Abstract
The mutualistic relationship between corals and their dinoflagellate endosymbionts is a key factor in the evolutionary success of hermatypic (reef building) corals. The endosymbiotic algae benefit corals in numerous ways that have contributed to the long term persistence of coral reefs over geologic time. In this chapter we review ecological and physiological aspects of the interactions between corals and their symbiotic algae in light of recent advances in our knowledge of the diversity of these symbionts. While the role of symbiont diversity in promoting coral survival during environmental bleaching events has been a major focus of recent research, its importance in other physiological and ecological contexts such as inorganic nutrient dynamics and photosynthetic carbon fluxes has received much less attention. We suggest that cost-benefit analysis is a useful approach to examine these symbioses in the context of environmental change and human impacts upon corals and coral reefs. Weighing the costs versus the benefits of the symbiotic association under specific environmental perturbations has potential for use as an indicator of the health of not only corals but indeed the whole coral reef ecosystem. Drastic changes in the stability of the symbiosis, evidenced by changes in the ratio of zooxanthellae to animal biomass in corals, may turn out to be a useful diagnostic indicator of stresses to coral reefs. By using new tools developed to assess the stability of the symbiosis, we may be better able to understand and predict the effects of future stressors and perturbations that threaten these beautiful reef ecosystems.
We dedicate this chapter to our late mentor and friend, Len Muscatine, who was a leading figure in research on algal-invertebrate symbiosis, and who played a major role in our professional development .
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Adey WH (1983) The microcosm: a new tool for reef research. Coral Reefs 1:193–201
Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426
Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Ann Rev Ecol Evol Syst 34:661–689
Baker AC (2004) Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, Berlin, pp 177–194
Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 430:741
Banaszak AT, LaJeunesse TD, Trench RK (2000) The synthesis of mycosporine-like amino acids (MAA’s) by cultured, symbiotic dinoflagellates. J Exp Mar Biol Ecol 249:219–233
Barnes DJ, Chalker BE (1990) Calcification and photosynthesis in reef-building corals and algae. In: Dubinsky Z (ed) Ecosystems of the world, 25: coral reefs. Elsevier, New York, pp 109–131
Bartley R, Bainbridge ZT, Lewis SE, Kroon FJ, Wilkinson SN, Brodie JE, Silburne DM (2014) Relating sediment impacts on coral reefs to watershed sources, processes and management: a review. Sci Total Environ 468–469:1138–1153
Borneman EH (2001) Aquarium corals: selection, husbandry, and natural history. Microcosm Ltd., Charlotte
Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326
Buddemeier RW, Baker AC, Fautin DG et al (2004a) The adaptive hypothesis of bleaching. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 427–444
Buddemeier RW, Kleypas JA, Aronson RB (2004b) Coral reefs & global climate change: potential contributions of climate change to stresses on coral reef ecosystems. Pew Center on Global Climate Change, Arlington
Chen CA, Wang J-T, Fang L-S, Yang Y-W (2005) Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Mar Ecol Prog Ser 295:113–121
Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenetic expression of specificity in a Cnidarian-algal symbiosis. Mar Ecol Prog Ser 222:85–96
Coles SL, Brown BE (2003) Coral bleaching – capacity for acclimatization and adaptation. Adv Mar Biol 46:181–223
Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43:209–216
Cook CB, D’Elia CF (1987) Are zooxanthellae ever nutrient-limited? Symbiosis 4:199–212
Cumbo VR, Baird AH, van Oppen MJH (2013) The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32:111–120
Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:259–262
D’Elia CF, Cook CB (1988) Methylamine uptake by zooxanthellae-invertebrate symbioses: insights into host ammonium environment and nutrition. Limnol Oceanogr 33:1153–1165
D’Elia CF, Domotor SL, Webb KL (1983) Nutrient uptake kinetics of freshly isolated zooxanthellae. Mar Biol 75:157–167
Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261
Dunlap WC, Chalker BE (1986) Identification and quantitation of near-UV absorbing compounds (S-320) in a hermatypic scleractinian. Coral Reefs 5:155–159
Enríguez S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceangr 50:1025–1032
Fagoonee I, Wilson HB, Hassell MP et al (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845
Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. Bioscience 43:606–611
