Skip to main content
Log in

Ammonia flux, physiological parameters, and Symbiodinium diversity in the anemonefish symbiosis on Red Sea coral reefs

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Despite the ecological importance of anemonefish symbioses, little is known about how nutritional contributions from anemonefish interact with sea anemone physiology and Symbiodinium (endosymbiotic dinoflagellate) genetic identity under field conditions. On Red Sea coral reefs, we measured variation in ammonia concentrations near anemones, excretion rates of anemonefish, physiological parameters of anemones and Symbiodinium, and genetic identity of Symbiodinium within anemones. Ammonia concentrations among anemone tentacles were up to 49% above background levels, and anemonefish excreted ammonia significantly more rapidly after diurnal feeding than they did after nocturnal rest, similar to their excretion patterns under laboratory conditions. Levels of 4 physiological parameters (anemone protein content, and Symbiodinium abundance, chlorophyll a concentration, and division rate) were similar to those known for laboratory-cultured anemones, and in the field did not depend on the number of anemonefish per anemone or depth below sea surface. Symbiodinium abundance varied significantly with irradiance in the shaded reef microhabitats occupied by anemones. Most anemones at all depths harbored a novel Symbiodinium 18S rDNA variant within internal transcribed spacer region 2 (ITS2) type C1, while the rest hosted known ITS2 type C1. Association with Symbiodinium Clade C is consistent with the symbiotic pattern of these anemones on other Indo-Pacific reefs, but the C1 variant of Symbiodinium identified here has not been described previously. We conclude that in the field, anemonefish excrete ammonia at rapid rates that correlate with elevated concentrations among host anemone tentacles. Limited natural variation in anemonefish abundance may contribute to consistently high levels of physiological parameters in both anemones and Symbiodinium, in contrast to laboratory manipulations where removal of fish causes anemones to shrink and Symbiodinium to become less abundant.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Achituv Y, Mizrahi L (1996) Recycling of ammonium within a hydrocoral (Millepora dichotoma)-zooxanthellae-cirripede (Savignium milleporum) symbiotic association. Bull Mar Sci 58:856–860

    Google Scholar 

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology and biogeography of Symbiodinium. Ann Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  • Barneah O, Weis VM, Perez S, Benayahu Y (2004) Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition matters. Mar Ecol Prog Ser 275:89–95

    Article  CAS  Google Scholar 

  • Berkelmans R, van Oppen JH (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 273:2305–2312

    Article  Google Scholar 

  • Bluthgen N, Menzel F, Hovestadt T (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17:341–346

    Article  PubMed  Google Scholar 

  • Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326

    Article  Google Scholar 

  • Chadwick NE, Arvedlund M (2005) Abundance of giant sea anemones and patterns of association with anemonefish in the northen Red Sea. J Mar Biol Assoc UK 85:1287–1292

    Article  Google Scholar 

  • Chadwick NE, Ďuriš Z, Horká I (2008) Biodiversity and behavior of shrimps and fishes symbiotic with sea anemones in the Gulf of Aqaba, northern Red Sea. In: Por FD (ed) Aqaba-Eilat, The improbable gulf: environment, biodiversity, and preservation. Magnes Press, Hebrew University, Jerusalem, pp 209–223

    Google Scholar 

  • Cleveland A, Verde EA, Lee RW (2010) Nutritional exchange in a tropical tripartite symbiosis. Mar Biol. doi:10.1007/s00227-010-1583-5

    Google Scholar 

  • Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34

    Article  PubMed  CAS  Google Scholar 

  • 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. Mar Biol 114:317–325

    Article  CAS  Google Scholar 

  • Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13:2445–2458

    Article  PubMed  CAS  Google Scholar 

  • Falkowski PG, Jokiel PL, Kinzie RA (1990) Irradiance and corals. In: Dubinsky Z (ed) Coral Reefs, Ecosystems of the World. Elsevier Science Publishers, Amsterdam, pp 89–107

    Google Scholar 

  • Fautin DG, Allen GR (1997) Anemone fishes and their host sea anemones, Revisedth edn. Western Australian Museum, Perth, p 160

    Google Scholar 

  • Fukatsu T (1999) Acetone preservation: a practical technique for molecular analysis. Mol Ecol 8:1935–1945

    Article  PubMed  CAS  Google Scholar 

  • Godinot C, Chadwick NE (2009) Phosphate excretion by anemonefish and uptake by giant sea anemones: demand outstrips supply. Bull Mar Sci 85:1–9

    Google Scholar 

  • Godwin J, Fautin DG (1992) Defense of host actinians by anemonefishes. Copeia 3:902–907

    Article  Google Scholar 

  • Holbrook SJ, Schmitt RJ (1997) Settlement patterns and process in a coral damselfish: In situ nocturnal observations using infared video. Proc 8th Int Coral Reef Symp 2:1143–1148

    Google Scholar 

  • Holbrook SJ, Schmitt RJ (2004) Population dynamics of a damselfish: effects of a competitor that also is an indirect mutualist. Ecology 85:979–985

