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

Marine Biology

Volumn 154, Issue 3, 2008, Pages 547-556

  Roopin, Modi ^a   Henry, Raymond P ^a   Chadwick, Nanette E ^a  

^a AUBURN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION; AMMONIA; BIOLOGICAL PRODUCTION; CLEARANCE RATE; CORAL REEF; EXCRETION; INVERTEBRATE; LABORATORY METHOD; MUTUALISM; NUTRIENT UPTAKE; PERCIFORM; PLANKTIVORE; SEAWATER; ZOOXANTHELLA;

ACTINIARIA; AMPHIPRION BICINCTUS; ANEMONE; ANTHOZOA; CNIDARIA; ENTACMAEA QUADRICOLOR; PISCES;

EID: 42449122595     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-008-0948-5     Document Type: Article

References (57)

1. 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
2. Allen GR (1991) Damselfishes of the World. Mergus Publishers, Melle, Germany, 271 pp
3. Allen GR, Randall JE (1980) A review of the damselfishes (Teleostei: Pomacentridae) of the Red Sea. Israel J Zool 29:1-98
4. 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
5. Becker JH, Grutter AS (2004) Cleaner shrimp do clean. Coral Reefs 23:515-520
6. 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
7. 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
8. 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
9. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119-125
10. 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
11. 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
12. 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
13. 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
14. 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
15. 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
16. 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
17. Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci USA 95:8676-8680
18. 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
19. Ellis AG, Midgley JJ (1996) A new plant-animal mutualism involving a plant with sticky leaves and a resident hemipteran. Oecologia 106:478-481
20. 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
21. 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
22. Fautin DG (1991) The anemonefish symbiosis: what is known and what is not. Symbiosis 10:23-46
23. 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
24. 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
25. Fricke HW (1979) Mating system, resource defense and sex change in the anemonefish Amphiprion akallopisos. Zeits Tierpsychol 50:313-326
26. Glaholt SP Jr, Vanni MJ (2005) Ecological responses to simulated benthic-derived nutrient subsidies mediated by omnivorous fish. Freshw Biol 50:1864-1881
27. Godwin J, Fautin DG (1992) Defense of host actinians by anemonefishes. Copeia 3:902-908
28. 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
29. Haines KC, Wheeler PA (1978) Ammonium and nitrate uptake by marine macrophytes Hypnea musciformis (Rhodophyta) and Macrocystis pyrifera (Phaeophyta). J Phycol 14:319-324
30. 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
31. Hattori A (2005) High mobility of the protandrous anemonefish Amphiprion frenatus: nonrandom pair formation in limited shelter space. Ichthyol Res 52:57-63
32. 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
33. 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
34. Holbrook SJ, Schmitt RJ (2005) Growth, reproduction and survival of a tropical sea anemone (Actiniaria): benefits of hosting anemonefish. Coral Reefs 24:67-73
35. Jobling M (1981) The influence of feeding on the metabolic rates of fishes: a short review. J Fish Biol 18:385-400
36. 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
37. Meroz A, Fishelson L (1997) Juvenile production of Amphiprion bicinctus (Pomacentridae, Teleostei) and rehabilitation of impoverished habitats. Mar Ecol Prog Ser 151:295-297
38. Meyer JL, Schultz ET (1985a) Migrating haemulid fishes as a source of nutrients and organic matter on coral reefs. Limnol Oceanogr 30:146-156
39. Meyer JL, Schultz ET (1985b) Tissue condition and growth rate of corals associated with schooling fish. Limnol Oceanogr 30:157-166
40. Miller DJ, Yellowlees D (1989) Inorganic nitrogen uptake by symbiotic marine cnidarians: a critical review. Proc R Soc Lond Ser B 237:109-125
41. 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
42. Muscatine L, D'Elia CF (1978) The uptake, retention, and release of ammonium by reef corals. Limnol Oceanogr 23:725-734
43. Muscatine L, Porter JW (1977) Reef corals mutualistic symbioses adapted to nutrient-poor environments. BioScience 27:454-460
44. Nizinski MS (1989) Ecological distribution, demography and behavioral observations on Periclimenes anthophilus, an atypical symbiotic cleaner shrimp. Bull Mar Sci 45:174-188
45. Porat D, Chadwick-Furman NE (2004) Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival. Hydrobiologia 530/531:513-520
46. 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
47. Randall JE, Fautin DG (2002) Fishes other than anemonefishes that associate with sea anemones. Coral Reefs 21:188-190
48. 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
49. 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
50. Solorzano L (1969) Determination of ammonium in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799-801
51. Spotte S (1996) Supply of regenerated nitrogen to sea anemones by their symbiotic shrimp. J Exp Mar Biol Ecol 198:27-36
52. Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. BioScience 51:235-246
53. 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
54. Syrett PJ (1981) Nitrogen metabolism of microalgae. Can Bull Fish Aquat Sci 210:182-210
55. Vanni MJ (2002) Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst 33:341-370
56. Whitledge TE (1982) Regeneration of nitrogen by the nekton and its significance in the northwest Africa upwelling ecosystem. Fish Bull 80:327-335
57. 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