Tracing 13C-enriched dissolved and particulate organic carbon in the bacteria-containing coral reef sponge Halisarca caerulea: Evidence for DOM feeding

Limnology and Oceanography

Volumn 53, Issue 4, 2008, Pages 1376-1386

  De Goeij, Jasper M ^a,b   Moodley, Leon ^c   Houtekamer, Marco ^c   Carballeira, Néstor M ^d   Van Duyl, Fleur C ^a  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^b CARMABI FOUNDATION   (Netherlands)

^c NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^d UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; CARBON ISOTOPE; CORAL REEF; DISSOLVED ORGANIC CARBON; ECOSYSTEM FUNCTION; ENVIRONMENTAL FATE; PARTICULATE ORGANIC CARBON; RESPIRATION; SOCIAL CHANGE; TRACER; TROPHIC INTERACTION;

ALGAE; ANTHOZOA; BACILLARIOPHYTA; BACTERIA (MICROORGANISMS); HALISARCA;

EID: 47349123676     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2008.53.4.1376     Document Type: Article

References (47)

1. BAINES, S. B., N. S. FISHER, AND J. J. COLE. 2005. Uptake of dissolved organic matter (DOM) and its importance to metabolic requirements of the zebra mussel, Dreissena polymorpha. Limnol. Oceanogr. 50: 36-47.
2. BOON, J. J., W. I. C. RIJPSTRA, J. W. DE LEEUW, AND P. A. SCHENCK. 1975. Phytenic acid in sediments. Nature 258: 414-416.
3. BOSCHKER, H. T. S., AND J. J. MIDDELBURG. 2002. Stable isotopes and biomarkers in microbial ecology. FEMS Microbiol. Ecol. 40: 85-95.
4. CANUEL, E. A., J. E. CLOERN, D. B. RINGELBERG, J. B. GUCKERT, AND G. H. RAU. 1995. Molecular and isotopic tracers used to examine sources of organic matter and its incorporation into the food webs of San Francisco Bay. Limnol. Oceanogr. 40: 67-81.
5. CARBALLEIRA, N., J. E. THOMPSON, E. AYANOGLU, AND C. DJERASSI. 1986. Biosynthetic studies of marine lipids. 5. The biosynthesis of long-chain branched fatty acids in marine sponges. J. Org. Chem. 51: 2751-2756.
6. CARBALLEIRA, N. M., L. MALDONADO, AND B. PORRAS. 1987. Isoprenoid fatty acids from marine sponges. Are sponges selective? Lipids 22: 767-769.
7. _, F. SHALABI, AND V. NEGRON. 1989. 2-Hydroxy fatty acids from marine sponges 2. The phospholipid fatty acids of the caribbean sponges Verongula gigantea and Aplysina archeri. Lipids 24: 229-232.
8. CARLSON, C. A. 2002. Production and removal processes, p. 91-152. In D. A. Hansell and C. A. Carlson [eds.], Biochemistry of marine dissolved organic matter. Academic Press.
9. DALSGAARD, J., M. ST. JOHN, G. KATTNER, D. MÜ LLER-NAVARRA, AND W. HAGEN. 2003. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46: 225-340.
10. DE GOEIJ, J. M., H. VAN DEN BERG, M. M. OOSTVEEN, E. H. G. EPPING, AND F. C. VAN DUYL. 2008. Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar. Ecol. Prog. Ser. 357: 139-151.
11. _, AND F. C. VAN DUYL. 2007. Coral cavities are sinks of dissolved organic carbon (DOC). Limnol. Oceanogr. 53: 2608-2617.
12. FAGERBAKKE, K. M., M. HELDAL, AND S. NORLAND. 1996. Content of carbon, nitrogen, oxygen, sulfur and phosphorus in native aquatic and cultured bacteria. Aquat. Microb. Ecol. 10: 15-27.
