Skip to main content

Host feeding and nutrient sufficiency for zooxanthellae in the sea anemone Aiptasia pallida

Abstract

Nutrient sufficiency of zooxanthellae in the sea anemone Aiptasia pallida cultured in low nutrient seawater depends on the availability of particulate food to the host. Zooxanthellae in anemones unfed for 20 to 30 d exhibited the following characteristics of nutrient deficiency: cell division rates decreased; chlorophyll a content gradually decreased from 2 to <1 pg cell−1; and C:N ratios increased from 7.5 to 16. Over a 3-mo period, algal populations in unfed anemones gradually decreased, indicating that zooxanthellae were lost faster than they were replaced by division. The mitotic index of zooxanthellae in unfed anemones was stimulated either by feeding the host or by the addition of inorganic N and P to the medium. Whether algae are nutrient-limited in hosts under field conditions has not been examined fully; however, C:N ratios in zooxanthellae from field-collected hosts are slightly higher (9.4 vs 7.5) than in hosts fed to repletion in laboratory cultures. This observation might indicate N limitation in the field.

This is a preview of subscription content, access via your institution.

Literature cited

  • Blank, R. J., Trench, R. K. (1986). Nomenclature of endosymbiotic dinoflagellates. Taxon 35: 286–294

    Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254

    Google Scholar 

  • Burris, R. E. (1983). Uptake and assimilation of 15NH4 + by a variety of corals. Mar. Biol. 75: 151–155

    Google Scholar 

  • Cates, N., McLaughlin, J. J. A. (1979). Nutrient availability for zooxanthellae derived from physiological activities of Condylactus spp. J. exp. mar. Biol. Ecol. 37: 31–41

    Google Scholar 

  • Chalker, B. E., Dunlap, W. C., Oliver, J. K. (1983). Bathymetric adaptations of reef-building corals at Davies Reef, Australia. II. Light saturation curves for photosynthesis and respiration. J. exp. mar. Biol. Ecol. 73: 37–56

    Google Scholar 

  • Chang, S. S., Prézelin, B. B., Trench, R. K. (1983). Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar. Biol. 76: 219–229

    Google Scholar 

  • Clayton, W. S. (1985). Pedal lacertion by the anemone Aiptasia pallida. Mar. Ecol. Prog. Ser. 21: 75–80

    Google Scholar 

  • Clayton, W. S., Lasken, H. R. (1984). Host feeding regime and zooxanthellal photosynthesis in the anemone, Aiptasia pallida (Verrill). Biol. Bull. mar. biol. Lab. Woods Hole 167: 590–600

    Google Scholar 

  • Cook, C. B. (1971). Transfer of 35S-labelled material from Aiptasia sp. to its endosymbiotic zooxanthellae. In: Lenhoff, H. M. et al. (eds.) Experimental Coelenterate Biology, University of Hawaii Press, Honolulu, p. 218–224

    Google Scholar 

  • Cock, C. B. (1972). Benefit to symbiotic zoochlorellae from feeding by green hydra. Biol. Bull. mar. biol. Lab., Woods Hole 142: 236–342

    Google Scholar 

  • Cook, C. B., D'Elia, C. F. (1987). Are natural populations of zooxanthellae ever nutrient-limited? Symbiosis 4: 199–212

    Google Scholar 

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

    Google Scholar 

  • D'Elia, C. F. (in press 1987 a). Biogeochemical nutrient cycles in coral reef ecosystems. In: Dubinsky, Z. (ed.) Coral Reef Ecosystems: Ecosystems of the World Series. Elsevier Science Publishers, Amsterdam

    Google Scholar 

  • D'Elia, C. F. (in press 1987 b). The cycling of elements in coral reefs. In: Alberts, J. J., Pomeroy, L. R. (eds.) A conference on ecosystem processes in honor of E. P. Odum. University of Georgia. Springer-Verlag, Heidelberg

    Google Scholar 

  • D'Elia, C. F., Webb, K. L. (1977). The dissolved nitrogen flux of reef corals. Proc. 3rd int. Coral Reef Symp., Vol I, University of Miami, Miami, p. 325–331

    Google Scholar 

  • Dawes, C. J., Chen, C.-P., Jewett-Smith, J., Marsh, A., Watts, S. A. (1984). Effect of phosphate and ammonium levels on photosynthetic and respiratory responses of the red alga Gracilaria verrucosa. Mar. Biol. 78: 325–328

