Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-22T18:43:18.742Z Has data issue: false hasContentIssue false
  • English
  • Français

Trophic importance of meiofauna to polychaetes in a seagrass (Zostera marina) bed as traced by stable isotopes

Published online by Cambridge University Press:  05 September 2013

Sun_Yong Ha ,
Won-Ki Min ,
Dong-Sung Kim  and
Kyung-Hoon Shin
Sun_Yong Ha
Affiliation:
Department of Environmental Marine Sciences, Hanyang University, 1271-3 dong, Sangnok-gu, Ansan, Kyeonggi-do, 425-791, Republic of Korea
Won-Ki Min
Affiliation:
Korea Ocean Research and Development Institute, Sa 2-dong, Sangrok-gu, Ansan, Kyeonggi-do, 425-600, Republic of Korea
Dong-Sung Kim
Affiliation:
Korea Ocean Research and Development Institute, Sa 2-dong, Sangrok-gu, Ansan, Kyeonggi-do, 425-600, Republic of Korea
Kyung-Hoon Shin*
Affiliation:
Department of Environmental Marine Sciences, Hanyang University, 1271-3 dong, Sangnok-gu, Ansan, Kyeonggi-do, 425-791, Republic of Korea
*
Correspondence should be addressed to: K.-H. Shin, Department of Environmental Marine Sciences, Hanyang University, 1271-3 dong, Sangnok-gu, Ansan, Kyeonggi-do, 425-791, Republic of Korea email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Stable carbon and nitrogen isotope ratios of benthic invertebrates and their potential food sources, such as suspended particulate organic matter (POM), benthic microalgae, attached algae and seagrass, were identified in Dong-dae Bay during the winter. The carbon stable isotope ratios demonstrate that filter feeders, such as oysters (−19.5 ± 1.0‰), use benthic microalgae (−21.2 ± 0.2‰) as a major food, and polychaetes such as Glycera spp. (−14.0 ± 0.6 ‰) preferentially use meiofauna, such as nematodes (−14.0 ± 0.4‰) and copepods (−13.3 ± 1.0‰). These meiofauna may feed on mixed resources (including bacteria) with the isotope ratios between benthic microalgae (−21.2 ± 0.2‰) and seagrass (−9.3 ± 01.0‰). These findings are consistent with the trophic enrichment in the nitrogen isotope ratios (by 3–4‰) between consumers and food sources. Moreover, the results of the MixSIR model based on the observed isotope ratios suggest a large seagrass contribution to the food sources of benthic organisms such as meiofauna (~53.7–62.6%) and macrobenthos (~41.1–68%) through the food web. This model additionally suggests a relatively large contribution of benthic microalgae to the food sources of filter feeders (i.e. 26.4% for oysters).

Keywords

stable isotopeZostera marinameiofaunabenthic microalgaeMixSIR
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 1 , February 2014 , pp. 121 - 127
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aberle, N. and Malzahn, A.M. (2007) Interspecific and nutrient-dependent variations in stable isotope fractionation: experimental studies simulating pelagic multitrophic systems. Oceologia 154, 291–303.CrossRefGoogle ScholarPubMed
Anesio, A.M., Abreu, P.C. and Biddanda, B.A. (2003) The role of free and attached microorganisms in the decomposition of estuarine macrophyte detritus. Estuarine, Coastal and Shelf Science 56, 197–201.CrossRefGoogle Scholar
Barillé, L., Prou, J., Héral, M. and Razet, D. (1997) Effects of high natural seaton concentrations on the feeding, selection, and absorption of the oyster Crassostrea gigas (Thunberg). Journal of Experimental Marine Biology and Ecology 212, 149–172.CrossRefGoogle Scholar
Bell, S.S., Walters, K. and Kern, J.C. (1984) Meiofauna from seagrass habitats: a review and prospectus for future research. Estuaries 7, 331–338.CrossRefGoogle Scholar
Blanchard, G.F., Sauriau, P.G., Cariou-Le, G., Gouleau, D., Garet, M.J., and Olivier, F. (1997) Kinetics of tidal resuspension of microbiota: testing the effects of sediment cohesiveness and bioturbation using flume experiments. Marine Ecology Progress Series 151, 17–25.CrossRefGoogle Scholar
Bunn, S.E., Barton, D.R., Hynes, N., Power, G. and Pope, M.A. (1989) Stable isotope analysis of carbon flow in a tundra river ecosystem. Canadian Journal of Fisheries and Aquatic Sciences 46, 1769–1775.CrossRefGoogle Scholar
Bunn, S.E., Loneragan, N.R. and Kempser, M.A. (1995) Effects of acid washing on stable ratios of C and N in penaeid shrimp and seagrass: implications for food-web studies using multiple stable isotopes. Limnology and Oceanography 40, 622–625.CrossRefGoogle Scholar
