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Nutrient transfer in a marine mutualism: patterns of ammonia excretion by anemonefish and uptake by giant sea anemones

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Abstract

Many symbioses involve multiple partners in complex, multi-level associations, yet little is known concerning patterns of nutrient transfer in multi-level marine mutualisms. We used the anemonefish symbiosis as a model system to create a balance sheet for nitrogen production and transfer within a three-way symbiotic system. We quantified diel patterns in excretion of ammonia by anemonefish and subsequent absorption by host sea anemones and zooxanthellae under laboratory conditions. Rates of ammonia excretion by the anemonefish Amphiprion bicinctus varied from a high of 1.84 μmole g−1 h−1 at 2 h after feeding, to a basal rate of 0.50 μmole g−1 h−1 at 24–36 h since the last meal. Conversely, host sea anemones Entacmaea quadricolor absorbed ammonia at a rate of 0.10 μmole g−1 h−1 during the daytime in ammonia-enriched seawater, but during the night reduced their absorption rate to near zero, indicating that ammonia uptake was driven by zooxanthella photosynthesis. When incubated together, net ammonia excretion was virturally zero, indicating that host anemones absorbed most of the ammonia produced by resident fish. Adult anemonefish weighed about 11 g under laboratory conditions, but on the coral reef may reach up to 64 g, resulting in a maximal potential ammonia load of >200 μmole h−1 produced by two adult fish during daylight hours. In contrast, host sea anemones weighed about 47 g in the laboratory, but under field conditions, large individuals may reach 680 g, so their maximal ammonia clearance rates may reach about 70 μmole h−1 during the daytime. As such, the ammonia load produced by adult anemonefish far exceeds the clearance rate of host anemones and zooxanthellae. Ammonia transfer likely occurs mainly during the daytime, when anemonefish consume zooplankton and excrete rapidly, and in turn the zooxanthellae are photosynthetically active and drive rapid ammonia uptake. We conclude that zooplanktivorous fishes that form mutualisms with coral reef cnidarians may serve as an important link between open water and benthic ecosystems, through the transfer of large quantities of nutrients to zooxanthellate hosts, thus enhancing coral reef productivity.

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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 

  • Allen GR (1991) Damselfishes of the World. Mergus Publishers, Melle, Germany, 271 pp

  • Allen GR, Randall JE (1980) A review of the damselfishes (Teleostei: Pomacentridae) of the Red Sea. Israel J Zool 29:1–98

    Google Scholar 

  • Arvedlund M, Iwao K, Brolund TM, Takemura A (2006) Juvenile Thalassoma amblycephalum Bleeker (Labridae, Teleostei) dwelling among the tentacles of sea anemones: a cleanerfish with an unusual client? J Exp Mar Biol Ecol 329:161–173

    Article  Google Scholar 

  • Becker JH, Grutter AS (2004) Cleaner shrimp do clean. Coral Reefs 23:515–520

    Google Scholar 

  • Bray RN, Purcell LJ, Miller AC (1986) Ammonium excretion in a temperate-reef community by a planktivorous fish, Chromis punctipinnis (Pomacentridae), and potential uptake by young giant kelp, Macrocystis pyrifera (Laminariales). Mar Biol 90:327–334

    Article  Google Scholar 

  • Bray RN, Miller AC, Johnson S, Krause PR, Robertson DL, Westcott AM (1988) Ammonium excretion by macroinvertebrates and fishes on a subtidal rocky reef in southern California. Mar Biol 100:21–30

    Article  CAS  Google Scholar 

  • Brett JR, Zala CA (1975) Daily pattern of nitrogen excretion and oxygen consumption of sockeye salmon (Oncorhynchus nerka) under controlled condition. J Fish Res Bd Can 32:2479–2486

    Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125

    Article  Google Scholar 

  • Bunkley-Williams L, Williams EH (1998) Ability of Pederson cleaner shrimp to remove juveniles of the parasitic cymothoid isopod, Anilocra haemuli, from the host. Crustaceana 71:862–869

