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Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals

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Abstract

Very little information exists on the effects of nitrate on corals, although this is the major form in which nitrogen is prescrit in tropical eutrophie coastal waters. In this study we incubated nubbins ofPorites porites and explants ofMontastrea annularis in laboratory photostats illuminated by halide lamps, with concentrations of nitrate of 0, 1, 5 and 20 μM, for 40 and 30 d, respectively, At the end of this period it was found that the population density of the zooxanthellae had increased significantly with increased nitrate concentration, suggesting nitrogen limitation of the growth rate of zooxanthellae in the control group. There were also significant increases in the amount of chlorophylla ande 2 per algal cell, in the volume of the algal cells, and in the protein per cell. Overall, the protein per unit surface increased, but this was attributable solely to increased algal protein: there was no significant change in host protein. Maximum gross photosynthesis normalized to surface area was enhanced by nitrate addition, reflecting the increase in algal population density. There was no change when normalized on a per cell basis. Respiration rate normalized to protein content was decreased by nitrate. The most dramatic change was in the rate of skeletogenesis, which decreased by ≅ in both species when exposed to nitrate enrichment. A model is presented which suggests that the diffusion-limited supply of CO2 from surrounding seawater is used preferentially by the enlarged zooxanthellae population for Photosynthesis, thereby reducing the availability of inorganic carbon for calcification. It is concluded that enhanced nitrate levels in tropical coastal waters will have a hitherto unrecognized effect on the growth rate of tropical coral reefs.

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References

  • Atkinson MJ, Carlson B, Crow GL (1995) Coral growth in highnutrient, low-pH seawater: a case study of corals raised in the Waikiki Aquarium. Coral Reefs 14: 215–223

    Google Scholar 

  • Berner T, Izhaki I (1994) Effect of exogcnous nitrogen levels on ultrastructure of zooxanthellae from the hermatypic coxalPocillopora damicornis. Pacif Sci 48: 254–262

    Google Scholar 

  • Burris JE, Porter JW, Laing WA (1983) Effects of carbon dioxide concentration on coxal photosynthesis. Mar Biol 75: 113–116

    Google Scholar 

  • Bythell JC (1990) Nutrient uptake in the reef-building coral Acropora palmata at natural environmental concentrations. Mar Ecol Prog Ser 68: 65–69

    Google Scholar 

  • Coffroth MA (1991) Cyclical mucous sheet formation on poritid corals in the San Blas Islands, Panama. Mar Biol 109: 35–40

    Google Scholar 

  • Cook CB, D'Elia CF, Muller-Parker G (1988) Host feeding and nutrient sufficiency for zooxanthellae in the sea anemoneAiptasia pallida. Mar Biol 98: 253–262

    Google Scholar 

  • Crossland CJ, Barnes DJ (1977) Nitrate assimilation enzymes from two hard corals,Acropora acuminata andGoniastrea australensis. Comp Biochem Physiol 57B: 151–157

    Google Scholar 

  • Davies PS (1984) The role of zooxanthellae in the nutritional energy requirements ofPocillopora eydouxi. Coral Reefs 2: 181–186

    Google Scholar 

  • Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101: 389–395

    Google Scholar 

  • Davies PS (1995) Coral nubbins and explants for reef assessment and laboratory ecotoxicology. Coral Reefs 14: 267–269

    Google Scholar 

  • D'Elia CF, Webb KL (1977) The dissolved nitrogen flux of reef corals. Proc 3rd int coxal Reef Symp 1: 325–330 [Taylor DL (ed) Rosenstiel School of Marine and Atmospheric Science, University of Miami]

    Google Scholar 

  • Dennison WC, Barnes DJ (1988) Effect of water motion on coxal photosynthesis and calcification. J exp mar Biol Ecol 115: 67–77

    Google Scholar 

  • Doty MS (1971) Measurement of water movement in reference to algal benthic growth. Botanica mar 14: 32–35

    Google Scholar 

  • Dubinsky Z, Stambler N, Ben-zion M, McCloskey LR, Muscatine L, Falkowsky PG (1990) The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc R Soc (Ser B) 239: 231–246

    Google Scholar 

  • Franzisket L (1974) Nitrate uptake by reef corals. Int Revue ges Hydrobiol 59: 1–7

    Google Scholar 

  • Harland AD, Davies PD (1995) Symbiont photosynthesis increases both respiration and photosynthesis in the symbiotic sea anemoneAnemonia viridis. Mar Biol 123: 715–722

    Google Scholar 

  • Hawker DW, Connell DW (1992) Standards and criteria for pollution control in coxal reef areas. In: Connell DW, Hawker DW (eds) Pollution in tropical aquatic systems. CRC Press, New York, pp 169–191

    Google Scholar 

  • Hoegh-Guldberg O, Smith GJ (1989) Influence of the population density of zooxanthellae and supply of ammonium on the biomass and metabolic characteristics of of the reef coralsSeriatophora hystrix andStylophora pistillata. Mar Ecol Prog Ser 57: 173–186

    Google Scholar 

  • Jeffrey SW, Humphxey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pfl 167: 191–194

    Google Scholar 

  • Kinsey DW (1987) Responses of coxal reef systems to elevated nutrient levels. In: Baldwin CL (ed) Nutrients in the Great Barrier Reef Region. Great Barrier Reef Marine Park Authority, Australia, pp 55–65