Fay SA, Weber MX (2012) The occurrence of mixed infections of Symbiodinium (Dinoflagellata) within individual hosts. J Phycol 48:1306–1316
Finney JC, Pettay DT, Sampayo EM et al (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 60:250–263
Fitt WK (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 81:9–17
Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685
Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65
Fitt WK, Gates RD, Hoegh-Guldberg O et al (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J Exp Mar Biol Ecol 373:102–110
Fransolet D, Roberty S, Plumier J-C (2012) Establishment of endosymbiosis: the case of cnidarians and Symbiodinium. J Exp Mar Biol Ecol 420:1–7
Gattuso J-P, Allemand D, Frankignolle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am Zool 39:160–183
Glynn PW (1991) Coral reef bleaching in the 1980s and possible connections with global warming. Trends Ecol Evol 6:175–179
Glynn PW, D’Croz L (1990) Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8:181–191
Godinot C, Ferrier-Pagès C, Sikorski S et al (2013) Alkaline phosphatase activity of reef-building corals. Limnol Oceangr 58:227–234
Grottoli AG, Rodrigues LJ, Palardy JE (2007) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189
Harland AD, Nganro NR (1990) Copper uptake by the sea anemone Anemonia viridis and the role of zooxanthellae in metal regulation. Mar Biol 104:297–301
Hatcher BG (1988) The primary productivity of coral reefs: a beggar’s banquet. Trends Ecol Evol 3:106–111
Hatcher BG (1997) Organic production and decomposition. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, New York, pp 140–174
Heikoop JM, Dunn JJ, Risk MJ et al (1998) Relationship between light and the δ15N of coral tissue: examples from Jamaica and Zanzibar. Limnol Oceanogr 43:909–920
Hirose M, Kinzie RA III, Hidaka M (2001) Timing and process of entry of zooxanthellae into oocytes of hermatypic corals. Coral Reefs 20:273–280
Hoegh-Guldberg O (1994) Population dynamics of symbiotic zooxanthellae in the coral Pocillopora damicornis exposed to elevated ammonium concentrations. Pac Sci 48:263–272
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshwat Res 50:839–866
Hoegh-Guldberg O, Williamson J (1999) Availability of two forms of nitrogen in the coral Pocillopora damicornis and its symbiotic zooxanthellae. Mar Biol 133:561–570
Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Hollingsworth LL, Kinzie RA III, Lewis TD et al (2005) Phototaxis of motile zooxanthellae to green light may facilitate symbiont capture by coral larvae. Coral Reefs 24:523
Iglesias-Prieto R, Beltrán VH, LaJeunesse TC et al (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Lond B 271:1757–1763
Jaubert J, Gattuso J-P (1989) An integrated nitrifying-denitrifying biological system capable of purifying seawater in a closed circuit system Deuxieme Congres International d’Aquariologie. Bulletin de l’Institut Oceanographique, Monaco, No. special 5, Monaco, pp 101–106
Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162
Kawaguti S (1953) Ammonium metabolism of the reef corals. Biol J Okayama Univ 1:171–176
Kemp DW, Hernandez-Pech X, Iglesias-Prieto R et al (2014) Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnol Oceangr 59:788–797
Knowlton N, Jackson JBC (2008) Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6:215–220
Knowlton N, Rohwer F (2004) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162(Suppl):S51–S62
Kopp C, Pernice M, Domart-Coulon I et al (2013) Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen. mBio 4:e00052–00013
LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400
LaJeunesse TC, Pettay DT, Sampayo EM et al (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 37:785–800
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 48:1380–1391
Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192
Lesser MP, Stat M, Gates RD (2013) The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32:603–611
Lipschultz F, Cook CB (2002) Uptake and assimilation of 15N-ammonium by the symbiotic sea anemones Bartholomea annulata and Aiptasia pallida: conservation versus recycling of nitrogen. Mar Biol 140:489–502
Little AF, Van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494
Marubini F, Davies PS (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar Biol 127:319–332
Mazel CH, Lesser MP, Gorbunov MY et al (2003) Green-fluorescent proteins in Caribbean corals. Limnol Oceangr 48:402–411
Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA et al (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4:e6364
Miller DJ, Yellowlees D (1989) Inorganic nitrogen uptake by symbiotic marine cnidarians: a critical review. Proc R Soc Lond B 237:109–125
Milliman JD, Meade RH (1983) Worldwide delivery of river sediment to the oceans. J Geol 91:1–21
Muller-Parker G, Cook CB, D’Elia CF (1994) Elemental composition of the coral Pocillopora damicornis exposed to elevated seawater ammonium. Pac Sci 48:234–246
