrossRefPubMedPubMedCentralGoogle Scholar
  17. Coma R, Ribes M (2003) Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101:205–215CrossRefGoogle Scholar
  18. Coma R, Ribes M, Serrano E, Jiménez E, Salat J, Pascual J (2009) Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proc Natl Acad Sci U S A 106:6176–6181CrossRefPubMedPubMedCentralGoogle Scholar
  19. Coma R, Serrano E, Linares C, Ribes M, Diaz D, Ballesteros E et al (2011) Sea urchins predation facilitates coral invasion in a marine reserve. PLoS One 6:e22017CrossRefPubMedPubMedCentralGoogle Scholar
  20. Coma R, Llorente-Llurba E, Serrano E, Gili JM, Ribes M (2015) Natural heterotrophic feeding by a temperate octocoral with symbiotic zooxanthellae: a contribution to understanding the mechanisms of die-off events. Coral Reefs 34:549–560CrossRefGoogle Scholar
  21. Crisci C, Bensoussan N, Romano JC, Garrabou J et al (2011) Temperature anomalies and mortality events in marine communities: insights of factors behind differential mortality impacts in the NW Mediterranean. PLoS One 6:e23814CrossRefPubMedPubMedCentralGoogle Scholar
  22. Dani V, Ganot P, Priouzeau F, Furla P, Sabourault C (2014) Are Niemann‐Pick type C proteins key players in cnidarian–dinoflagellate endosymbioses? Mol Ecol 23:4527–4540CrossRefPubMedGoogle Scholar
  23. Danovaro R, Dinet A, Duineveld G, Tselepides A (1999) Benthic response to particulate fluxes in different trophic environments: a comparison between the gulf of lions–Catalan Sea (western-Mediterranean) and the Cretan Sea (eastern-Mediterranean). Program Oceanogr 44:287–312CrossRefGoogle Scholar
  24. Davy SK, Lucas IAN, Turner JR (1996) Carbon budgets in temperate anthozoan-dinoflagellate symbioses. Mar Biol 126:773–783CrossRefGoogle Scholar
  25. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol R 76:229–261CrossRefGoogle Scholar
  26. Duclaux GN (1977) Recherches sur quelques associations symbiotiques d’algues et de métazoaires. Thèse de doctorat d’etat ès sciences naturelles, Université Pierre et Marie Curie Paris 6 (CNRS AO 12–445). 292 pGoogle Scholar
  27. Dunn SR, Schnitzler CE, Weis VM (2007) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc R Soc B Biol Sci 274:3079–3085CrossRefGoogle Scholar
  28. Ezzat L, Merle P-L, Furla P, Buttler A, Ferrier-Pagès C et al (2013) The Response of the Mediterranean Gorgonian Eunicella singularis to thermal stress is independent of its nutritional regime. PLoS One 8:e64370CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ferrier-Pagès C, Peirano A, Abbate M, Cocito S, Negri A, Rottier C, Riera P, Rodolfo-Metalpa R, Reynaud S (2011) Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa. Limnol Oceanogr 56:1429–1438CrossRefGoogle Scholar
  30. Ferrier-Pagès C, Reynaud S, Béraud E, Rottier C, Menu D, Duong G, Gévaert F (2015) Photophysiology and daily primary production of a symbiotic gorgonian. Photosynth Res 123:95–104CrossRefPubMedGoogle Scholar
  31. Fine M, Zibrowius H, Loya Y (2001) Oculinapatagonica: a non-lessepsian scleractinian coral invading the Mediterranean Sea. Mar Biol 138:1195–1203CrossRefGoogle Scholar
  32. Fit WK, Pardy RL, Littler MM (1982) Photosynthesis, respiration and contribution to community productivity of the symbiotic sea anemone Anthopleura elegantissima (Brandt, 1835). J Exp Mar Biol Ecol 61:213–232CrossRefGoogle Scholar
  33. Forcioli D, Merle PL, Caligara C, Ciosi M, Muti C, Francour P, Cerrano C, Allemand D (2011) Symbiont diversity is not involved in depth acclimation in the Mediterranean sea whip Eunicella singularis. Mar Ecol Prog Ser 439:57–71CrossRefGoogle Scholar