    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 

  • Cleveland A, Verde EA, Lee R (2003) Investigating the physiological basis for the clownfish/host anemone symbiosis: do resident fish provide their host with nitrogen? Abstract, 4th internat symbiosis soc conference, Halifax, Nova Scotia

  • Cleveland A, Verde EA, Lee R (2006) Nutritional exchange in clownfish/host anemone symbiosis: stable isotope analysis demonstrates nutrient exchange is bi-directional. Abstract, 5th internat symbiosis congress, Vienna

  • Crossland CJ (1983) Dissolved nutrients in coral reef waters. In: Bames DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, Townsville, pp 56–68

    Google Scholar 

  • Danilo TD, Yap HT (2000) Ammonium and phosphate excretion in three common echinoderms from Philippine coral reefs. J Exp Mar Ecol Biol 251:227–238

    Article  Google Scholar 

  • Davy KS, Trautman DA, Borowitzka MA, Hinde R (2002) Ammonium excretion by a symbiotic sponge supplies the nitrogen requirements of its rhodophyte partner. J Exp Biol 205:3505–3511

    PubMed  CAS  Google Scholar 

  • Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci USA 95:8676–8680

    Article  PubMed  CAS  Google Scholar 

  • Durbin EG, Durbln AG (1981) Assimilation efficiency and nitrogen excretion of a filter-feeding planktivore, the Atlantic menhaden, Brevoortia tyrannus (Pisces: Clupeidae). Fish Bull US 79:601–616

    Google Scholar 

  • Ellis AG, Midgley JJ (1996) A new plant–animal mutualism involving a plant with sticky leaves and a resident hemipteran. Oecologia 106:478–481

    Article  Google Scholar 

  • Enders EC, Boisclair D, Boily P, Magnan P (2006) Effect of body mass and water temperature on the standard metabolic rate of juvenile yellow perch, Perca flavescens (Mitchill). Environ Biol Fish 76:399–407

    Article  Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals: ammonium ions and organic materials maintain the density of zooxanthellae. Bioscience 43:606–611

    Article  Google Scholar 

  • Fautin DG (1991) The anemonefish symbiosis: what is known and what is not. Symbiosis 10:23–46

    Google Scholar 

  • Fautin DG, Allen GR (1997) Anemone fishes and their host sea anemones: a guide for aquarists and divers, revised edition.Western Australian Museum, Perth, 160 pp

  • Fautin DG, Guo CC, Hwang JS (1995) Costs and benefits of the symbiosis between the anemoneshrimp Periclimenes brevicarpalis and its host Entacmaea quadricolor. Mar Ecol Prog Ser 129:77–84

    Article  Google Scholar 

  • Fricke HW (1979) Mating system, resource defense and sex change in the anemonefish Amphiprion akallopisos. Zeits Tierpsychol 50:313–326

    Google Scholar 

  • Glaholt SP Jr, Vanni MJ (2005) Ecological responses to simulated benthic-derived nutrient subsidies mediated by omnivorous fish. Freshw Biol 50:1864–1881

    Article  CAS  Google Scholar 

  • Godwin J, Fautin DG (1992) Defense of host actinians by anemonefishes. Copeia 3:902–908

    Article  Google Scholar 

  • Haertel-Borer SS, Allen DM, Dame RF (2004) Fishes and shrimps are significant sources of dissolved inorganic nutrients in intertidal salt marsh creeks. J Exp Mar Biol Ecol 311:79–99

    Article  CAS  Google Scholar 

  • Haines KC, Wheeler PA (1978) Ammonium and nitrate uptake by marine macrophytes Hypnea musciformis (Rhodophyta) and Macrocystis pyrifera (Phaeophyta). J Phycol 14:319–324

    Article  CAS  Google Scholar 

  • Hall RO, Koch BJ, Marshall MC, Taylor BW, Tronstad LM (2007) How body size mediates the role of animals in nutrient cycling in aquatic ecosystems. In: Hildrew AG, Raffaelli DG, Edmonds-Brown R (eds) Body size: the structure and function of aquatic ecosystems. Cambridge University Press, Cambridge, pp 286–305

