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Effects of nutritional history on nitrogen assimilation in congeneric temperate and tropical scleractinian corals

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Abstract

The nutritional history of corals is known to affect metabolic processes such as inorganic nutrient uptake and photosynthesis, but little is known about how it affects assimilation efficiency of ingested prey items or the partitioning of prey nitrogen between the host and symbiont. The temperate scleractinian coral Oculina arbuscula and its tropical congener Oculina diffusa were acclimated to three nutritional regimes (fed twice weekly, starved, starved with an inorganic nutrient supplement), then fed Artemia nauplii labeled with the stable isotope tracer 15N. Fed corals of both species had the lowest assimilation efficiencies (36–51% for O. arbuscula, 38–57% for O. diffusa), but were not statistically different from the other nutritional regimes. Fed and starved corals also had similar NH4+ excretion rates. This is inconsistent with decreased nitrogen excretion and reduced amino acid catabolism predicted by both the nitrogen recycling and conservation paradigms. In coral host tissue, ~90% of the ingested 15N was in the TCA-insoluble (protein and nucleic acids) and ethanol-soluble (amino acids/low molecular weight compounds) within 4 h of feeding. The TCA-insoluble pool was also the dominant repository of the label in zooxanthellae of both species (40–53% in O. arbuscula, 50–60% in O. diffusa). However, nutritional history had no effect on the distribution of prey 15N within the biochemical pools of the host or the zooxanthellae for either species. This result is consistent with the nitrogen conservation hypothesis, as preferential carbon metabolism would minimize the effects of starvation on nitrogen-containing biochemical pools.

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References

  • Achituv Y, Ben-Zion M, Mizrahi L (1994) Carbohydrate, lipid, and protein content of zooxanthellae and animal fractions of the coral Pocillopora damicornis exposed to ammonium enrichment. Pac Sci 48:224–233

    CAS  Google Scholar 

  • Anthony KRN (1999) Coral suspension feeding on fine particulate matter. J Exp Mar Biol Ecol 232:85–106

    Article  Google Scholar 

  • Burris RH (1983) Uptake and assimilation of 15NH4+ by a variety of corals. Mar Biol 75:151–156

    CAS  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 

  • Clayton W, Lasker HR (1984) Host feeding regime and zooxanthellal photosynthesis in the sea anemone, Aiptasia pallida. Biol Bull 167:590–600

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Cook CB, Muller-Parker G, D’Elia CF (1992) Ammonium enhancement of dark carbon fixation and nitrogen limitation in symbiotic zooxanthellae: effects of feeding and starvation of the sea anemone Aiptasia pallida. Limnol Oceanogr 37:131–139

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Davy SK, Cook CB (2001) The relationship between nutritional status and carbon flux in the zooxanthellate sea anemone Aiptasia pallida. Mar Biol 139:999–1005

    Article  CAS  Google Scholar 

  • D’Elia CF (1977) The uptake and release of dissolved phosphorus by reef corals. Limnol Oceanogr 22:301–315

    CAS  Google Scholar 

  • D’Elia CF, Cook CB (1988) Methylamine uptake by zooxanthellae–invertebrate symbioses: insights into host ammonium environment and nutrition. Limnol Oceanogr 33:1153–1165

    CAS  Google Scholar 

  • D’Elia C, Webb K (1977) The dissolved nitrogen flux of reef corals. Proc 3rd Int Coral Reef Symp, Miami, pp 325–330

  • D’Elia CF, Wiebe WJ (1990) Biogeochemical nutrient cycles in coral reef ecosystems. In: Dubinsky Z (ed) Ecosystems of the world, vol 25: coral reefs. Elsevier, Amsterdam, pp 49–74

  • Dubinsky Z, Jokiel PL (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324

    Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. BioScience 34:705–709

    CAS  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

    Google Scholar 

  • Ferrier-Pages C, Gattuso JP, Cauwet G, Jaubert J, Allemand D (1998) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172:265–274

    CAS  Google Scholar 

  • Ferrier-Pages C, Gattuso JP, Dallot S, Jaubert J (2000) Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19:103–113

    Article  Google Scholar 

  • Ferrier-Pages C, Witting J, Tambutte E, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22:229–240

    Article  Google Scholar 

  • Fitt WK, Pardy RL (1981) Effects of starvation, and light and dark on the energy metabolism of symbiotic and aposymbiotic sea anemones, Anthopleura elegantissima. Mar Biol 61:199–206

    Google Scholar 

  • Fitt WK, Pardy RL, Littler MM (1982) Photosynthesis, respiration and contribution to community productivity of the symbiotic sea anemone Anthopleura elegantissima. J Exp Mar Biol Ecol 61:213–232

