Zooxanthellar symbionts shape host sponge trophic status through translocation of carbon

Biological Bulletin

Volumn 219, Issue 3, 2010, Pages 189-197

  Weisz, Jeremy B ^a,b   Massaro, Andrew J ^a   Ramsby, Blake D ^a,c   Hill, Malcolm S ^a  

^a UNIVERSITY OF RICHMOND   (United States)

^b LINFIELD COLLEGE   (United States)

^c UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENTHIC-PELAGIC COUPLING; CARBON; CARBONATE; CORAL REEF; CYST; DINOFLAGELLATE; MARINE ECOSYSTEM; MARINE ENVIRONMENT; NITROGEN; SHALLOW WATER; SPONGE; SYMBIONT; SYMBIOSIS; TRANSLOCATION; TROPHIC STATUS;

ANTHOZOA; CLIONA; DINOPHYCEAE; FORAMINIFERA; INVERTEBRATA; MOLLUSCA; PROTISTA;

EID: 78650663269     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.1086/BBLv219n3p189     Document Type: Article

References (41)

1. Carlos, A. A., B. K. Baillie, M. Kawachi, and T. Maruyama. 1999.Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. J.Phycol. 35: 1054-1062.
2. Chanton, J. P., and F. G. Lewis. 1999. Plankton and dissolved inorganic carbon isotopic composition in a river-dominated estuary:Apalachicola Bay, Florida. Estuar. Coasts 22: 575-583.
3. Corredor, J. E., C. R. Wilkinson, V. P. Vicente, J. M. Morell, and E. Otero. 1988. Nitrate release by Caribbean reef sponges. Limnol. Oceanogr. 33: 114-120.
4. Falkowski, P. G., and Z. Dubinsky. 1981. Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289: 172-174.
5. Fogel, M. L., and L. A. Cifuentes. 1993. Isotope fractionation during primary production. Pp. 73-100 in Organic Geochemistry, M. H. Engel and S. A. Macko, eds. Springer, New York.
6. Fü tterer, D. K. 1974. Significance of the boring sponge Cliona for the origin of fine grained material of carbonate sediments. J. Sediment. Res. A 44: 79-84.
7. Garson, M. J., A. E. Flowers, R. I. Webb, R. D. Charan, and E. J. McCaffrey. 1998. A sponge/dinoflagellate association in the haplosclerid sponge Haliclona sp.: cellular origin of cytotoxic alkaloids by Percoll density gradient fractionation. Cell Tissue Res. 293: 365-373.
8. Garson, M. J., R. Clark, R. I. Webb, K. L. Field, and R. D. Charan. 1999. Ecological role of cytotoxic alkaloids: Haliclona n. sp., an unusual sponge/dinoflagellate association. Mem. Queensl. Mus. 44: 205-213.
9. Granados, C., C. Carmargo, Z. Zea, and J. A. Sánchez. 2008. Phylogenetic relationships among zooxanthellae (Symbiodinium) associated to excavating sponges (Cliona spp.) reveal an unexpected lineage in the Caribbean. Mol. Phylogenet. Evol. 49: 554-560.
10. Granek, E. F., J. E. Compton, and D. L. Phillips. 2009. Mangroveexported nutrient incorporation by sessile coral reef invertebrates. Ecosystems 12: 462-472.
11. Hentschel, U., K. M. Usher, and M. W. Taylor. 2006. Marine sponges as microbial fermenters. FEMS Microbiol. Ecol. 55: 167-177.
12. Hill, M. S. 1996. Symbiotic zooxanthellae enhance boring and growth rates of the tropical sponge Anthosigmella varians forma varians. Mar. Biol. 125: 649-654.
13. Hill, M. S. 1999. Morphological and genetic examination of phenotypic variability in the tropical sponge Anthosigmella varians. Mem. Queensl. Mus. 44: 239-247.
14. Lamb, K., and P. K. Swart. 2008. The carbon and nitrogen isotopic values of particulate organic material from the Florida Keys: a temporal and spatial study. Coral Reefs 27: 351-362.
15. Lipschultz, F., and C. B. Cook. 2002. Uptake and assimilation of N-15-ammonium by the symbiotic sea anemones Bartholomea annulata and Aiptasia pallida: conservation versus recycling of nitrogen. Mar. Biol. 140: 489-502.
16. Muscatine, L., and E. Cernichiari. 1969. Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. 137: 506-523.
17. Phillips, D. L., and J. W. Gregg. 2001. Uncertainty in source partitioning using stable isotopes. Oecologia 127: 171-179.
18. Piniak, G. A., and F. Lipschultz. 2002. Role of host feeding and inorganic nitrogen in the partitioning of prey nitrogen between host and zooxanthellae in the anemone Aiptasia pallida. Pp. 527-532 in Proceedings of the 9th International Coral Reef Symposium, Vol. 1, M. K. Moosa et al., eds. 23-27 October 2000, Bali, Indonesia.