    Article  Google Scholar 

  • Holbrook SJ, Schmitt RJ (2005) Growth, reproduction and survival of a tropical sea anemone (Actiniaria): benefits of hosting anemonefish. Coral Reefs 24:67–73

    Article  Google Scholar 

  • Karako-Lampert S, Katcoff DJ, Achituv Y, Dubinsky Z, Stambler N (2004) Do clades of symbiotic dinoflagellates in scleractinian corals of the Gulf of Eilat (Red Sea) differ from those of other coral reefs? J Exp Mar Biol Ecol 311:301–314

    Article  Google Scholar 

  • Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62

    Article  PubMed  Google Scholar 

  • Kuguru B, Winters G, Beer S, Santos SR, Chadwick NE (2007) Adaptation strategies of the corallimorpharian Rhodactis rhodostoma to irradiance and temperature. Mar Biol 151:1287–1298

    Article  Google Scholar 

  • Kuguru B, Chadwick NE, Achituv Y, Zendbank K, Tchernov D (2008) Mechanisms of habitat segregation between corallimorpharians: photosynthetic parameters and Symbiodinium types. Mar Ecol Prog Ser 369:115–129

    Article  Google Scholar 

  • 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 37:866–880

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Article  Google Scholar 

  • LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134

    Article  PubMed  CAS  Google Scholar 

  • LaJeunesse TC, Loh WK, 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. Limnol Oceanogr 48:2046–2054

    Article  Google Scholar 

  • Lampert-Karako S, Stambler N, Katcoff DJ (2008) Effects of depth and eutrophication on the zooxanthella clades of Stylophora pistillata from the Gulf of Eilat (Red Sea). Aquat Conserv Mar Freshw Ecosyst 18:1039–1045

    Article  Google Scholar 

  • Liberman T, Genin A, Loya Y (1995) Effects on growth and reproduction of the coral Stylophora pistillata by the mutualistic damselfish Dascyllus marginatus. Mar Biol 121:741–746

    Article  Google Scholar 

  • Loya Y, Lubinsevsky H, Rosenfeld M, Kramarsky-Winter E (2004) Nutrient enrichment caused by in situ fish farms at Eilat, Red Sea is detrimental to coral reproduction. Mar Pollut Bull 49:344–353

    Article  PubMed  CAS  Google Scholar 

  • Maroz A, Fishelson L (1997) Juvenile production of Amphiprion bicinctus (Pomacentridae, Teleostei) and rehabilitation of impoverished habitats. Mar Ecol Prog Ser 151:295–297

    Article  Google Scholar 

  • Meyer JL, Schultz ET (1985) Migrating haemulid fishes as a source of nutrients and organic matter on coral reefs. Limnol Oceanogr 30:146–156

    Article  Google Scholar 

  • Miller DJ, Yellowlees D (1989) Inorganic nitrogen uptake by symbiotic marine cnidarians: a critical review. Proc R Soc Lond B 237:109–125

    Article  Google Scholar 

  • Mokady O, Loya Y, Lazar B (1998) Ammonium contribution from boring bivalves to their coral host—a mutualistic symbiosis? Mar Ecol Prog Ser 169:295–301

    Article  CAS  Google Scholar 

  • Muller-Parker G, Davy SK (2001) Temperate and tropical algal-sea anemone symbioses. Inver Biol 120:104–123

    Article  Google Scholar 

  • Patzner RA (2004) Associations with sea anemones in the Mediterranean Sea: a review. Ophelia 58:1–11

    Google Scholar 

  • Pinnegar JK, Polunin NVC (2006) Planktivorous damselfish supports significant nitrogen and phosphorus fluxes to Mediterranean reefs. Mar Biol 148:1089–1099

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Polunin NVC, Koike I (1987) Temporal focusing of nitrogen release by a periodically feeding herbivorous reef fish. J Exp Mar Biol Ecol 111:285–296

    Article  Google Scholar 

  • Porat D, Chadwick-Furman NE (2004) Effects of anemonefish on giant sea anemones: Expansion behavior, growth and survival. Hydrobiologia 530/531:513–520

    Google Scholar 

  • Porat D, Chadwick-Furman NE (2005) Effects of anemonefish on giant sea anemones: Ammonium uptake, zooxanthella content and tissue regeneration. Mar Freshw Behav Physiol 38:43–51

    Article  CAS  Google Scholar 

  • Randall JE, Fautin DG (2002) Fishes other than anemonefishes that associate with sea anemones. Coral Reefs 21:188–190

    Google Scholar 

  • Reynolds JM, Bruns BU, Fitt WK (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Nat Acad Sci USA 105:13674–13678

    Article  PubMed  CAS  Google Scholar 

  • Rohwer F, Seguritan V, Azam F (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10

    Article  Google Scholar 

  • Roopin M, Chadwick NE (2009) Benefits to host sea anemones from ammonia contributions of resident anemonefish. J Exp Mar Biol Ecol 370:27–34