    Article  CAS  Google Scholar 

  • FitzGerald LM, Szmant AM (1988) Amino acid metabolism: adaptations to low nutrient conditions? Proc 6th Int Coral Reef Symp, Townsville 3:5–9

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

    Google Scholar 

  • Grover R, Maguer JF, Reynaud-Vaganay S, Ferrier-Pages C (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol Oceanogr 47:782–790

    Google Scholar 

  • Hoegh-Guldberg O (1994) Population dynamics of symbiotic zooxanthellae in the coral Pocillopora damicornis exposed to elevated ammonium [(NH4)2SO4] concentrations. Pac Sci 48:263–272

    CAS  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 the reef corals Seriatopora hystrix and Stylophora pistillata. Mar Ecol Prog Ser 57:173–186

    CAS  Google Scholar 

  • Houlbreque F, Tambutte E, Ferrier-Pages C (2003) Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 296:145–166

    Article  Google Scholar 

  • Johannes R, Coles S and Kuenzel N (1970) The role of zooplankton in the nutrition of some scleractinian corals. Limnol Oceanogr 15:579–586

    Google Scholar 

  • Kelty R (2000) Phosphorus uptake and allocation in the sea anemone Aiptasia pallida and the coral Madracis mirabilis. PhD dissertation, University of Maryland, College Park, Md.

  • Lenhoff HM, Roffman B (1971) Two methods for fractionating small amounts of radioactive tissue. In: Lenhoff HM, Muscatine L, Davis LV (eds) Experimental coelenterate biology. University of Hawaii Press, Honolulu, pp 265–271

  • Lipschultz F, Cook CB (2002) Uptake and assimilation of 15N-ammonium by the sea anemones, Aiptasia pallida and Bartholomea annulata: interaction of host and zooxanthellae. Mar Biol 140:489–502

    Article  CAS  Google Scholar 

  • Macintyre IG, Pilkey OH (1969) Tropical reef corals: tolerance of low temperatures on the North Carolina continental shelf. Science 166:374–375

    Google Scholar 

  • Marubini F, Davies PS (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar Biol 127:319–328

    CAS  Google Scholar 

  • McAuley PJ, Cook CB (1994) Effects of host feeding and dissolved ammonium on cell division and nitrogen status of zooxanthellae in the hydroid Myrionema amboinense. Mar Biol 121:343–348

    Google Scholar 

  • Miller MW (1995) Growth of a temperate coral: effects of temperature, light, depth, and heterotrophy. Mar Ecol Prog Ser 122:217–225

    Google Scholar 

  • Mills MM (2000) Corals feeding on sediments? Ingestion, assimilation, and contributions to coral nutrition. PhD dissertation, University of Maryland, College Park, Md.

  • Mills MM, Lipschultz F, Sebens KP (2004) Particulate matter ingestion and associated nitrogen uptake by four species of scleractinian corals. Coral Reefs (in press)

  • Muller-Parker G (1985) Effect of feeding regime and irradiance on the photophysiology of the symbiotic sea anemone Aiptasia pulchella. Mar Biol 90:65–74

    Google Scholar 

  • Muller-Parker G, D’Elia C, Cook CB (1988) Nutrient limitation of zooxanthellae: effects of host feeding history on nutrient uptake by isolated algae. Proc 6th Int Coral Reef Symp, Townsville 3:15–19

  • Muller-Parker G, Cook CB, D’Elia CF (1990) Feeding affects phosphate fluxes in the symbiotic sea anemone Aiptasia pallida. Mar Ecol Prog Ser 60:283–290

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    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, Pool RR, Cernichiari E (1972) Some factors influencing selective release of soluble organic material by zooxanthellae from reef corals. Mar Biol 13:298–308

    CAS  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 coral. Proc R Soc Lond B 236:311–324

    Google Scholar 

  • Parsons RT, Maita Y, Lalli CR (1984) A manual of chemical and biological methods for seawater analysis. Pergamon, Elmsford

  • Piniak GA (2001) The effects of symbiotic condition and nutritional history on prey capture and use by anemones and corals. PhD dissertation, Duke University, Durham, N.C.

  • Piniak GA, Lipschultz F (2002) Role of host feeding and inorganic nitrogen in the partitioning of prey nitrogen between host and zooxanthellae in the anemone Aiptasia pallida. Proc 9th Int Coral Reef Symp, Bali, pp 527–532

  • Piniak GA, Lipschultz F, McClelland J (2003) Assimilation and partitioning of prey nitrogen within two anthozoans and their endosymbiotic zooxanthellae. Mar Ecol Prog Ser 262:125–136

    Google Scholar 

  • Rahav O, Dubinsky Z, Achituv Y, Falkowski PG (1989) Ammonium metabolism in the zooxanthellate coral, Stylophora pistillata. Proc R Soc Lond B 236:325–337