    Google Scholar 

  • Domotor, S. L., D'Elia, C. F. (1984). Nutrient uptake kinetics and growth of zooxanthellae maintained in laboratory culture. Mar. Biol. 80: 93–101

    Google Scholar 

  • Falkowski, P. G., Dubinsky, Z. (1981). Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature, Lond. 289: 172–174

    Google Scholar 

  • Fitt, W. K., Chang, S. S., Trench, R. K. (1981). Motility patterns of different strains of the symbiotic dinoflagellate Symbiodinium (=Gymnodinium) microadriaticum (Freudenthal) in culture. Bull mar. Sci. 31: 436–433

    Google Scholar 

  • Goldman, J. R., McCarthy, J. J., Peavey, D. G. (1979). Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature, Lond 279: 210–215

    Google Scholar 

  • Gordon, D. M., Birch, P. B., McComb, A. J. (1981). Effects of inorganic phosphorus and nitrogen on the growth of an estuarine Cladophora in culture. Bot. Mat. 24: 93–106

    Google Scholar 

  • Graneli, E., Sundback, K. (1985). The response of planktonic and microbenthic algal assemblages to nutrient enrichment in shallow coastal waters, southwest Sweden. J. exp. mar. Biol. Ecol. 85: 253–268

    Google Scholar 

  • Hoegh-Gulderg, O., Hinde, R., Miscatine, L. (1986). Studies on a nudibranch that contains zooxanthellae II. Contribution of zooxanthellae to animal respiration (CZAR) in Pteraeolidia ianthina with high and low densities of zooxanthellae. Proc. R. Soc. London, Ser. B 228: 511–521

    Google Scholar 

  • Hunter, T. (1984). The energetics of asexual reproduction: pedal laceration in the symbiotic sea anemone Aiptasia pulchella (Carlgren 1943). J. exp. mar. Biol. Ecol. 83: 127–147

    Google Scholar 

  • Jeffrey, S. W., Haxo, F. T. (1968). Photosynthetic pigments of symbiotic dinoflagellates (zooxanthellae) from corals and clams. Biol. Bull. biol. Lab., Woods Hole 135: 145–165

    Google Scholar 

  • Lowry, O. H., Rosenbrough, N. J., Farr, A. L., Randall, R. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265–276

    Google Scholar 

  • McAuley, P. J. (1986). Isolation of viable uncontamined Chlorella from green hydra. Limnol. Oceanogr. 31: 222–224

    Google Scholar 

  • McDuff, R. E., Chisholm, S. W. (1982). The calculation of in situ growth rates of phytoplankton populations from fractions of cells undergoing mitosis: a clarification. Limnol. Oceanogr. 27: 783–788

    Google Scholar 

  • Menzel, D. W., Ryther, J. H. (1961). Annual variation in primary production of the Sargasso Sea off Bermuda. Deep-Sea Res 7: 282–288

    Google Scholar 

  • Meyer, J. L., Schultz, E. T. (1985). Tissue condition and growth rate of corals associated with schooling fish. Limnol. Oceanogr. 30: 157–166

    Google Scholar 

  • Morris, B., Barnes, J., Brown, F., Markham, J. (1977). The Bermuda Marine Environment. Volume I, Bermuda Biological Station for Research, Inc. Special Publication No. 15

  • Muller-Parker, G. (1984). Photosynthesis-irradiance responses and photosynthetic periodicity in the sea anemone Aiptasia pulchella and its zooxanthellae. Mar. Biol. 82: 225–232

    Google Scholar 

  • 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. (1987). Seasonal variation in light-shade adaptation of natural populations of the symbiotic sea anemone Aiptasia pulchella (Carlgren 1943) in Hawaii. J. exp. mar. Biol. Ecol. 112: 165–183

    Google Scholar 

  • Muscatine, L., Porter, J. W. (1977). Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27: 454–459

    Google Scholar 

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

    Google Scholar 

  • Muscatine, L., Marian, R. E. (1982). Dissolved inorganic nitrogen flux in symbiotic and nonsymbiotic medusae. Limnol. Oceanogr. 27: 910–927

    Google Scholar 

  • Muscatine, L., Wilkerson, F. P., McCloskey, L. R. (1986). Regulation of population density of symbiotic algae in a tropical marine jellyfish. Mar. Ecol. Prog. Ser. 32: 279–290

    Google Scholar 

  • Parker, G. M. (1984). Dispersal of zooxanthellae on coral reefs by predators on cnidarians. Biol. Bull. mar. biol. Lab., Woods Hole 167: 159–167