Bustamante, R. and Branch, G. (1996) The dependence of intertidal consumers on kelp-derived organic matter on the west coast of South Africa. Journal of Experimental Marine Biology and Ecology 196, 1–28.CrossRefGoogle Scholar
Coffin, R.B., Fry, B. and Wright, R.T. (1989) Carbon isotopic compositions of estuarine bacteria. Limnology and Oceanography 34, 1305–1310.CrossRefGoogle Scholar
Congie, B. and Barillé, L. (1999) Does bivalve mucus favour the growth of their main food source, microalgae? Oceanologica Acta 22, 441–450.Google Scholar
Congi, B., Barillé, L., Massé, G. and Beninger, P.G. (2003) Selection and processing of large suspended algae in the oyster Crassostrea gigas. Marine Ecology Progress Series 250, 145–152.Google Scholar
Couch, C.A. (1989) Carbon and nitrogen stable isotopes of meiobenthos and their food resources. Estuarine, Coastal and Shelf Science 28, 433–441.CrossRefGoogle Scholar
Crosby, M.P., Langdon, C.J. and Newell, R.I.E. (1989) Importance of refractory plant material to the carbon budget of the oyster Crassostrea virginica. Marine Biolgoy 100, 343–352.CrossRefGoogle Scholar
Danovaro, R. (1996) Detritus–bacteria–meiofauna interactions in a seagrass bed (Posidonia oceanica) of the NW Mediterranean. Marine Biolgy 127, 1–13.CrossRefGoogle Scholar
Danovaro, R. and Fabiano, M. (1995) Seasonal and interannual variation of benthic bacteria in a seagrass bed of the Mediterranean Sea: relationship with labile organic compounds and other environmental factors. Aquatic Microbial Ecology 9, 17–26.CrossRefGoogle Scholar
Danovaro, R. and Gambi, C. (2002) Biodiversity and trophic structure of nematode assemblages in seagrass systems: evidence for a coupling with changes in food availability. Marine Biology 141, 667–677.Google Scholar
Danovaro, R., Fabiano, M. and Boyer, M. (1994) Seasonal changes of benthic bacteria in a seagrass bed (Posidonia oceanica) of the Ligurian Sea in relation to origin composition and fate of the sediment organic matter. Marine Biology 119, 489–500.CrossRefGoogle Scholar
Decottignies, P., Beninger, P.G., Rincé, Y. and Riera, P. (2007) Trophic interactions between two introduced suspension-feeders, Crepidula fornicate and Crassostrea gigas, are influenced by seasonal effects and qualitative selection capacity. Journal of Experimental Marine Biology and Ecology 342, 231–241.CrossRefGoogle Scholar
Deegan, L.A. and Garritt, R.H. (1997) Evidence for spatial variability in estuarine food webs. Marine Ecology Progress Series 147, 31–47.CrossRefGoogle Scholar
De Jonge, V.N. and van Beusekom, J.E.E. (1992) Contribution of resuspended microphytobenthos to total phytoplankton in the Ems estuary. Limnology and Oceanography 40, 766–778.Google Scholar
DeNiro, M.J. and Epstein, S. (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.CrossRefGoogle Scholar
DeNiro, M.J. and Epstein, S. (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.CrossRefGoogle Scholar
De Troch, M., Gurdebeke, S., Fiers, F. and Vincx, M. (2001) Zonation and structuring factors of meiofauna communities in a tropical seagrass bed (Gazi Bay, Kenya). Journal of Sea Research 45, 45–61.CrossRefGoogle Scholar
Doi, H., Chang, K.H. and Nakano, S. (2011) Nitrogen and carbon isotope fractionations of zooplankton consumers in ponds: potential effects of seston C:N stoichiometry. Marine and Freshwater Research 62, 66–71.CrossRefGoogle Scholar
Doi, H., Matsumasa, M., Fujikawa, M., Kanou, K., Suzuki, T. and Kikuchi, E. (2009) Macroalgae and seagrass contribution to gastropods in sub-tropical and temperate tidal flats. Journal of the Marine Biological Association of the United Kingdom 89, 399–404.CrossRefGoogle Scholar
Dubois, S., Jean-Louis, B., Bertrand, B. and Lefebvre, S. (2007) Isotope trophic-step fractionation of suspension-feeding species: implications for food partitioning in coastal ecosystems. Journal of Experimental Marine Biology and Ecology 351, 121–128.CrossRefGoogle Scholar
Ellison, A.M. (2004) Bayesian inference in ecology. Ecology Letters 7, 509–520.CrossRefGoogle Scholar
