Abstract
Scleractinian corals may acquire Symbiodinium from their parents (vertically) or from the environment (horizontally). In the present study, adult colonies of the coral Acropora longicyathus from One Tree Island (OTI) on the southern Great Barrier Reef (Australia) acquired two distinct varieties of symbiotic dinoflagellates (Symbiodinium) from the environment. Adult colonies had either Symbiodinium from clade C (86.7%) or clade A (5.3%), or a mixture of both clades A and C (8.0% of all colonies). In contrast, all 10-day-old juveniles were associated with Symbiodinium from clade A, while 83-day-old colonies contained clades A, C and D even though they were growing at the same location. Symbiodinium from clade A were dominant in both 10- and 83-day-old juveniles (99 and 97% of all recruits, respectively), while clade D was also found in 31% of 83-day-old juveniles. Experimental manipulation also revealed that parental association (with clade A or C), or the location within the OTI reef, did not influence which clade of symbiont was acquired by juvenile corals. The differences between the genetic identity of populations of Symbiodinium resident in juveniles and adult A. longicyathus suggest that ontogenetic changes in the symbiosis may occur during the development of scleractinian corals. Whether or not these changes are due to host selective processes or differences in the physical environment associated with juvenile versus adult colonies remains to be determined.
References
Babcock R, Bull G, Harrison P, Heyward A, Oliver J, Wallace C, Willis B (1986) Syncronous spawning of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394
Baker A (2002) Is coral bleaching really adaptive? Reply. Nature 415:602
Baker A (2003) Flexibility and specificity in coral–algal symbiosis: Diversity, ecology and biogeography of Symbiodinium. Annual Review of Ecology, Evolution and Systematics 34:661–689
Baker A, Romanski A (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: comment on Goulet (2006). Mar Ecol Prog Ser 335:237–242
Banaszak A, LaJeunesse T, Trench R (2000) The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. J Exp Mar Biol Ecol 249:219–233
Banaszak A, Barba Santos M, LaJeunesse T, Lesser M (2006) The distribution of mycosporine-like amino acids (MAAs) and the phylogenetic identity of symbiotic dinoflagellates in cnidarian hosts from the Mexican Caribbean. J Exp Mar Biol Ecol 337:131–146
Booth DJ, Beretta GA (2002) Changes in a fish assemblage after a coral bleaching event. Mar Ecol Prog Ser 245:205–212
Chen C, Wei N, Tsai W, Fang L (2005) Symbiont diversity in the scleractinian corals from tropical reefs and non-reefal communities in Taiwan. Coral Reefs 24:11–22
Coffroth M, Santos R, Goulet T (2001) Early ontogenetic expression of specificity in a cnidarian–algal symbiosis. Mar Ecol Prog Ser 222:85–96
Dennis C (2002) Reef under threat from ‘bleaching’ outbreak. Nature 415:947
Drollet JH, Faucon M, Maritorena S, Martin PMV (1994) A survey of environmental physicochemical parameters during a minor coral mass bleaching event in Tahiti in 1993. Mar Freshw Res 45:1149–1156
Enriquez S,Mendez E, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032
Fadlallah Y (1983) Sexual reproduction, development and larval biology in scleractinian corals. Coral Reefs 2:129–150
Frith C (1983) Some aspects of lagoon sedimentation and circulation at One Tree Reef, Southern Great Barrier-Reef. BMR J Aust Geol Geophys 8:211–221
Goulet T, Coffroth M (2003) Stability of an octocoral–algal symbiosis over time and space. Mar Ecol Prog Ser 250:117–124
Harrison P, Ward S (2001) Elevated levels of nitrogen and phosphorus reduce fertilization success of gametes from scleractinian reef corals. Mar Biol 139:1057–1068
Helmuth B, Sebens K, Daniel T (1997) Morphological variation in coral aggregations: branch spacing and mass flux to coral tissues. J Exp Mar Biol Ecol 209:233–259
Hoegh-Guldberg O, Jones R, Ward S, Loh W (2002) Is coral bleaching really adaptive? Nature 415:601–602
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 113:163–175
Iglesias-Prieto R, Trench R (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll–protein complexes to different photon–flux densities. Mar Biol 130:23–33
Jones R (1997) Changes in zooxanthellar densities and chlorophyll concentrations in corals during and after a bleaching event. Mar Ecol Prog Ser 158:51–59
Jones R, Ward S, Amri A, Hoegh-Guldberg O (2000) Changes in quantum efficiency of photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event. Mar Freshw Res 51:63–71