  34. Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a Zooxanthellae: taxonomy, life cycle, and morphology. Eukariotic Microbiol 9:45–52Google Scholar
  35. Furla P, Allemand D, Shick JM, Ferrier- Pagès C, Richier S, Plantivaux A, Merle PL, Tambutté (2005) The symbiotic anthozoan: a physiological chimera between algal and animal. Integr Comp Biol 45:595–604CrossRefPubMedGoogle Scholar
  36. Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, Cigliano M et al (2009) Mass mortality in North-western Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Change Biol 15:1090–1103CrossRefGoogle Scholar
  37. Gori A, Bramanti L, López-González P, Thoma JN, Gili JM (2012) Characterization of the zooxanthellate and azooxanthellate morphotypes of the Mediterranean gorgonian Eunicella singularis. Mar Biol 159:1485–1496CrossRefGoogle Scholar
  38. Hoogenboom M, Rodolfo-Metalpa R, Ferrier-Pagès C (2010) Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocora caespitosa. J Exp Biol 213:2399–2409CrossRefPubMedGoogle Scholar
  39. Jones RJ, Hoegh‐Guldberg O, Larkum AWD, Schreiber U (1998) Temperature‐induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230CrossRefGoogle Scholar
  40. Kersting DK, Bensoussan N, Linares C (2013) Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming. PLoS One 8:e70820CrossRefPubMedPubMedCentralGoogle Scholar
  41. Koukouras A, Kühlmann D, Voultsiadou E, Vafidis D, Dounas C, Chintiroglou C, Koutsoubas D (1998) The macrofaunal assemblage associated with the scleractinian coral Cladocora caespitosa (L.) in the Aegean Sea. Ann Inst Océanogr 74:97–114Google Scholar
  42. Kružić P, Benkovic L (2008) Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea (Croatia). Mar Ecol 29:125–139CrossRefGoogle Scholar
  43. Kružić P, Sršen P, Benković L (2012) The impact of seawater temperature on coral growth parameters of the colonial coral Cladocora caespitosa (Anthozoa, Scleractinia) in the eastern Adriatic Sea. Facies 58:477–491CrossRefGoogle Scholar
  44. 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
  45. LaJeunesse TC, Loh WKW, vanWoesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern great barrier reef corals relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054CrossRefGoogle Scholar
  46. LaJeunesse TC, Pettay T, Sampayo EM, Phongsuwan N, Brown B, Obura D, Hoegh-Guldberg O, Fitt WK (2010) Special paper: 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
  47. 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 48:1380–1391CrossRefPubMedGoogle Scholar
  48. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278CrossRefPubMedGoogle Scholar
  49. Leydet PK, Hellberg ME (2015) The invasive coral Oculina patagonica has not been recently introduced to the Mediterranean from the western Atlantic. BMC Evol Biol 15:79CrossRefPubMedPubMedCentralGoogle Scholar
  50. Loh WKW, Carter D, Hoegh-Guldberg O (1998) Diversity of zooxanthellae from scleractinian corals of One tree island (The Great Barrier Reef). In: Greenwood JG, Hall NJ (eds) Proceedings of the Australian coral reef society, BrisbaneGoogle Scholar
  51. Lough JM, van Oppen MJH (2009) Introduction: coral bleaching-patterns, processes, causes and consequences. Coral Bleaching. Ecol Stud 205:1–5CrossRefGoogle Scholar
  52. Meron D, Rodolfo-Metalpa R, Cunning R, Baker AC, Fine M, Banin E (2012) Changes in microbial communities in response to a natural pH gradient. ISME J 6:1775–1785CrossRefPubMedPubMedCentralGoogle Scholar