Escavarage, V., Gareía, M.E. and Castel, J. (1989) The distribution of meiofauna and its contribution to detritic pathways in tidal flats (Arcachon Bay, France). Scientia Marina 53, 551–559.Google Scholar
Fry, B. (2006) Stable isotope ecology. New York: Springer.CrossRefGoogle Scholar
Fry, B. and Sherr, E.B. (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contributions in Marine Science 27, 13–47.Google Scholar
Heck, K., Able, K., Roman, C. and Fahay, M. (1995) Composition, abundance, biomass, and production of macro fauna in a New England estuary: comparisons among eelgrass meadows and other nursery habitats. Estuaries and Coasts 18, 379–389.CrossRefGoogle Scholar
Herman, P.M.J., Middelburg, J.J., Widdows, J., Lucas, C.H. and Heip, C.H.R. (2000) Stable isotopes as trophic tracers: combining field sampling and manipulative labelling of food resources for macrobenthos. Marine Ecology Progress Series 204, 79–92.CrossRefGoogle Scholar
Hilborn, R. and Mangel, M. (1997) The ecological detective. Princeton, NJ: Princeton University Press, 315 pp.Google Scholar
Holmer, M., Duarte, C.M., Boschker, H.T.S. and Barrón, C. (2004) Carbon cycling and bacterial carbon sources in pristine and impacted Mediterranean seagrass sediments. Marine Ecology Progress Series 36, 227–237.Google Scholar
Incze, L.S., Mayer, L.M., Sherr, E.B. and Makco, S.A. (1982) Carbon inputs to bivalve mollusks: a comparison of two estuaries. Canadian Journal of Fisheries and Aquatic Sciences 39, 1348–1352.CrossRefGoogle Scholar
Jaschinski, S., Brepohl, D.C. and Sommer, U. (2008) Carbon sources and trophic structure in an eelgrass Zostera marina bed, based on stable isotope and fatty acid analyses. Marine Ecology Progress Series 358, 103–114.CrossRefGoogle Scholar
Kanaya, G., Takagi, S. and Kikuchi, E. (2008) Spatial dietary variations in Laternula marilina (Bivalvia) and Hediste spp. (Polychaeta) along environmental gradients in two brackish lagoons. Marine Ecology Progress Series 359, 133–144.CrossRefGoogle Scholar
Kang, C.H., Kim, J.B., Lee, K.S., Kim, J.B., Lee, P.Y. and Hong, J.S. (2003) Trophic importance of benthic microalgae to macrozoobenthos in coastal bay systems in Korea: dual stable C and N isotope analyses. Marine Ecology Progress Series 259, 79–92.CrossRefGoogle Scholar
Kang, C.K., Choy, E.J., Paik, S.K., Park, H.J., Lee, K.S. and An, S. (2007) Contributions of primary organic matter sources to macroinvertebrate production in an intertidal salt marsh (Scirpus triqueter) ecosystem. Marine Ecology Progress Series 334, 131–143.CrossRefGoogle Scholar
Kenworthy, W.J. and Thayer, G.W. (1984) Production and decomposition of the roots and rhizomes of seagrasses Zostera marina and Thalassia testudinum, in temperate and subtropical marine ecosystems. Bulletin of Marine Science 35, 364–379.Google Scholar
Lebreton, B., Richar, P., Galois, R., Radenac, G., Brahmia, A., Colli, G., Grouazel, M., André, C., Guillou, G. and Blanchard, G. (2012) Food sources used by sediment meiofauna in intertidal Zostera noltii seagrass bed: a seasonal stable isotope study. Marine Biology 159, 1537–1550.CrossRefGoogle Scholar
Leduc, D. and Probert, P.K. (2009) The effect of bacterivorous nematodes on detritus incorporation by macrofaunal detritivores: a study using stable isotope and fatty acid analyses. Journal of Experimental Marine Biology and Ecology 371, 130–139.CrossRefGoogle Scholar
Lee, S.Y., Fong, C.W. and Wu, R.S.S. (2001) The effect of structure of seagrass (Zostera japonica) canopy structure on associated fauna: a study using artificial seagrass units and sampling of natural beds. Journal of Experimental Marine Biology and Ecology 259, 23–50.CrossRefGoogle ScholarPubMed
Lee, S.Y., Lee, S.M. and Choi, C.I. (2005) Phenology and reproductive effort of two Zostera marina L. populations on the southern coast of Korea. Ocean and Polar Research 27, 67–74.Google Scholar
McCutchan, J.H., Lewis, W.M., Kendall, C. and McGrath, C.C. (2003) Variation in trophic shift for stable isotope ratios of carbon, nitogen, and sulfur. Oikos 102, 378–390.CrossRefGoogle Scholar
Minagawa, M. and Wada, E. (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.CrossRefGoogle Scholar
Montagna, P.A. (1984) In situ measurement of meiobenthic grazing rates on sediment bacteria and edaphic diatoms. Marine Ecology Progress Series 18, 119–130.CrossRefGoogle Scholar
