Holobiont assemblages of dominant coral species (Symbiodinium types and coral species) shape Caribbean reef community structure
PDF

How to Cite

Grajales, A., & Sanchez, J. A. (2016). Holobiont assemblages of dominant coral species (Symbiodinium types and coral species) shape Caribbean reef community structure. Revista De La Academia Colombiana De Ciencias Exactas, Físicas Y Naturales, 40(155), 300–311. https://doi.org/10.18257/raccefyn.294

Downloads

Download data is not yet available.

Métricas Alternativas


Dimensions

Abstract

Research on coral reef community structure suggests that fine spatial-temporal stochasticity drives biodiversity patterns in this tropical marine ecosystem. The combination of a coral colony and its zooxanthella, or holobiont, should therefore be used as the community indivisible units to better understand this structure. Research in zooxanthellae (Symbiodinium) diversity has allowed the identification of specific or generalist host associations. The distribution of specific symbionts depends on both the host identity and the environmental conditions. This study determined the identity on these symbionts within hard corals communities (Scleractinia and Milleporina) at 27 sites on the upper slope habitat (mixed zone) in Cartagena, Colombia (Southwestern Caribbean Sea). Zooxanthellae identification was made with RFLPs analysis (18S, SSU, rDNA), DGGE, and DNA sequencing (ITS2, rDNA). Different combinations of coral species and their specific Symbiodinium types (holobionts) were determined as different ecological units. Taking each holobiont as a variable, a cluster community structure analysis was made and compared to the pattern obtained from using coral species alone. Different site groupings occurred for holobionts and species, where higher similarities were found using holobionts. O. annularis and O. faveolata, two dominant coral species, formed independently different Symbiodinium associations, depending on depth. Their symbiont preference can be under higher selection pressure than previously thought, if they act as different ecological units. © 2016. Acad. Colomb. Cienc. Ex. Fis. Nat. All rights reserved.

https://doi.org/10.18257/raccefyn.294
PDF

References

Ainsworth, T. D., Thurber, R. V., & Gates, R. D. 2010. The future of coral reefs: a microbial perspective. Trends in Ecology & Evolution, 25 (4): 233-240.

Baker AC. 2003. Flexibility and specificity in coral–algal symbiosis:diversity, ecology and biogeography of Symbiodinium. Annual Reviews of Ecology and Systematics. 34:661-689.

Baker AC, Rowan R. 1997. Diversity of symbiotic dinoflagellates (zooxanthellae) in scleractinian corals of the Caribbean and Eastern Pacific. Proceedings of the Eighth International Coral Reef Symposium. 2:1301-1306.

Blackall LL, Wilson B, & van Oppen MJ. 2015. Coral–The World’s Most Diverse Symbiotic Ecosystem. Molecular Ecology (in press).

Cáceres SM, & Sánchez JA. 2015. Growth strategies of an abundant reef-building coral in the southern Caribbean (Undaria tenuifolia). Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales. 39 (152): 348-357.

Camargo C, Maldonado J, Alvarado E, Moreno-Sánchez R, Mendoza S, Manrique N, Mogollón, A, Osorio J, Grajales A, Sánchez JA. 2009. Community involvement in management for maintaining coral reef resilience and biodiversity in southern Caribbean marine protected areas. Biodiversity & Conservation. 18: 935-956.

Clarke KR, Warwick RM. 2001. Change in marine communities: an approach to statistical analysis and interpretation. 2nd edition. PRIMER-E: Plymouth.

Coffroth MA, Lasker, HR, Diamond ME, Bruenn, JA, Bermingham E. 1992. DNA fingerprints of a gorgonian coral: A method for detecting clonal structure in a vegetative species. Marine Biology. 114: 317-325.

Coleman AW, Suarez A, Goff LJ. 1994. Molecular delineation of species and syngens in volvocacean green algae (Chlorophyta). Journal of Phycology. 30: 80-90.

Connolly SR, Hughes TP, Bellwood DR, Karlson RH. 2005 Community Structure of Corals and Reef Fishes at Multiple Scales. Science. 2005; 309 (5739):1363-5. doi: 10.1126/science.1113281 PMID: 16123298

Díaz-Pulido G, Sánchez JA, Zea SE, Garzón Ferreira J. 2004. Esquemas de distribución espacial en la comunidad bentónica de arrecifes coralinos continentales y oceánicos del Caribe colombiano. Revista de la Academia de Ciencias-Colombia. 108: 337-347.

Dornelas M, Connolly SR, Hughes TP. 2006. Coral reef diversity refutes the neutral theory of Biodiversity. Nature. 440: 80-82.