    Google Scholar 

  • Kinsey DW, Davies PI (1979) Effects of elevated nitrogen and phosphorus on coxal reef growth. Limnol Oceanogr 24: 935–940

    Google Scholar 

  • Lesser MP, Weis VM, Patterson MR, Jokiel PL (1994) Effects of morphology and water motion on carbon delivery and productivity in the reef coral,Pocillopora damicornis (Linnaeus): diffusion barriers, inorganic carbon limitation, and biochemical plasticity. J exp mar Biol Ecol 178: 153–179

    Google Scholar 

  • Lowry OH, Roscbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J biol Chem 193: 265–275

    PubMed  Google Scholar 

  • Markwell MAK, Haas SM, Bieber LL, Tolbert NE (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Analyt Biochem 87: 206–210

    PubMed  Google Scholar 

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

    Google Scholar 

  • Muller-Parker G, Cook CB, D'Elia CF (1994a) Elemental composition of the coralPocillopora damicornis exposed to elevated seawater ammonium. Pacif Sci 48: 234–246

    Google Scholar 

  • Muller-Parker G, McCloskey LR, Hoegh-Guldberg O, McAuley PJ (1994b) Effect of ammonium enrichment on animal and algal biomass of the coxalPocillopora damicornis. Pacif Sci 48: 273–283

    Google Scholar 

  • Muscatine L (1967) Glycerol excretion by symbiotic algae from corals and tridacna and its control by the host. Science, NY 156: 516–519

    Google Scholar 

  • Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coxal. Proc R Soc (Ser B) 236: 311–324

    Google Scholar 

  • Muscatine L, Falkowsky PG, Porter JW, Dubinsky Z (1984) Fate of photo synthetically fixed carbon in light- and shade-adapted colonies of the symbiotic coralStylophora pistillata. Proc R Soc (Ser B) 222: 181–202

    Google Scholar 

  • Prézelin BB (1987) Photosynthetic physiology of dinoflagellates. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell Scientific Publishers, Oxford, pp 174–223

    Google Scholar 

  • Rinkevich B, Loya Y (1983) Oriented translocation of energy in grafted reef corals. Coral Reefs 1: 243–247

    Google Scholar 

  • Snidvongs A, Kinzie III RA (1994) Effects of nitrogen and phosphorus enrichment on in vivo symbiotic zooxanthellae ofPocillopora damicornis. Mar Biol 118: 705–711

    Google Scholar 

  • Stambler N, Popper N, Dubinsky Z, Stimson J (1991) Effects of nutrient enrichment and water motion on the coralPocillopora damicornis. Pacif Sci 45: 299–307

    Google Scholar 

  • Stimson J (1992) The effect of ammonium addition on coxal growth rate. Proc. 7th int coral Reef Symp (Abstract) 1: p. 383 [Richmond RH (ed) University of Guam, Mangilao, Guam]

    Google Scholar 

  • Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coralPocillopora damicornis (L.) under nitrogen-enrichment and control conditions. J exp mar Biol Ecol 153: 63–74

    Google Scholar 

  • Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. 2nd edn. Bull Fish Res Bd Can 167: 1–310

    Google Scholar 

  • Syrett PJ (1981) Nitrogen metabolism of microalgae. Physiological bases of phytoplankton ecology. Can Bull Fish aquat Sciences 210: 182–210

    Google Scholar 

  • 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

    Google Scholar 

  • Tomascik T, Sander F (1985) Effects of eutrophication on reefbuilding corals. I. Growth rate of the reef-building coralMontastrea annularis. Mar Biol 87: 143–155

    Google Scholar 

  • Walter SD, Feinstein AR, Wells CK (1987) Coding ordinal independent variables in multiple regression analyses. Am J Epidem 125: 319–323

    Google Scholar 

  • Webb KL, Wiebe WJ (1978) The kinetics and possible significance of nitrate uptake by several algal-invertebrate symbioses. Mar Biol 47: 21–27

    Google Scholar 

  • Weis VM, Smith GJ, Muscatine L (1989) A “CO2 supply” mechanism in zooxanthellate cnidarians: role of carbonic anhydrase. Mar Biol 100: 195–202

    Google Scholar 

  • Wilkerson FP, Kremer P (1992) DIN, DON, PO4 flux by a medusa with algal symbionts. Mar Ecol Prog Sex 90: 237–250

    Google Scholar 

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

    Google Scholar 

  • Wilkerson FP, Trench RK (1986) Uptake of dissolved inorganic nitrogen by the symbiotic clamTridacna gigas and the coralAcropora sp. Mar Biol 93: 237–246

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis. 2nd edn. Prentice-Hall International, Inc., Englewood Cliffs, New Jersey

    Google Scholar 

Download references

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Authors and Affiliations

  1. Bellairs Research Institute of McGill University, St. James, Barbados

    F. Marubini

  2. Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, University of Glasgow, G12 8QQ, Glasgow, Scotland

    P. S. Davies

Authors
  1. F. Marubini
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  2. P. S. Davies
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Communicated by J.P. Thorpe, Port Erin F. Marubini

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Marubini, F., Davies, P.S. Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar. Biol. 127, 319–328 (1996). https://doi.org/10.1007/BF00942117

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  • DOI: https://doi.org/10.1007/BF00942117

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