  53. Mitchelmore CL, Alan Verde E, Ringwood AH, Weis VM (2003) Differential accumulation of heavy metals in the sea anemone Anthopleura elegantissima as a function of symbiotic state. Aquat Toxicol 64:317–329CrossRefPubMedGoogle Scholar
  54. Morri C, Peirano A, Bianchi CN (2001) Is the Mediterranean coral Cladocora caespitosa an indicator of climatic change? Archo Oceanogr Limnol 22:139–144Google Scholar
  55. Muscatine L, Goiran C, Land L, Jaubert J, Cuif JP, Allemand D (2005) Stable isotopoes (δ13C and δ15N) of organic matrix from coral skeleton. Proc Natl Acad Sci U S A 102:1525–1530CrossRefPubMedPubMedCentralGoogle Scholar
  56. Mydlarz LD, Jones LE, Harvell C (2006) Innate immunity, environmental drivers and disease ecology of marine and freshwater invertebrates. Annu Rev Ecol Evol Syst 37:251–288CrossRefGoogle Scholar
  57. Peirano A, Morri C, Bianchi CN, Rodolfo-Metalpa R (2001) Biomass, carbonate standing stock and production of the Mediterranean coral Cladocora caespitosa (L.). Facies 44:75–80CrossRefGoogle Scholar
  58. Perez T, Garrabou J, Sartoretto S, Harmelin JG, Francour P, Vacelet J (2000) Mortalité massive d’invertébrés marins: un événement sans précédenten Méditerranéenord-occidentale. Rend Acad Sci 323:853–865CrossRefGoogle Scholar
  59. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergences timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30CrossRefPubMedGoogle Scholar
  60. Pochon X, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis and evolution. PeerJ 2:e394CrossRefPubMedPubMedCentralGoogle Scholar
  61. Richier S, Merle PL, Furla P, Pigozzi D, Sola F, Allemand D (2003) Characterization of superoxide dismutases in anoxia-and hyperoxia-tolerant symbiotic cnidarians. BBA-Gen Subjects 1621:84–91CrossRefGoogle Scholar
  62. Rodolfo-Metalpa R, Bianchi CN, Peirano A, Morri C (2005) Tissue necrosis and mortality of the temperate coral Cladocora caespitosa. Ital J Zoo 72:271–276CrossRefGoogle Scholar
  63. Rodolfo-Metalpa R, Richard C, Allemand D, Bianchi CN, Morri C, Ferrier-Pagès C (2006) Response of zooxanthellae in symbiosis with the Mediterranean corals Cladocora caespitosa and Oculina patagonica to elevated temperatures. Mar Biol 150:45–55CrossRefGoogle Scholar
  64. Rodriguez-Lanetty M (2003) Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rDNA. Mol Phylogenet Evol 28:152–168CrossRefPubMedGoogle Scholar
  65. Rodriguez-Lanetty M, Loh W, Carter D, Hoegh-Guldberg O (2011) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Mar Biol 138:1175–1181Google Scholar
  66. Roth MS (2014) The engine of the reef: photobiology of the coral-algal symbiosis. Adv Microbiol 5:422Google Scholar
  67. Rubio-Portillo, Vázquez-Luis M, Izquierdo Muñoz A, Ramos Esplá AA (2014) Distribution paterns of alien coral Oculina patagonica De Angelis D’Ossat, 1908 in Western Mediterranean Sea. J Sea Res 85:372–378CrossRefGoogle Scholar
  68. Salomidi M, Katsanevakis S, Issaris Y, Tsiamis K, Katsiaras N (2013) Anthropogenic disturbances of coastal habitats promotes the spread of the introduced scleractinian coral Oculina patagonica in the Mediterranean Sea. Biol Invasions 15:1961–1971CrossRefGoogle Scholar
  69. Sampayo AM, Dove S, LaJeunesse (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519CrossRefPubMedGoogle Scholar
  70. Sartoretto S, Harmelin JG, Bachet F, Bejaoui N, Lebrun O et al (2008) The alien coral Oculina patagonica De Angelis, 1908 (Cnidaria, Scleractinia) in Algeria and Tunisia. Aquat Invasions 3:173–180CrossRefGoogle Scholar