Fabricius KE, De’ath G. 2008. Photosynthtic symbionts and energy supply determine octocoral biodiversity in coral reefs. Ecology. 89 (11): 3163-73. ISI:000261053500020.

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. Microbial Ecology. 60 (1): 250-263.

Felsestein J. 1985. Confidence limits on phylogenies:an approach using the bootstrap. Evolution. 39:783-791.

Goreau TF. 1959. The ecology of Jamaican coral reefs:1. Species composition and zonation. Ecology. 40:67-90.

Goulet TL. 2006. Most coral may not change their symbionts. Marine Ecology Progress Series. 321: 1-7. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Ser. 41:95-98.

Hubbell SP. 2001. The unified neutral theory of biodiversity and biogeography, Princeton University Press.

Huelsenbeck JP, Ronquist F. 2001. MrBAYES: Bayesian inference of phylogeny. Bioinformatics. 17: 754-755

Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes- Bonilla H, home PE. 2004. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proceedings of the Royal Society London B. 271:1757-1763.

Iglesias-Prieto R, Matta JL, Robins WA & Trench RK. 1992. Photosynthetic response to elevated temperature in the symbiotic dinoflagelate Symbiodinium microadriaticum in culture. Proceedings of the National Academy of Science. USA 89: 10302-10305.

Kaandorp JA.1986. Rocky substrate communities of the infralitoral fringe of the Bulonnais coast, NW France. A quantitative survey using cluster analysis. Marine Biology. 92:255- 265.

Kimes NE, Van Nostrand JD, Weil E, Zhou J, & Morris PJ. 2010. Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. Environmental microbiology. 12 (2): 541-556.

LaJeunesse TC. 2005 Species radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Molecular Biology and Evolution. 22: 570-581.

LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK. 2003. Low symbiont diversity in southern Great Barrier Reef corals relative to those of the Caribbean.

Limnology and Oceanography. 48: 2046-2054. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK. 2003 Low symbiont diversity in southern Great Barrier Reef corals relative to those of the Caribbean. Limnology and Oceanography. 48, Table supplement.

LaJeunesse TC. 2002 Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology. 141: 387-400.

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. Journal of Phycology. 37: 866-80.

LaJeunesse TC, Trench RK. 2000 The biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone, Anthopleura elegantissima (Brandt). Biological Bulletin. 199:126-134

Leggat W, Ainsworth T, Bythell J, Dove S, Gates, R, Hoegh-Guldberg O, Iglesias-Prieto R, and Yellowlees D. 2007. The hologenome theory disregards the coral holobiont. Nature Reviews Microbiology. 5 (10).

Little AF Van Oppen JH, Willis BL. 2004 Flexibility in Algal Endosymbioses Shapes Growth in Reef Corals Science. 304: 1492-1494.

Littman RA, van Oppen MJ, Willis BL. 2008. Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). Journal of Experimental Marine Biology and Ecology. 2008 Sep 12; 364 (1): 48-53.

Littman RA, Bourne DG, & Willis BL. 2010. Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host. Molecular Ecology. 19 (9): 1978-1990.

López-Angarita J, Moreno-Sánchez R, Maldonado J, JA Sánchez. 2013. Evaluating linked social-ecological systems in Marine Protected Areas. Conservation Letters. 7: 241-252. DOI:10.1111/conl.12063

Marrugan AE, Henderson PA. 2003 Exploring the excess of rare species in natural species abundance distributions. Nature 422: 714-716.

McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, & Warner ME. 2012. Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Marine Ecology Progress Series. 462: 1-7.

McKenna Jr JE. 2003. An enhanced cluster analysis program with bootstrap significance testing for ecological community analysis. Environmental Modelling & Software. 18:205-220.

McNally KL, Govind NS, Thome PE, Trench RK. 1994 Small subunit ribosomal DNA sequence analyses and a reconstruction of the inferred phylogeny among symbiotic dinoflagellates (Pyrrophyta). Journal of Phycology. 30:316-329.

Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJ. 2009 The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS One. 4 (7): e6364.

Muscatine L. 1990. The role of symbiotic algae in carbon and energy flux in reef corals. Coral Reefs. 25: 1-29.

Muscatine L, Porter JW. 1977. Reef corals:mutualistic symbioses adapted to nutrient-poor environments. Bioscience. 27:454-460.

Pinzón JH., Weil E. 2011. Cryptic species within the Atlantic-Caribbean genus Meandrina (Scleractinia): a multidisciplinary approach and description of the new species Meandrina jacksoni. Bulletin of Marine Science. 87 (4): 823-853.

Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J. 2006. Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Molecular phylogenetics and Evolution. 38(1): 20-30.

Porto I, Granados C, Restrepo JC, Sánchez JA. 2008. Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean Reefs. PLoS ONE. 3:e2160.

Posada D, Crandall KA. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics. 14 (9): 817-818.

Putnam HM, Stat M, Pochon X, & Gates RD. 2012. Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proceedings of the Royal Society of London B: Biological Sciences, rspb20121454.

Restrepo JD, Zapata P, Díaz JM., Garzón-Ferreira J, García CB. 2006 Fluvial fluxes into the Caribbean Sea and their impact on coastal ecosystems: The Magdalena River, Colombia. Global and Planetary Change. 50: 33-49.

Rowan R, Knowlton N, Baker AC, Jara J. 1997. Landscape ecology of algal symbiont communities explains variation in episodes of coral bleaching. Nature. 388: 265-269.

Rowan R, Knowlton N. 1995. Intraspecific Diversity and Ecological Zonation in Coral-Algal Symbiosis. Proceedings of the National Academy of Science USA. 92: 2850-2853.

Rowan R & Powers DA.1991. A molecular genetic identification of zooxanthellae and the evolution of animal-algal symbioses. Science. 251: 1348-1351.

Sánchez JA, Pizarro V, Acosta AR, Castillo P, Herron P, Marines JC, Martines P, Orozco C. 2005. Evaluation coral ref. Benthic communities in remote Caribbean atolls (Quitasueño, Serana and Roncador banks) to recommend marine-protected areas for the seaflower biosphere reserve. Atoll Research Bulletin. 531: 1-65.

Sánchez JA, Zea S & Díaz JM. 1997. Gorgonian communities of two contrasting environments from oceanic Caribbean atolls. Bulletin of Marine Science. 61 (2): 61-72.

Santos SR, Kinzie III RA, Sakai CK & Coffroth MA. 2003. Molecular Characterization of Nuclear Small Subunit (18S)-rDNA pseudogenes in a symbiotic dinoflagellate (Symbiodinium, Dinophyta). Journal of Eukaryote Microbiology. 50: 417-421.

Silverstein RN, Correa AM, Baker AC. 2012. Specificity is rarely absolute in coral–algal symbiosis: implications for coral response to climate change. Proceedings of the Royal Society of London B: Biological Sciences. 279 (1738):2609-2618.

Swofford, DL. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW. 2006. Multi-year, seasonal genotypic surveys of coralalgal symbioses reveal prevalent stability or post-bleaching reversion. Marine Biology. 148:711-722.

Toller WW, Rowan R, Knowlton N. 2001a Zooxanthellae of the Montastrea annularis species complex: patterns of distribution of four taxa of Symbiodinium across different reefs and across depths. Biological Bulletin. 201: 348-359.

Toller WW, Rowan R, Knowlton N. 2001b. Repopulation of zooxanthellae in Caribbean corals Montastrea annularis and Montastrea faveolata following experimental and disease induced bleaching. Biological Bulletin. 201: 360-373.

Velásquez J, López-Angarita J, JA Sánchez. 2011. Benthic foraminifera as indicators of ecosystem resilience in protected and non-protected coral reefs of the Southern Caribbean. Biodiversity & Conservation. 20: 3591-3603. doi: 10.1007/s10531-011-0152-7

Velásquez J, Sánchez, JA. 2015. Octocoral Species Assembly and Coexistence in Caribbean Coral Reefs. PloS ONE. 10:e0129609

Vernette G, Mauffret A, Bobier C, Briceno L, Gayet J. 1992. Mud diapirism, fan sedimentation and strike-slip faulting, Caribbean Colombian margin. Tectonophysics. 202: 335-349.

Warner ME, LaJeunesse TC, Robinson JD, Thur R.M. 2006. The ecological distribution and comparative photobiology of symbiotic dinoflagellate from reef corals in Belize: Potential implications for coral bleaching. Limnology and Oceanography 51 (4): 1887-1897.

Weiss, VM, Reynolds WS, Deboer MD, Krupp DA. 2001. Hostsymbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral reefs. 20 (3):301-308.

Zea S. 2001. Patterns of sponge (Porifera, Demospongiae) distribution in remote, oceanic reef complexes of the southwestern Caribbean. Rev. Acad. Colomb. Cienc. 25 (97): 579-592.

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Copyright (c) 2016 Journal of the Colombian Academy of Exact, Physical and Natural Sciences