    Article  CAS  Google Scholar 

  • Roopin M, Henry RP, Chadwick NE (2008) Nutrient transfer in a marine mutualism: patterns of ammonia excretion by anemonefish and uptake by giant sea anemones. Mar Biol 154:547–556

    Article  CAS  Google Scholar 

  • Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742

    Article  PubMed  CAS  Google Scholar 

  • Rowan R, Powers DA (1991a) A molecular genetic identification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1351

    Article  PubMed  CAS  Google Scholar 

  • Rowan R, Powers DA (1991b) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73

    Article  CAS  Google Scholar 

  • Rüppell E, Leuckart FS (1828) NeuewirbelloseThiere des RothenMeeres. In: Rüppell E (ed) Atlas zuder Reiseimnördlichen Afrika Erste Abtheilung Zoologie. Brunner, Frankfurt am Main, pp 1–22

    Google Scholar 

  • Sampayo EM, Dove S, LaJeunesse TC (2009) Cohesive molecular genetic data deliniate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519

    Article  PubMed  CAS  Google Scholar 

  • Santos SR, Taylor DJ, Kinzie RA, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111

    Article  PubMed  CAS  Google Scholar 

  • Santos SR, Kinzie RA III, Sakai K, Coffroth MA (2003) Molecular characterization of nuclear small subunit (18S)-rDNA pseudogenes in a symbiotic dinoflagellate (Symbiodinium, Dinophyta). J Eukaryot Microbiol 50:417–421

    Article  PubMed  CAS  Google Scholar 

  • Scott A, Harrison PL (2007) Embryonic and larval development of the host sea anemones Entacmaea quadricolor and Heteractis crispa. Biol Bull 213:110–121

    Article  PubMed  Google Scholar 

  • Solorzano L (1969) Determination of ammonium in natural waters by the phenol hypochlorite method. Limnol Oceanogr 14:799–801

    Article  CAS  Google Scholar 

  • Spotte S (1996) Supply of regenerated nitrogen to sea anemones by their symbiotic shrimp. J Exp Mar Biol Ecol 198:27–36

    Article  Google Scholar 

  • Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246

    Article  Google Scholar 

  • Stambler N, Levy O, Vaki L (2008) Photosynthesis and respiration of hermatypic zooxanthellate Red Sea corals from 5–7 m depth. Israeli J Plant Sci 56:45–53

    Article  CAS  Google Scholar 

  • Taylor DL (1974) Symbiotic marine algae: taxonomy and biological fitness. In: Vernberg WB (ed) Symbiosis in the Sea. University of South Carolina Press, Columbia, pp 245–262

    Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Nat Acad Sci USA 101:13531–13535

    Article  PubMed  CAS  Google Scholar 

  • Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006a) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722

    Article  Google Scholar 

  • Thornhill DJ, Fitt WK, Schmidt GW (2006b) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25:515–519

    Article  Google Scholar 

  • Titlyanov EA, Shaposhnikova MG, Zvalinskii VI (1980) Photosynthesis and adaptation of corals to irradiance. 1. Contents and native state of photosynthetic pigments in symbiotic microalgae. Photosynthetica 14:413–421

    CAS  Google Scholar 

  • Toller WW, Rowan R, Knowlton N (2001) Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol Bull 201:348–359

    Article  PubMed  CAS  Google Scholar 

  • Ulstrup KE, van Oppen MJH (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12:3477–3484

    Article  PubMed  CAS  Google Scholar 

  • Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59:1069–1080

    Article  PubMed  CAS  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc Nat Acad Sci USA 96:8007–8012

    Article  PubMed  CAS  Google Scholar 

  • Winters G, Loya Y, Rottgers R, Beer S (2003) Photoinhibition in shallow-water colonies of the coral Stylophora pistillata as measured in situ. Limnol Oceanogr 48:1388–1393

    Article  Google Scholar 

  • Zhang Z, Green BR, Cavalier-Smith T (2000) Phylogeny of ultrarapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. J Mol Evol 51:26–41

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Baraka Kuguru for field assistance, and Mark Liles, Dusty Kemp, and Greg Schmidt for assistance with DGGE analysis. Joseph Szczebak created the artwork for Fig. 1. Funding was provided by start-up funds to NEC and a graduate research award to MR, both from Auburn University. This research is submitted in partial fulfillment of the requirements for a M.Sc. degree to MR at Auburn University. All sampling for this study complies with the current laws of Israel. This is contribution #51 of the Auburn University Marine Biology Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nanette E. Chadwick.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Roopin, M., Thornhill, D.J., Santos, S.R. et al. Ammonia flux, physiological parameters, and Symbiodinium diversity in the anemonefish symbiosis on Red Sea coral reefs. Symbiosis 53, 63–74 (2011). https://doi.org/10.1007/s13199-011-0110-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-011-0110-x

Keywords

Navigation