Abstract
The mixing pattern along a summer salinity gradient in the estuary Odense Fjord was evaluated using nutrient concentrations as well as 13C and 15N isotope signatures of suspended and sediment organic matter, immobile macrophytes (Fucus vesiculosus and Ruppia maritima), and benthic fauna (Mya arenaria, Hediste (Nereis) diversicolor, and Arenicola marina). Trophic discrimination (Δ13C and Δ15N) of the infaunal consumers (suspension feeders and detritivores) was assessed from the obtained mixing patterns along the estuarine gradient. Correspondence between salinity, DIC, and DIN in Odense Fjord implies conservative mixing as also evident from linear relationships between salinity and δ13C and δ15N signatures of most living organic pools. Isotope signatures of suspended organic matter (i.e., diatoms) indicate that the river to marine DIC and DIN end-members have daily/weekly δ13C and δ15N averages during summer from − 10 to 0‰ and 10–12 to 0–5‰, respectively. Stable isotope signatures of long-lived macrophytes stationary at specific locations in Odense Fjord showed δ13C levels that were about 7‰ higher than for suspended particles and 3–4‰ higher than for sediment organic matter, while no such difference was evident for δ15N. The food of invertebrate consumers (M. arenaria, H. diversicolor, and A. marina) determined from the estuarine δ13C and δ15N patterns provided the first ever reported trophic discrimination of these animals. Thus, Δ13C was 1.9, 1.6, and 1.3‰ and Δ15N was 4.4, 5.0, and 3.5‰ for the three species, respectively. Accordingly, benthic suspension and deposit feeders in Odense Fjord are largely supported by a diet consisting of benthic and pelagic microalgae, however, with a possible slight shift in diet proportions or to other food sources in the lower reaches of the estuarine gradient.
Similar content being viewed by others
References
Aberson, M.J.R., S.G. Bolam, and R.G. Hughes. 2016. The effect of sewage pollution on the feeding behaviour and diet of Hediste (Nereis diversicolor (O.F. Müller, 1776)) in three estuaries in south-east England, with implications for saltmarsh erosion. Marine Pollution Bulletin 105 (1): 150–160.
Ahad, J.M.E., R.S. Ganeshram, R.G.M. Spencer, G. Uher, R.C. Upstill-Goddard, and G.L. Cowie. 2006. Evaluating the sources and fate of anthropogenic dissolved inorganic nitrogen (DIN) in two contrasting North Sea estuaries. Science of the Total Environment 372: 317–333.
Altabet, M.A. 2001. Nitrogen isotopic evidence for micronutrient control of fractional NO3 − utilization in the equatorial Pacific. Limnology and Oceanography 46 (2): 368–380.
Amt, Fyns. 2004. Vandmiljøovervågning. Kystvande 2003. Odense: Fyns Amt.
Andresen, M., and E. Kristensen. 2002. The importance of bacteria and microalgae in the diet of the deposit-feeding polychaete Arenicola marina. Ophelia 56 (3): 179–196.
Antonio, E.S., A. Kasai, M. Ueno, Y. Ishihi, H. Yokoyama, and Y. Yamashita. 2012. Spatial-temporal feeding dynamics of benthic communities in an estuary-marine gradient. Estuarine, Coastal and Shelf Science 112: 86–97.
Baeta, A., R. Pinto, I. Valiela, P. Richard, N. Niquil, and J.C. Marques. 2009. δ15N and δ13C in the Mondego estuary food web: Seasonal variation in producers and consumers. Marine Environmental Research 67 (3): 109–116.
Bannon, R.O., and C.T. Roman. 2008. Using stable isotopes to monitor anthropogenic nitrogen inputs to estuaries. Ecological Applications 18 (1): 22–30.
Bergamino, L., and N.B. Richoux. 2015. Spatial and temporal changes in estuarine food web structure: Differential contributions of marsh grass detritus. Estuaries and Coasts 38 (1): 367–382.
Boller, A.J., P.J. Thomas, C.M. Cavanaugh, and K.M. Scott. 2015. Isotopic discrimination and kinetic parameters of RubisCO from the marine bloom-forming diatom, Skeletonema costatum. Geobiology 13 (1): 33–43.
Bristow, L.A., T.D. Jickells, K. Weston, A. Marca-Bell, R. Parker, and J.E. Andrews. 2013. Tracing estuarine organic matter sources into the southern North Sea using C and N isotopic signatures. Biogeochemistry 113 (1-3): 9–22.
Bui, T.H.H., and S.Y. Lee. 2014. Does ‘you are what you eat’ apply to mangrove grapsid crabs? PLoS One 9 (2): e89074. https://doi.org/10.1371/journal.pone.0089074.