Muscatine L, D’Elia CF (1978) The uptake, retention, and release of ammonium by reef corals. Limnol Oceanogr 23:725–734
Muscatine L, Kaplan IR (1994) Resource partitioning by reef corals as determined from stable isotope composition. II. δ15N of zooxanthellae and animal tissue versus depth. Pac Sci 48:304–312
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–459
Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition. I. d13C of zooxanthellae and animal tissue vs depth. Mar Biol 100:185–193
Palumbi SR, Barshis DJ, Traylor-Knowles N et al (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–897
Pasternak Z, Bchar A, Abelson A, Achituv Y (2004) Initiation of symbiosis between the soft coral Heteroxenia fuscescens and its zooxanthellae. Mar Ecol Prog Ser 279:113–116
Rees TAV (1987) The green hydra symbiosis and ammonium I. The role of the host in ammonium assimilation and its possible regulatory significance. Proc R Soc Lond B 229:299–314
Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60:185–203
Roth MS, Deheyn DD (2013) Effects of cold stress and heat stress on coral fluorescence in reef-building corals. Sci Rpt 3: doi:10.1038/srep01421
Rowan R (1991) Molecular systematics of symbiotic algae. J Phycol 27:661–666
Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral/algal symbiosis. Proc Natl Acad Sci U S A 92:2850–2853
Rowan R, Powers DA (1992) Ribosomal RNA sequences and the diversity of symbiotic dinoflagellates (zooxanthellae). Proc Natl Acad Sci U S A 89:3639–3643
Salih A, Larkum AWD, Cox G, Kuhl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853
Santos SR, Coffroth MA (2003) Molecular evidence that dinoflagellates belonging to the genus Symbiodinium Freudenthal are haploid. Biol Bull 204:10–20
Simkiss K (1964) Phosphates as crystal poisons of calcification. Biol Rev 39:487–505
Smith SV (1981) Responses of Kaneohe Bay, Hawaii, to relaxation of sewage stress. In: Neilson BJ, Cronin LE (eds) Estuaries and nutrients. Humana Press, Clifton, pp 391–441
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 8:23–43s
Stat M, Baker AC, Bourne DG et al (2012) Molecular delineation of species in the coral holobiont. Adv Mar Biol 63:1–65
Swanson R, Hoegh-Guldberg O (1998) Amino acid synthesis in the symbiotic sea anemone Aiptasia pulchella. Mar Biol 131:83–93
Szmant AM, Ferrer LM, Fitzgerald LM (1990) Nitrogen excretion and O:N ratios in reef corals: evidence for conservation of nitrogen. Mar Biol 104:119–127
Takabayashi M, Adams LM, Pochon X, Gates RD (2012) Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai’i and Florida. Coral Reefs 31:157–167
Takahashi T (2004) Fate of industrial carbon dioxide. Science 305:352–353
Tchernov D, Gorbunov MY, de Vargas C et al (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci U S A 101:13531–13535
Thomas FIM, Atkinson MJ (1997) Ammonium uptake by coral reefs: effects of water velocity and surface roughness on mass transfer. Limnol Oceangr 42:81–88
Thornhill DJ, LaJeunesse TC, Kemp DW et al (2006) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722
Trench RK (1987) Dinoflagellates in non-parasitic symbioses. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell Scientific Publications, Oxford, pp 530–570
Trench RK (1993) Microalgal-invertebrate symbioses: a review. Endocyt Cell Res 9:135–175
Veron JEN (2000) Corals of the world, V1. Australian Institute of Marine Science, Townsville
Veron JEN, Pichon M (1976) Scleractinia of Eastern Australia. Part I. Families Thamnesteriidae, Astrocoeniidae, Pocilloporidae. Austr Inst Mar Sci Monogr Ser I:1–86
Wiedenmann J, D’Angelo C, Smith EG et al (2012) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:160–164
Wilkinson C (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville
Wooldridge SA (2009) Water quality and coral bleaching thresholds: formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58:745–751
Wooldridge SA (2010) Is the coral-algae symbiosis really ‘mutually beneficial’ for the partners? Bioessays 32:615–625
Yonge CM, Nicholls AG (1931) Studies on the physiology of corals. IV. The structure, distribution and physiology of zooxanthellae. Sci Rep Great Barrier Reef Exped 1:135–176
Acknowledgements
We thank Katrina Helm for drafting Figs. 5.1, 5.2, and 5.3. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. This is Contribution No. 1937 of the Harbor Branch Oceanographic Institute.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Muller-Parker, G., D’Elia, C.F., Cook, C.B. (2015). Interactions Between Corals and Their Symbiotic Algae. In: Birkeland, C. (eds) Coral Reefs in the Anthropocene. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7249-5_5
Download citation
DOI: https://doi.org/10.1007/978-94-017-7249-5_5
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-017-7248-8
Online ISBN: 978-94-017-7249-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)