19. Rosell, D., and M. J. Uriz. 1992. Do associated zooxanthellae and the nature of the substratum affect survival, attachment and growth of Cliona viridis (Porifera, Hadromerida)? An experimental approach. Mar. Biol. 114: 503-507.
20. Rutzler, K. 1975. The role of burrowing sponges in bioerosion. Oecologia 19: 203-216.
21. Rutzler, K. 1990. Associations between Caribbean sponges and photosynthetic organisms. Pp. 455-466 in New Perspectives in Sponge Biology, K. Rutzler, ed. Smithsonian Institution Press, Washington, DC.
22. Sara, M., and L. Liaci. 1964. Symbiotic associations between zooxanthellae and two marine sponges of the genus Cliona. Nature 203: 321.
23. Scalera-Liaci, L., M. Sciscioli, E. Lepore, and E. Gaino. 1999. Symbiotic zooxanthellae in Cinachyra tarentina, a non-boring demosponge. Endocytobiosis Cell Res. 13: 105-114.
24. Schmahl, G. 1990. Community structure and ecology of sponges associated with four southern Florida coral reefs. Pp. 376-383 in New Perspectives in Sponge Biology, K. Rutzler, ed. Smithsonian Institution Press, Washington, DC.
25. Schönberg, C. H. L. 2002. Substrate effects on the bioeroding demosponge Cliona orientalis. 1. Bioerosion rates. P. S. Z. N.: Mar. Ecol. 23: 313-326.
26. Schönberg, C. H. L., and W. K. W. Loh. 2005. Molecular identity of the unique symbiotic dinoflagellates found in the bioeroding demosponge Cliona orientalis. Mar. Ecol. Prog. Ser. 299: 157-166.
27. Schönberg, C. H. L., and R. Suwa. 2007. Why bioeroding sponges are better hosts for symbiotic dinoflagellates than many corals. Pp. 569- 580 in Porifera Research: Biodiversity, Innovation and Sustainability, Proceedings of the 7th International Sponge Symposium, M. R. Custódio et al., eds. 7-13 May 2006, Rio de Janeiro.
28. Schönberg, C. H. L., R. Suwa, M. Hidaka, and W. K. W. Loh. 2008. Sponge and coral zooxanthellae in heat and light: preliminary results of photochemical efficiency monitored with pulse amplitude modulated fluorometry. Mar. Ecol. 29: 247-258.
29. Simpson, T. L. 1984. The Cell Biology of Sponges. Springer-Verlag, New York.
30. Southwell, M. W. 2007. Sponge impacts on coral reef N cycling, Florida Keys, USA. Ph.D. dissertation, University of North Carolina at Chapel Hill.
31. Sullivan, K. M., and M. Chiappone. 1992. A comparison of belt quadrant and species presence absence sampling of stony coral (Scleractinia and Milleporina) and sponges for evaluating species patterning on patch reefs of the central Bahamas. Bull. Mar. Sci. 50: 464 - 488.
32. Tanaka, Y., T. Miyajima, I. Koike, T. Hayashibara, and H. Ogawa. 2006. Translocation and conservation of organic nitrogen within the coral-zooxanthella symbiotic system of Acropora pulchra, as demonstrated by dual isotope-labeling techniques. J. Exp. Mar. Biol. Ecol. 336: 110-119.
33. Vacelet, J. 1982. Algal-sponge symbioses in the coral reef of New Caledonia: a morphological study. Pp. 713-719 in Proceedings of the 4th International Coral Reef Symposium, Vol. 2, E. D. Gomez et al., eds. 18-22 May 1981, University of the Philippines, Manila.
34. Veuger, B., B. D. Eyre, D. Maher, and J. J. Middelburg. 2007. Nitrogen incorporation and retention by bacteria, algae, and fauna in a subtropical intertidal sediment: An in situ 15N-labeling study. Limnol. Oceanogr. 52: 1930-1942.
35. Weisz, J. B. 2006. Measuring impacts of associated microbial communities on Caribbean reef sponges: searching for symbiosis. Ph.D. dissertation, University of North Carolina at Chapel Hill.
36. Weisz, J. B., U. Hentschel, N. Lindquist, and C. S. Martens. 2007. Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar. Biol. 152: 475-483.
37. Wiedenmayer, F. 1977. Shallow Water Sponges of the Western Bahamas. Birkhauser Verlag, Basel.
38. Wilkinson, C. R. 1983. Net primary productivity in coral reef sponges. Science 219: 410-412.
39. Wilkinson, C. R. 1987. Significance of microbial symbionts in sponge. Symbiosis 4: 135-146.
40. Wilkinson, C. R. 1992. Symbiotic interactions between marine sponges and algae. Pp. 112-151 in Algae and Symbioses, W. Reisser, ed. Biopress, Bristol, UK.
41. Yellowlees, D., T. A. V. Rees, and W. Leggat. 2008. Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ. 31: 679-694.