Advertisement

Marine Biology

, Volume 104, Issue 1, pp 119–127 | Cite as

Nitrogen excretion and O:N ratios in reef corals: Evidence for conservation of nitrogen

  • A. M. Szmant
  • L. M. Ferrer
  • L. M. FitzGerald
Article

Abstract

Rates of ammonia excretion, and respiration to excretion (atomic O:N) ratios were measured for three species of scleractinian coral from the Bahamas, during August 1986 and March 1987, to test the hypothesis that zooxanthellate reef species have lower rates of amino acid catabolism and higher dependence on lipid and carbohydrate catabolism than nonzooxanthellate species. Freshly collected individuals of two reef species,Montastrea annularis andAcropora cervicornis, have significantly lower mean ammonia excretion rates [51 ± 66 nmol (mg-at N)−1 h−1 and 192 ± 172 nmol (mg-at N)−1 h−1, respectively] than those of the tropical nonzooxanthellate speciesTubastrea coccinea [257 ± 68 nmol (mg-at N)−1 h−1]. The temperate nonzooxanthellate coralAstrangia poculata has mean excretion rates [632 ± 242 nmol (mg-at N)−1 h−1] which are much higher than those of all three tropical species. O:N ratios for the two reef species were generally greater than 300, while those of the nonzooxanthellate species ranged from 17 to 39 forT. coccinea and from 8 to 12 forA. poculata. The two reef species conserve nitrogen by having relatively low rates of amino acid catabolism, and support most of their metabolic needs by catabolizing the lipids and carbohydrates they receive from their zooxanthellae. The tropical nonzooxanthellate species has lower rates of ammonia excretion and respiration, and higher O:N ratios than the temperate nonzooxanthellate coral, which may be an indication that the former has less food available to it. The ammonia production rates of the reef species would support doubling times (growth rates) of the zooxanthellae of 13 to 22 d. These growth rates agree with observed rates obtained by mitotic index methods, and with suggestions that growth of zooxanthellae within many corals may be nitrogen-limited.

Keywords

Lipid Carbohydrate Respiration Production Rate Reef Coral 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature cited