  71. Savage AM, Goodson MS, Visram S, Trapido-Roshental H, Wiedenmann J, Douglas AE (2002) Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and sea anemones. Mar Ecol Prog Ser 244:17–26CrossRefGoogle Scholar
  72. Serrano E, Coma R, Marta R (2013) Pattern of Oculina patagonica occurrence along the Iberian Peninsula Coastline: a first step to understand the factors affecting its invasion dynamics. Rapp Commint Mer Médit 40Google Scholar
  73. Schiller C (1993) Ecology of the symbiotic coral Cladocora caespitosa (L.) (Faviidae, Scleractinia) in the Bay of Piran (Adriatic Sea): I. Distribution and Biometry. Mar Ecol 14:205–219CrossRefGoogle Scholar
  74. Serrano E, Coma R (2012) A phase shift from macroalgal to coral dominance in the Mediterranean. Coral Reefs 31:1199CrossRefGoogle Scholar
  75. Suggett DJ, Hall-Spencer JM, Rodolfo-Metalpa R, Boatman TG, Paytin R, Tye Pettay D, Johnson VR, Warner ME, Lawson T (2012) Sea anemones may thrive in a high CO2 world. Global Chang Biol 18:3015–3025CrossRefGoogle Scholar
  76. Templado J (2014) Future trends of Mediterranean biodiversity. In: Goffredo S, Dubinsky Z (eds) The Mediterranean Sea. Its history and present challenges. Springer, Dordrecht, pp 479–498Google Scholar
  77. Thornhill DJ, Yiang X, Pettay DT, Zhong SSR (2013) Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol 2:4499–4515CrossRefGoogle Scholar
  78. Tremblay P, Peirano A, Ferrier-Pagès C (2011) Heterotrophy in the Mediterranean symbiotic coral Cladocora caespitosa: comparison with two other scleractinian species. Mar Ecol Prog Ser 422:165–177CrossRefGoogle Scholar
  79. Turley CM (1999) The changing Mediterranean Sea – a sensitive ecosystem? Prog Oceanogr 44:387–400CrossRefGoogle Scholar
  80. Visram S, Wiedenmann J, Douglas AE (2006) Molecular diversity of symbiotic algae of the genus Symbiodinium (Zooxanthellae) in cnidarians of the Mediterranean Sea. J Mar Biol Assoc UK 86:1281–1283CrossRefGoogle Scholar
  81. Wang J, Douglas AE (1998) Nitrogen recycling or nitrogen conservation in an alga-invertebrate symbiosis? J Exp Biol 201:2445–2453PubMedGoogle Scholar
  82. Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694CrossRefPubMedGoogle Scholar
  83. Zabala M, Ballesteros E (1989) Surface-dependent strategies and energy flux in benthic marine communities or, why corals do not exist in the Mediterranean. Sci Mar 53:3–17Google Scholar
  84. Zibrowius H, Ramos A (1983) Oculina patagonica. Scléractiniarie exotique en Méditerraenée-nouvelles observations dans le Sud-Est de l’Espagne. CIESM 28:297–301Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Pilar Casado-Amezúa
    • 1
    • 2
    Email author
  • Alejandro Terrón-Sigler
    • 1
  • Jorge H. Pinzón
    • 3
  • Paola Furla
    • 4
  • Didier Forcioli
    • 4
  • Denis Allemand
    • 5
  • Marta Ribes
    • 6
  • Rafel Coma
    • 7
  1. 1.Hombre y Territorio AssociationSevillaSpain
  2. 2.EU-US Marine Biodiversity Research GroupFranklin Institute, University of AlcaláMadridSpain
  3. 3.Department of BiologyUniversity of Texas ArlingtonTXUSA
  4. 4.UMR 1112 INRA-UNSAUniversity of Nice-Sophia AntipolisNice Cedex 2France
  5. 5.Centre Scientifique de MonacoMonacoMonaco
  6. 6.Institute of Marine Sciences-Spanish National Research Council (ICM-CSIC)BarcelonaSpain
  7. 7.Center for Advanced Studies of Blanes-Spanish National Research Council (CEAB-CSIC)BlanesSpain

Personalised recommendations