Moore, J.W. and Semmens, B.X. (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11, 470–480.CrossRefGoogle ScholarPubMed
Olsen, Y., Fox, S.E., Teichberg, M., Otter, M. and Valiela, I. (2011) δ15N and δ13C reveal differences in carbon flow through estuarine benthic food webs in response to the relative availability of macroalgae and eelgrass. Marine Ecology Progress Series 421, 83–96.CrossRefGoogle Scholar
Ouisse, V., Riera, P., Migné, A., Leroux, C. and Davoult, D. (2012) Food web analysis in intertidal Zostera marina and Zostera noltii communities in winter and summer. Marine Biology 159, 165–175.CrossRefGoogle Scholar
Page, H.M. (1997) Importance of vascular plant and algal production to macro-invertebrate consumers in a southern California salt marsh. Estuarine, Coastal and Shelf Science 45, 823–834.CrossRefGoogle Scholar
Peterson, B.J. and Fry, B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology, Evolution, and Systematics 18, 293–320.CrossRefGoogle Scholar
Riera, P. and Richard, P. (1996) Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine bay of Marennes-Oleron. Estuarine, Coastal and Shelf Science 42, 347–360.CrossRefGoogle Scholar
Riera, P., Stal, L. and Nieuwenhuize, J. (2000) Heavy δ15N in intertidal benthic algae and invertebrates in the Scheldt Estuary (The Netherlands): effect of riverine nitrogen inputs. Estuarine, Coastal and Shelf Science 51, 365–372.CrossRefGoogle Scholar
Schaal, G., Riera, P. and Leroux, C. (2008) Trophic coupling between two adjacent benthic food webs within a man-made intertidal area: a stable isotopes evidence. Estuarine, Coastal and Shelf Science 77, 523–534.CrossRefGoogle Scholar
Shaffer, G.P. and Sullivan, M.J. (1988) Water column productivity attributable to displaced benthic diatoms in well-mixed shallow estuaries. Journal of Phycology 24, 132–140.Google Scholar
Sinenstad, C.A. and Wissmar, R.C. (1985) δ13C evidence of origins and fates of organic carbon in estuarine and nearshore food webs. Marine Ecology Progress Series 22, 141–152.CrossRefGoogle Scholar
Tenore, K.R., Cammen, L., Findlay, S.E.G. and Phillips, N. (1982) Perspectives of research on detritus: do factors controlling the availability of detritus to macroconsumers depend on its source? Journal of Marine Research 40, 473–489.Google Scholar
Tenore, K.R., Tietjen, J.H. and Lee, J.J. (1977) Effect of meiofauna on incorporation of aged eelgrass, Zostera marina, detritus by polychaete Nephthys incisa. Journal of the Fisheries Research Board of Canada 34, 563–567.CrossRefGoogle Scholar
Valentine, J.F. and Duffy, J.E. (2006) The central role of grazing in seagrass ecology. In Larkum, A.W.D., Orth, R.J. and Duarte, C.M. (eds) Seagrasses: biology, ecology and conservation. Dordrecht: Springer, pp. 463–501.Google Scholar
Vanderklift, M.A. and Ponsard, S. (2003) Sources of variation in consumer-diet delta N-15 enrichment: a meta-analysis. Oecologia 136, 169–182.CrossRefGoogle Scholar
Vander Zanden, M.J. and Rasmussen, J.B. (2001) Variation in delta N-15 and delta C-13 trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46, 2061–2066.CrossRefGoogle Scholar
Warwick, R.M. (1987) Meiofauna: their role in marine detrital systems. In Moriarty, D.J.W. and Pullin, R.S.V. (eds) Detritus and microbial ecology in aquaculture. ICLARM conference proceedings, Bellagio, Como, Italy, 26–31 August 1985. Manila, Phillipines: International Center for Living Aquatic Resources Management, pp. 282–295.Google Scholar
Widdows, J., Brinsley, M.D., Bowley, N. and Barrett, C. (1998) A benthic annular flume for in situ measurement of suspension feeding/biodeposition rates and erosion potential of intertidal cohesive sediments. Estuarine, Coastal and Shelf Science 46, 2–38.CrossRefGoogle Scholar
Williams, C.J., Jaffé, R., Anderson, W.T. and Jochem, F.J. (2009) Importance of seagrass as a carbon source for heterotrophic bacteria in a subtropical estuary (Florida Bay). Estuarine, Coastal and Shelf Science 85, 507–514.CrossRefGoogle Scholar
Zurburg, W., Smaal, A.A.D., Héral, M. and Danker, N. (1994) Seston dynamics and bivalve feeding in the Bay of Marennes-Oléron (France). Netherlands Journal of Aquatic Ecolgy 28, 459–466.CrossRefGoogle Scholar