  1. Baldwin, E. (1964). An introduction to comparative biochemistry. 4th ed Cambridge University Press, Cambridge, EnglandGoogle Scholar
  2. Båmstedt, U. (1985). Seasonal excretion rates of macrozooplankton from the Swedish west coast. Limnol. Oceanogr. 30: 607–617Google Scholar
  3. Battey, J. F., Patton, J. S. (1984). A reevaluation of glycerol in carbon translocation in zooxanthellae-coelenterate symbiosis. Mar. Biol. 79: 27–38Google Scholar
  4. Battey, J. F., Patton, J. S. (1987). Glycerol translocation inCondylactis gigantea. Mar. Biol. 95: 37–46Google Scholar
  5. Bayne, B. L., Scullard, C. (1977). Rates of nitrogen excretion by species ofMytilus (Bivalvia: Mollusca). J. mar. biol. Ass. U.K. 57: 5–369Google Scholar
  6. Boucher-Rodoni, R., Mangold, K. (1985). Ammonia excretion during feeding and starvation inOctopus vulgaris. Mar. Biol. 86: 193–197Google Scholar
  7. Campbell, J. W. (1973). Nitrogen excretion. In: Prosser, C. L. (ed.) Comparative animal physiology. 3rd ed. W. B. Saunders, Philadelphia, p. 279–316Google Scholar
  8. Cook, C. B., D'Elia, C. F. (1987). Are natural populations of zooxanthellae ever nutrient limited? Symbiosis 4: 199–212Google Scholar
  9. Cook, C. B., D'Elia, C. F., Muller-Parker, G. (1988). Host feeding and nutrient sufficiency for zooxanthellae in the sea anemoneAiptasia pallida. Mar. Biol. 98: 253–262Google Scholar
  10. Droop, M. R. (1963). Algae and invertebrates in symbiosis. Symp. Soc. gen. Microbiol. 13: 171–199Google Scholar
  11. Ferrer, L. M., Szmant, A. M. (1988). Nutrient regeneration by the endolithic community in coral skeletons. Proc. 6th int. Symp. coral Reefs (in press). [Choat, J. H. et al. (eds.) Sixth International coral Reef Symposium Executive Committee, Townsville, Australia]Google Scholar
  12. Fitt, W. K., Pardy, R. L. (1981). Effects of starvation, and light and dark on the energy metabolism of symbiotic and aposymbiotic sea anemones,Anthopleura elegantissima. Mar. Biol. 61: 199–205Google Scholar
  13. FitzGerald, L. M., Szmant, A. M. (1988). Amino acid metabolism: adaptations to low nutrient conditions? Proc. 6th int. Symp. coral Reefs (in press). [Choat, J. H. et al. (eds.) Sixth International Coral Reef Symposium Executive Committee, Townsville, Australia]Google Scholar
  14. Froelich, A. S. (1980). Studies of the reproduction, nutrition and symbiosis with zooxanthellae of the temperate scleractinian coralAstrangia danae. Ph.D. dissertation, University of Rhode IslandGoogle Scholar
  15. Gladfelter, E. H., Monahan, R. K., Gladfelter, W. B. (1978). Growth rates of five reef-building corals in the northeastern Caribbean. Bull. mar. Sci. 28: 728–734Google Scholar
  16. Hull, C. H., Nie, N. H. (1981). SPPS update. 7–9: new procedures and facilities for releases 7–9. McGraw Hill Book Co., New YorkGoogle Scholar
  17. Ikeda, T. (1972). Nutritional ecology of marine zooplankton. Mem. Fac. Fish. Hokkaido Univ. 22: 1–97Google Scholar
  18. Ikeda, T., Mitchell, A. W. (1982). Oxygen uptake, ammonia excretion and phosphate excretion by krill and other Antarctic zooplankton in relation to body size and chemical composition. Mar. Biol. 71: 283–298Google Scholar
  19. Johannes, R., Wiebe, W. (1970). Method for determination of coral tissue biomass and composition. Limnol. Oceanogr. 15: 822–824Google Scholar
  20. Kawaguti, S. (1953). Ammonium metabolism of the reef corals. Biol. J. Okayama Univ. 1: 171–176Google Scholar
  21. Kremer, P. (1982). Effects of food availability on the metabolism of the ctenophoreMnemiopsis mccradyi. Mar. Biol. 71: 149–156Google Scholar
  22. Kremer, P., Canino, M. F., Gilmer, R. W. (1986). Metabolism of epipelagic tropical ctenophores. Mar. Biol. 90: 403–412Google Scholar
  23. Lee, R. F., Hirota, J. (1973). Wax esters in tropical zooplankton and nekton and the geographical distribution of wax esters in marine copepods. Limnol. Oceanogr. 18: 227–239Google Scholar
  24. Marsh, J. A. (1970). Primary productivity of reef-building calcareous and red algae. Ecology 51: 255–263Google Scholar
  25. Muscatine, L. (1967). Glycerol excretion by symbiotic algae from corals andTridacna and its control by the host. Science, N.Y. 156: 516–519Google Scholar
  26. Muscatine, L. (1974). Endosymbiosis of cnidarians and algae. In: Muscatine, L. H. M. Lenhoff, (eds.) Coelenterate biology. Academic Press, New York, p. 359–395Google Scholar
  27. Muscatine, L., D'Elia, C. F. (1978). The uptake, retention and release of ammonium by reef corals. Limnol. Oceanogr. 23: 725–734Google Scholar
  28. Muscatine, L., Falkowski, P. G., Porter, J. W., Dubinsky, Z. (1984). Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coralStylophora pistillata. Proc. R. Soc. (Ser. B) 222: 181–202Google Scholar
  29. Muscatine, L., Lenhoff, H. M. (1965) Symbiosis of hydra and algae. II. Effects of limited food and starvation on growth of symbiotic and aposymbiotic hydra. Biol. Bull. mar. biol. Lab., Woods Hole 129: 316–328Google Scholar