    Google Scholar 

  • Patton, J. S., Burris, J. E. (1983). Lipid synthesis extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar. Biol. 75: 131–136

    Google Scholar 

  • Porter, J. W., Muscatine, L., Dubinsky, Z., Falkowski, P. G. (1984). Primary production and photoadaptation in light-and shadeadapted colonies of the symbiotic coral, Stylophora pistillata. Proc. R. Soc. London, Ser. B 222: 161–180

    Google Scholar 

  • Schoenberg, D. A., Trench, R. K. (1980). Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of S. microadriaticum. Proc. R. Soc. London, Ser. B 207: 445–460

    Google Scholar 

  • Smith, G. J. (1986). Ontogenetic influences on carbon flux in Aulactinia stelloides polyps (Anthozoa: Actinaria) and their endosymbiotic algae. Mar. Biol. 92: 361–369

    Google Scholar 

  • Smith, D. C. (1979). From extracellular to intracellular: the establishment of a symbiosis. Proc. R. Soc. London, Ser. B 204: 115–130

    Google Scholar 

  • Snedecor, G. W., Cochran, W. G. (1980). Statistical Methods, 507 pp. Iowa University Press, Ames

    Google Scholar 

  • Steele, R. D. (1975). Stages in the life history of a symbiotic zooxanthella in pellets extruded by its host Aiptasia tagetes (Duch. and Mich.) (Coelenterata, Anthozoa). Biol. Bull. mar. biol. Lab., Woods Hole 149: 590–600

    Google Scholar 

  • Steele, R. D. (1976). Light intensity as a factor in the regulation of the density of symbiotic zooxanthellae in Aiptasia tagetes (Coelenterata, Anthozoa). J. Zool. (Lond.) 179: 387–405

    Google Scholar 

  • Steen, R. G. (1986). Evidence for heterotrophy by zooxanthellae in symbiosis with Aiptasia pulchella. Biol. Bull. mar. biol. Lab., Woods Hole 170: 267–278

    Google Scholar 

  • Sterrer, W. (ed.) (1986). Marine fauna and flora of Bermuda. Wiley-Interscience, New York

    Google Scholar 

  • Strathmann, R. R. (1967). Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol. Oceanogr. 12: 411–418

    Google Scholar 

  • Summons, R. E., Boag, T. S., Osmund, C. B. (1986). The effect of ammonium on photosynthesis and the pathway of ammonium assimilation in Symbiodinium microadriaticum in vitro and in symbiosis with tridacnid clams and corals. Proc. R. Soc. London, Ser. B 227: 147–159

    Google Scholar 

  • Szmant-Froelich, A., Pilson, M. E. Q. (1977). Nitrogen excretion by colonies of the temperate coral Astrangia danae with and without zooxanthellae. Proc. 3rd int Coral Reef Symp., Vol. I, Univ. of Miami, p. 418–423

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

    Google Scholar 

  • Trench, R. K. (1971). The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates III. The effect of homogenates of host tissues on the excretion of photosynthetic products in vitro by zooxanthellae from two marine coelenterates. Proc. R. Soc. London, Ser. B 177: 251–264

    Google Scholar 

  • Trench, R. K. (1979). The physiology of plant-animal symbiosis. Annu. Rev. Plant Physiol. 30: 485–531

    Google Scholar 

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

    Google Scholar 

  • Wilkerson, F. P., Trench, R. K. (1986). Uptake of dissolved inorganic nitrogen by the symbitic clam Tridacna gigas and the coral Acropora sp. Mar. Biol. 93: 237–246

    Google Scholar 

  • Wilkerson, F. P., Muscatine, L., Muller-Parker, G. (1983). Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol. Oceanogr. 28: 1009–1014

    Google Scholar 

  • Yonge, C. M., Nicholls, A. G. (1931). Studies on the physiology of corals IV. The structure, distribution and physiology of the zooxanthellae. Sci. Rpts. Gt. Barrier Reef Exped., Vol. I, p. 135–176

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by J. P. Grassle, Woods Hole

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cook, C.B., D'Elia, C.F. & Muller-Parker, G. Host feeding and nutrient sufficiency for zooxanthellae in the sea anemone Aiptasia pallida . Mar. Biol. 98, 253–262 (1988). https://doi.org/10.1007/BF00391203

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00391203

Keywords

  • Chlorophyll
  • Cell Division
  • Field Condition
  • Mitotic Index
  • Nutrient Deficiency