13. FROST, B. W. 1987. Porifera, p. 27-53. In T. J. Pandian and F. J. Vernberg [eds.], Animal energetics. Academic Press.
14. GINSBURG, R. N. 1983. Geological and biological roles of cavities in coral reefs, p. 148-153. In D. Barnes [ed.], Perspectives on coral reefs. Australian Institute of Marine Science.
15. GRAEVE, M., G. KATTNER, AND W. HAGEN. 1994. Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: Experimental evidence of trophic markers. J. Exp. Mar. Biol. Ecol. 182: 97-110.
16. GUO, L., AND P. H. SANTSCHI. 1997. Composition and cycling of colloids in marine environments. Rev. Geophys. 35: 17-40.
17. HALL, D., S. Y. LEE, AND T. MEZIANE. 2006. Fatty acids as trophic tracers in an experimental estuarine food chain: Tracer transfer. J. Exp. Mar. Biol. Ecol. 336: 42-53.
18. HARVEY, H. R. 2006. Sources and cycling of organic matter in the marine water column, p. 1-25. In J. K. Volkman [ed.], The handbook of environmental chemistry. Springer-Verlag.
19. HELDAL, M., S. NORLAND, AND O. TUMYR. 1985. X-ray microanalytic method for measurement of dry matter and elemental content of individual bacteria. Appl. Environ. Microbiol. 50: 1251-1257.
20. KOIKE, I., H. SHIGEMITSU, T. KAZUKI, AND K. KAZUHIRO. 1990. Role of sub-micrometre particles in the ocean. Nature 345: 242-244.
21. LATYSHEV, N. A., N. V. NAUMENKO, V. I. SVETASHEV, AND Y. Y. LATYPOV. 1991. Fatty acids of reef-building corals. Mar. Ecol. Prog. Ser. 76: 295-301.
22. LOH, A. N., J. E. BAUER, AND E. A. CANUEL. 2006. Dissolved and particulate organic matter source-age characterization in the upper and lower Chesapeake Bay: A combined isotope and biochemical approach. Limnol. Oceanogr. 51: 1421-1431.
23. MASOOD, A., K. D. STARK, AND N. SALEM JR. 2005. A simplified and efficient method for the analysis of fatty acid methyl esters suitable for large clinical studies. J. Lipid. Res. 46: 2299-2305.
24. MEZIANE, T., AND M. TSUCHIYA. 2000. Fatty acids as tracers of organic matter in the sediment and food web of a mangrove/intertidal flat ecosystem, Okinawa, Japan. Mar. Ecol. Prog. Ser. 200: 49-57.
25. 13C-labeling study. Limnol. Oceanogr. 45: 1224-1234.
26. MILLER, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory.
27. MOODLEY, L., H. T. S. BOSCHKER, J. J. MIDDELBURG, R. PEL, P. M. J. HERMAN, E. DE DECKERE, AND C. H. R. HEIP. 2000. Ecological significance of benthic foraminifera: 13C labelling experiments. Mar. Ecol. Prog. Ser. 202: 289-295.
28. _, J. J. MIDDELBURG, H. T. S. BOSCHKER, G. C. A. DUINEVELD, R. PEL, P. M. J. HERMAN, AND C. H. R HEIP. 2002. Bacteria and Foraminifera: Key players in a short term deep-sea benthic response to phytodetritus. Mar. Ecol. Prog. Ser. 236: 23-29.
29. PILE, A. J., M. R. PATTERSON, AND J. D. WITMAN. 1996. In situ grazing on plankton < 10 νm by the boreal sponge Mycale lingua. Mar. Ecol. Prog. Ser. 141: 95-102.
30. REISWIG, H. M. 1971. Particle feeding in natural populations of three marine demosponges. Biol. Bull. 141: 568-591.
31. RIBES, M., R. COMA, AND J. M. GILI. 1999. Natural diet and grazing rate of the temperate sponge Dysidea avara (Demospongiae, Dendroceratida) throughout an annual cycle. Mar. Ecol. Prog. Ser. 176: 179-190.