  30. Muscatine, L., Marian, R. E. (1982). Dissolved inorganic nitrogen flux in symbiotic and nonsymbiotic medusae. Limnol. Oceanogr. 27: 910–927Google Scholar
  31. Muscatine, L., Masuda, H. and Burnap, R. (1979). Ammonium uptake by symbiotic and aposymbiotic reef corals. Bull. mar. Sci. 29: 572–575Google Scholar
  32. Patton, J. S., Burris, J. E. (1983). Lipid synthesis and extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar. Biol. 75: 131–136Google Scholar
  33. Peters, E. C., Cairns, S. D., Pilson, M. E. Q., Wells, J. W., Japp, W. C., Lang, J. C., Valeski, C. E., Gollahon, L. S. (1988). Nomenclature and biology ofAstrangia poculata. Proc. biol. Soc. Wash. 101: 234–250Google Scholar
  34. Pomeroy, L. R., Kuenzler, E. J. (1969). Phosphorus turnover by coral reef animals. Proc. 2nd natn. Symp. Radioecol. (Ann Arbor, 1967). 2: 474–482. (Copies available from: National Technical Service, U.S. Department of Commerce, Springfield, Va 22161, USA; Ref. AEC-CONF-670503)Google Scholar
  35. Porter, J. W. (1974). Zooplankton feeding by the Caribbean reefbuilding coralMontastrea annularis. Proc. 2nd int. Symp. coral Reefs 1: 111–125. [Cameron, A. M. et al. (eds.) Great Barrier Reef Committee, Brisbane, Australia]Google Scholar
  36. Porter, J. W. (1976). Autotrophy, heterotrophy and resource partitioning in Caribbean reef corals. Am. Nat. 110: 731–742Google Scholar
  37. Quetin, L. B., Ross, R. M., Uchio, K. (1980). Metabolic characteristics of mid water zooplankton: ammonia excretion, O:N ratios, and the effect of starvation. Mar. Biol. 59: 201–209Google Scholar
  38. Reimer, A. A. (1971). Observations on the relationships between several species of tropical zoanthids (Zoanthidea, Coelenterata) and their zooxanthellae. J. exp. mar. Biol. Ecol. 7: 207–214Google Scholar
  39. Slawyk, G., MacIsaac, J. J. (1972). Comparison of two automated ammonia methods in a region of coastal upwelling. Deep-Sea Res. 19: 521–524Google Scholar
  40. Steele, R. D. (1975). Stages in the life history of a symbiotic zooxanthella in pellets extruded by its hostAiptasia tagetes (Duch. and Mich.) (Coelenterata: Anthozoa). Biol. Bull. mar. biol. Lab., Woods Hole 149: 590–600Google Scholar
  41. Steele, R. D. (1976). Light intensity as a factor in the regulation of the density of symbiotic zooxanthellae inAiptasia tagetes (Coelenterata, Anthozoa). J. Zool., Lond. 179: 387–405Google Scholar
  42. Steele, R. D., Goreau, N. I. (1977). The breakdown of symbiotic zooxanthellae in the sea anemonePhylactis (=Qulactis)flosculifera (Actiniaria). J. Zool., Lond. 181: 421–437Google Scholar
  43. Syrett, P. J. (1981). Nitrogen metabolism of microalgae. In: Platt, T. (ed.) Physiological bases of phytoplankton ecology. Can. Bull. Fish. aquat. Sciences 210: 182–210Google Scholar
  44. Szmant-Froelich, A., Johnson, A. V., Hoehn, T., Battey, J., Smith, G. J., Fleischmann, E., Porter, J. W., Dallmeyer, D. (1981). The physiological effects of oil drilling mud on the Caribbean coralMontastrea annularis. Proc. 4th int. Symp. coral Reefs 1: 163–168. [Gomez, E. D. et al. (eds.) Marine Sciences Center, University of the Philippines, Quezon City]Google Scholar
  45. Szmant-Froelich, A., Pilson, M. E. Q. (1977). Nitrogen excretion by colonies of the temperate coralAstrangia danae with and without zooxanthellae. Proc. 3rd int. Symp. coral Reefs 1: 417–424. [Taylor, D. L. (ed.) School of Marine and Atmospheric Sciences, University of Miami]Google Scholar
  46. Szmant-Froelich, A., Pilson, M. E. Q. (1984). Effects of feeding frequency and symbiosis with zooxanthellae on nitrogen metabolism and respiration of the coralAstrangia danae. Mar. Biol. 81: 153–162Google Scholar
  47. Verity, P. G. (1985). Ammonia excretion rates of oceanic copepods and implications for estimates of primary production in the Sargasso Sea. Biol. Oceanogr. 3: 249–282Google Scholar
  48. Wilkerson, F. P., Kobayashi, D., Muscatine, L. (1988). Mitotic index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 7: 29–36Google Scholar
  49. Wilkerson, F. P., Muscatine, L. (1984). Uptake and assimilation of dissolved inorganic nitrogen by a symbiotic sea anemone. Proc. R. Soc. (Ser. B) 221: 71–86Google Scholar
  50. Wilkerson, F. P., Trench, R. K. (1986). Uptake of dissolved inorganic nitrogen by the symbiotic clamTridacna gigas and the coralAcropora sp. Mar. Biol. 93: 237–246Google Scholar
  51. Yamazato, K. (1970). Calcification in a solitary coral,Fungia scutaria Lamarck, in relation to environmental factors. Bull. Sci. Eng Div. Univ. Ryukyus Math (Naha, Okinawa) (Math. nat. Sciences) 13: 57–122Google Scholar
  52. Yonge, C. M., Nicholls, A. G. (1931). Studies on the physiology of corals. IV. The structure, distribution and physiology of the zooxanthellae. Scient. Rep. Gt Barrier Reef Exped. 1: 135–176Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • A. M. Szmant
    • 1
  • L. M. Ferrer
    • 1
  • L. M. FitzGerald
    • 1
  1. 1.Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA

Personalised recommendations