    CAS  Google Scholar 

  • Rees TAV, Ellard FM (1989) Nitrogen conservation and the green hydra symbiosis. Proc R Soc Lond B 236:203–212

    CAS  Google Scholar 

  • Reynaud S, Ferrier-Pages C, Sambrotto R, Julliet-Leclerc A, Jaubert J, Gattuso JP (2002) Effect of feeding on the carbon and oxygen isotopic composition in the tissues and skeleton of the zooxanthellate coral Stylophora pistillata. Mar Ecol Prog Ser 238:81–89

    Google Scholar 

  • Roberts JM, Davies PS, Fixter LM (1999) Symbiotic anemones can grow when starved: nitrogen budget for Anemonia viridis in ammonium-supplemented seawater. Mar Biol 133:29–35

    Article  Google Scholar 

  • Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar Biol 127:303–317

    Google Scholar 

  • Simkiss K (1964) Phosphates as crystal poisons of calcification. Biol Rev 39:487–505

    CAS  PubMed  Google Scholar 

  • Smith GJ, Muscatine L (1999) Cell cycle of symbiotic dinoflagellates: variation in G1 phase-duration with anemone nutritional status and macronutrient supply in the Aiptasia pulchella–Symbiodinium pulchrorum symbiosis. Mar Biol 134:405–418

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New York

  • Steen RG (1986) Evidence for heterotrophy by zooxanthellae in symbiosis with Aiptasia pulchella. Biol Bull 170:267–278

    Google Scholar 

  • Stimson J, Kinzie RA III (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153:63–74

    Google Scholar 

  • Szmant AM (1997) Nutrient effects on coral reefs: a hypothesis on the importance of topographic and trophic complexity on nutrient dynamics. Proc 8th Int Coral Reef Symp, Panama 2:1527–1532

  • Szmant AM, Ferrer LM, FitzGerald LM (1990) Nitrogen excretion and atomic oxygen to nitrogen ratios in reef corals: evidence for conservation of nitrogen. Mar Biol 104:119–128

    CAS  Google Scholar 

  • Szmant-Froelich A (1981) Coral nutrition: comparison of the fate of 14C from ingested labeled brine shrimp and from the uptake of NaH14CO3 by its zooxanthellae. J Exp Mar Biol Ecol 55:133–144

    Article  CAS  Google Scholar 

  • Szmant-Froelich A, Pilson M (1977) Nitrogen excretion by colonies of the temperate coral Astrangia danae with and without zooxanthellae. Proc 3rd Int Coral Reef Symp, Miami, pp 417–423

  • Szmant-Froelich A, Pilson MEQ (1980) The effects of feeding frequency and symbiosis with zooxanthellae on the biochemical composition of Astrangia danae Milne Edwards and Haime 1849. J Exp Mar Biol Ecol 48:85–97

    Article  CAS  Google Scholar 

  • Szmant-Froelich A, Pilson MEQ (1984) Effects of feeding frequency and symbiosis with zooxanthellae on nitrogen metabolism and respiration of the coral Astrangia danae. Mar Biol 81:153–162

    CAS  Google Scholar 

  • Wang JT, Douglas AE (1998) Nitrogen recycling or nitrogen conservation in an alga–invertebrate symbiosis? J Exp Biol 201:2445–2453

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Zamer WE (1986) Physiological energetics of the intertidal sea anemone Anthopleura elegantissima: I. Prey capture, absorption efficiency and growth. Mar Biol 92:299–314

    Google Scholar 

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Acknowledgements

This work was supported by the PADI Foundation, the Oak Foundation, the Munson Foundation, Sigma Xi, an Aleane Webb Dissertation Research Fellowship, and a National Science Foundation Dissertation Improvement Grant (no. 9972616) to G.A.P. The manuscript was improved by comments from W. Kirby-Smith, R. Forward, L. Crowder, and two anonymous reviewers. This is contribution no. 1650 of the Bermuda Biological Station for Research.

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  1. Gregory A. Piniak

    Present address: USGS Pacific Science Center, 400 Natural Bridges Drive, Santa Cruz, CA 95060, USA

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  1. Duke University Marine Laboratory, 135 Duke Marine Lab Road, Beaufort, NC 28516, USA

    Gregory A. Piniak

  2. Bermuda Biological Station for Research, Ferry Reach, GE01, St. George’s , Bermuda

    Fredric Lipschultz

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  1. Gregory A. Piniak
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Correspondence to Gregory A. Piniak.

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Communicated by P.W. Sammarco, Chauvin

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Piniak, G.A., Lipschultz, F. Effects of nutritional history on nitrogen assimilation in congeneric temperate and tropical scleractinian corals. Marine Biology 145, 1085–1096 (2004). https://doi.org/10.1007/s00227-004-1410-y

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