32. RICHTER, C., M. WUNSCH, M. RASHEED, I. KÖTTER, AND M. I. BADRAN. 2001. Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature 413: 726-730.
33. RODITI, H. A., N. S. FISHER, AND S. A. SAÑUDO-WILHELMY. 2000. Uptake of dissolved organic carbon and trace elements by zebra mussels. Nature 407: 78-80.
34. RONTANI, J. F., AND J. K. VOLKMAN. 2003. Phytol degradation products as biogeochemical tracers in aquatic environments. Org. Geochem. 34: 1-35.
35. SCHEFFERS, S. R., G. NIEUWLAND, R. P. M. BAK, AND F. C. VAN DUYL. 2004. Removal of bacteria and nutrient dynamics within the coral reef framework of Curaçao (Netherlands Antilles). Coral Reefs 23: 413-422.
36. TRANVIK, L. J., E. B. SHERR, AND B. F. SHERR. 1993. Uptake and utilization of 'colloidal DOM' by heterotrophic flagellates in seawater. Mar. Ecol. Prog. Ser. 92: 301-309.
37. VACELET, J., AND C. DONADEY. 1987. A new species of Halisarca (Porifera, Demospongiae) from the Caribbean, with remarks on the cytology and affinities of the genus, p. 5-12. In W. C. Jones [ed.], European contributions to the taxonomy of sponges. Publications of the Sherkin Island Marine Station. Litho Press.
38. VAN DUYL, F. C., G. J. GAST, W. STEINHOFF, S. KLOFF, M. J. W. VELDHUIS, AND R. P. M. BAK. 2002. Factors influencing the short-term variation in phytoplankton composition and biomass in coral reef waters. Coral Reefs 21: 293-306.
39. _, S. R. SCHEFFERS, F. I. M. THOMAS, AND M. DRISCOLL. 2006. The effect of water exchange on bacterioplankton depletion and inorganic nutrient dynamics in coral reef cavities. Coral Reefs 25: 23-36.
40. VASSEUR, P. 1974. The overhangs, tunnels and dark reef galleries of Tulear (Madagascar) and their sessile invertebrate communities. Proc. 2nd Int. Coral Reef Symp. 2: 143-160.
41. VISO, A. C., AND J. C. MARTY. 1993. Fatty acids from 28 marine microalgae. Phytochemistry 34: 1521-1533.
42. VOLKMAN, J. K. 2006. Lipid biomarkers for marine organic matter, p. 27-70. In J. K. Volkman [ed.], The handbook of environmental chemistry. Springer-Verlag.
43. _, S. M. BARRETT, S. I. BLACKBURN, M. P. MANSOUR, E. L. SIKES, AND F. GELIN. 1998. Microalgal biomarkers: A review of recent research developments. Org. Geochem. 29: 1163-1179.
44. WILD, C., M. HUETTEL, A. KLUETER, S. G. KREMB, M. Y. M. RASHEED, AND B. B. JØRGENSEN. 2004. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428: 66-70.
45. WILKINSON, C., AND R. GARRONE. 1980. Nutrition of marine sponges. Involvement of symbiotic bacteria in the uptake of dissolved carbon, p. 157-161. In D. C. Smith and Y. Tiffon [eds.], Nutrition in the lower metazoa. Pergamon Press.
46. WUNSCH, M., S. M. AL-MOGHRABI, AND I. KÖTTER. 2000. Communities of coral reef cavities in Jordan, Gulf of Aqaba (Red Sea). Proc. 9th Int. Coral Reef Symp. 1: 595-600.
47. YAHEL, G., J. H. SHARP, D. MARIE, C. HAESE, AND A. GENIN. 2003. In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: Bulk DOC is the major source for carbon. Limnol. Oceanogr. 48: 141-149.