LaJeunesse T (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
LaJeunesse T (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400
LaJeunesse T, Loh W, van Woesik R, Hoegh-Guldberg O, Schmidt G, Fitt W (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054
Lewis C, Coffroth M (2004) The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304:1490–1492
Little A, van Oppen M, Willis B (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1942–1944
Loh W, 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 75th Anniversary Conference, Heron Island October 1997. School of Marine Science. The University of Queensland, Brisbane, pp 141–150
Loh W, Loi T, Carter D, Hoegh-Guldberg O (2001) Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species, Seriatopora hystrix and Acropora longicyathus, in the Indo-West Pacific. Mar Ecol Prog Ser 222:97–107
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131
Meesters E, Hilterman M, Kardinaal E, Keetman M, de Vries M, Bak R (2001) Colony size–frequency distributions of scleractinian coral populations: spatial and interspecific variation. Mar Ecol Prog Ser 209:43–54
Mieog J, van Oppen M, Cantin N, Stam W, Olsen J (2007) Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26:449–457
Muscatine L (1989) Adventures in symbiosis. Am Zool 29:1203–1208
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27:454–460
Muscatine L, Goiran C, Land L, Jaubert J, Cuif J, Allemand D (2005) Stable isotopes (Delta C-13 and Delta N-15) of organic matrix from coral skeleton. Proc Natl Acad Sci USA 102:1525–1530
Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27
Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34:407–417
Rowan R, Powers DA (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73
Salih A, Larkum A, Cox G, Kuhl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853
Santos S, Taylor D, Coffroth M (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: implications for extrapolating to the intact symbiosis. J Phycol 37:900–912
Sokal R, Rohlf F (1995) Biometry. W. H. Freeman and Company, New York
Stanley G (2003) The evolution of modern corals and their early history. Earth Sci Rev 60:195–225
Stanley G, Swart P (1995) Evolution of the coral–zooxanthellae symbiosis during the Triassic: a geochemical approach. Paleobiology 21:179–199
Toller W, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull 201:360–373
Ulstrup K, van Oppen M (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12:3477–3484
van Oppen M, Palstra F, Piquet A, Miller D (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host–symbiont selectivity. Proc R Soc Lond B 268:1759–1767
van Oppen M, Mahiny A, Done T (2005) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24:482–487
Veron J (2000) Corals of the world. Australian Institute of Marine Science, Townsville
Wallace C (1985) Reproduction, recruitment and fragmentation in 9 sympatric species of the coral genus Acropora. Mar Biol 88:217–233
Ward S (1997) The effect of elevated nitrogen and phosphorus on the reproduction of three species of acroporid reef corals. Ph.D. thesis, Southern Cross University, p 235
Weis V, Reynolds W, deBoer M, Krupp D (2001) Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of scleractinian coral Fungia scutaria. Coral Reefs 20:301–308
Zardoya R, Costas E, Lopez-Rodas V, Garrido-Pertierra A, Bautista JM (1995) Revised dinoflagellate phylogeny inferred from molecular analysis of large-subunit ribosomal RNA gene sequences. J Mol Evol 41:637–645
Acknowledgments
The authors would like to thank Maruricio Rodriguez-Lanetty for comments on early versions of the manuscript. Our thanks also extend to two anonymous reviewers whose comments greatly improved the quality of the final manuscript. We are grateful to the staff at One Tree Island Research Station, special thanks to Pam and Konrad Beinsen and Ali Marshall and Matt Smith, for their support in the field. This work was funded by the Australian Research Council Centre for Excellence in Coral Reef Studies (http://www.coralcoe.org.au) as well as the Coral Reef Targeted Research Project (http://www.gefcoral.org) to Ove Hoegh-Guldberg and by a Terry Walker Student Research Fellowship to Maria Gomez Cabrera from the Australian Coral Reef Society.
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del C. Gómez-Cabrera, M., Ortiz, J.C., Loh, W.K.W. et al. Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus . Coral Reefs 27, 219–226 (2008). https://doi.org/10.1007/s00338-007-0315-x
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DOI: https://doi.org/10.1007/s00338-007-0315-x