  • Hattori A (2005) High mobility of the protandrous anemonefish Amphiprion frenatus: nonrandom pair formation in limited shelter space. Ichthyol Res 52:57–63

    Article  Google Scholar 

  • Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualism: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53

    Article  PubMed  Google Scholar 

  • Hoegh-Guldberg GO, Williamson J (1999) Availability of two forms of dissolved nitrogen to the coral Pocillopora damicornis and its symbiotic zooxanthellae. Mar Biol 133:561–570

    Article  CAS  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 

  • Jobling M (1981) The influence of feeding on the metabolic rates of fishes: a short review. J Fish Biol 18:385–400

    Article  Google Scholar 

  • Kobayashi M, Hattori A (2006) Spacing pattern and body size composition of the protandrous anemonefish Amphiprion frenatus inhabiting colonial host anemones. Ichthyol Res 53:1–6

    Article  Google Scholar 

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

    Google Scholar 

  • Meyer JL, Schultz ET (1985b) Tissue condition and growth rate of corals associated with schooling fish. Limnol Oceanogr 30:157–166

    Google Scholar 

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

  • Muscatine L, D’Elia CF (1978) The uptake, retention, and release of ammonium by reef corals. Limnol Oceanogr 23:725–734

    CAS  Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals mutualistic symbioses adapted to nutrient-poor environments. BioScience 27:454–460

    Article  Google Scholar 

  • Nizinski MS (1989) Ecological distribution, demography and behavioral observations on Periclimenes anthophilus, an atypical symbiotic cleaner shrimp. Bull Mar Sci 45:174–188

    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

    Article  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 

  • Roopin M (2007) Symbiotic benefits to sea anemones from the metabolic byproducts of anemonefish. M.Sc thesis, Department of Biological Sciences, Auburn University, 157 pp

  • Schaus MH, Vanni MJ, Wissing TE, Bremigan MT, Garvey JE, Stein RA (1997) Nitrogen and phosphorus excretion by detrivorous gizzard shad in a reservoir ecosytem. Limnol Oceanogr 42:1386–1397

    Article  CAS  Google Scholar 

  • Solorzano L (1969) Determination of ammonium in natural waters by the phenolhypochlorite 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 (2005) Bio-optical properties of the northern Red Sea and the Gulf of Eilat (Aqaba) during winter 1999. J Sea Res 54:186–203

    Article  Google Scholar 

  • Syrett PJ (1981) Nitrogen metabolism of microalgae. Can Bull Fish Aquat Sci 210:182–210

    Google Scholar 

  • Vanni MJ (2002) Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst 33:341–370

    Article  Google Scholar 

  • Whitledge TE (1982) Regeneration of nitrogen by the nekton and its significance in the northwest Africa upwelling ecosystem. Fish Bull 80:327–335

    CAS  Google Scholar 

  • Wilkerson FP, Muscatine L (1984) Uptake and assimilation of dissolved inorganic nitrogen by a symbiotic sea anemone. Proc R Soc Lond Ser B 221:71–86

    CAS  Google Scholar 

Download references

Acknowledgments

We thank the many undergraduate students and technicians who assisted in aquarium tank maintenance and animal care during this study. This study was submitted in partial fulfillment of the M.Sc. degree to MR at Auburn University. Funding was provided by start-up funds to NEC from Auburn University and by NSF IBN 02-30005 to RPH. Experiments performed in this study comply with the current laws of USA. This is publication #32 of the Marine Biology Program at Auburn University.

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Correspondence to Nanette E. Chadwick.

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Communicated by S.A. Poulet.

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Roopin, M., Henry, R.P. & Chadwick, N.E. Nutrient transfer in a marine mutualism: patterns of ammonia excretion by anemonefish and uptake by giant sea anemones. Mar Biol 154, 547–556 (2008). https://doi.org/10.1007/s00227-008-0948-5

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