Bunn, S.E., N.R. Loneragan, and M.A. Kempster. 1995. Effects of acid washing on stable-isotope ratios of C and N in penaeid shrimp and seagrass - implications for food-web studies using multiple stable isotopes. Limnology and Oceanography 40 (3): 622–625.
Burkhardt, S., U. Riebesell, and I. Zondervan. 1999. Effects of growth rate, CO2 concentration, and cell size on the stable carbon isotope fractionation in marine phytoplankton. Geochimica et Cosmochimica Acta 63 (22): 3729–3741.
Cahill, A.G., R. Jakobsen, T.B. Mathiesen, and C.K. Jensen. 2013. Risks attributable to water quality changes in shallow potable aquifers from geological carbon sequestration leakage into sediments of variable carbonate content. International Journal of Greenhouse Gas Control 19: 117–125.
Carlier, A., P. Riera, J.-M. Amouroux, J.-Y. Bodiou, and A. Grémare. 2007. Benthic trophic network in the Bay of Banyuls-sur-Mer (northwest Mediterranean, France): An assessment based on stable carbon and nitrogen isotopes analysis. Estuarine, Coastal and Shelf Science 72 (1-2): 1–15.
Caut, S., E. Angulo, and F. Courchamp. 2009. Variation in discrimination factors (δ15N and δ13C): The effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46 (2): 443–453.
Choi, W.-J., J.-H. Kwak, S.-S. Lim, H.-J. Park, S.X. Chang, S.-M. Lee, M.A. Arshad, S.-I. Yun, and H.-Y. Kim. 2017. Synthetic fertilizer and livestock manure differently affect δ15N in the agricultural landscape: A review. Agriculture, Ecosystems and Environment 237: 1–15.
Choy, E.J., P. Richard, K.-R. Kim, and C.-K. Kang. 2009. Quantifying the trophic base for benthic secondary production in the Nakdong River estuary of Korea using stable C and N isotopes. Journal of Experimental Marine Biology and Ecology 382 (1): 18–26.
Christensen, B., A. Vedel, and E. Kristensen. 2000. Carbon and nitrogen fluxes in sediment inhabited by suspension-feeding (Nereis diversicolor) and non-suspension-feeding (Nereis virens) polychaetes. Marine Ecology Progress Series 192: 203–217.
Christianen, M.J., J.J. Middelburg, S.J. Holthuijsen, J. Jouta, T.J. Compton, T. van der Heide, T. Piersma, J.S.S. Damste, H.W. van der Veer, S. Schouten, and H. Olff. 2017. Benthic primary producers are key to sustain the Wadden Sea food web: Stable carbon isotope analysis at landscape scale. Ecology 98 (6): 1498–1512.
Connolly, R.M., D. Gorman, J.S. Hindell, T.N. Kildea, and T.A. Schlacher. 2013. High congruence of isotope sewage signals in multiple marine taxa. Marine Pollution Bulletin 71 (1-2): 152–158.
Deegan, L.A., and R.H. Garritt. 1997. Evidence for spatial variability in estuarine food webs. Marine Ecology Progress Series 147: 31–47.
Delefosse, M., G.T. Banta, P. Canal-Vergés, G. Penha-Lopes, C.O. Quintana, T. Valdemarsen, and E. Kristensen. 2012. Macrobenthic community response to the Marenzelleria viridis (Polychaeta) invasion of a Danish estuary. Marine Ecology Progress Series 461: 83–94.
DeNiro, M.J., and S. Epstein. 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochinica Acta 45 (3): 341–351.
Deutsch, B., and M. Voss. 2006. Anthropogenic nitrogen input traced by means of δ15N values in macroalgae: Results from in-situ incubation experiments. Science of the Total Environment 366 (2-3): 799–808.
Dias, E., P. Morais, A.M. Cotter, C. Antunes, and J.C. Hoffman. 2016. Estuarine consumers utilize marine, estuarine and terrestrial organic matter and provide connectivity among these food webs. Marine Ecology Progress Series 554: 21–34.
Doctor, D.H., C. Kendall, S.D. Sebestyen, J.B. Shanley, N. Ohte, and E.W. Boyer. 2008. Carbon isotope fractionation of dissolved inorganic carbon (DIC) due to outgassing of carbon dioxide from a headwater stream. Hydrological Processes 22 (14): 2410–2423.
Elsdon, T.S., and S.D. Connell. 2009. Spatial and temporal monitoring of coastal water quality: Refining the way we consider, gather, and interpret patterns. Aquatic Biology 5: 157–166.
France, R.L. 1995. Carbon-13 enrichment in benthic compared to planktonic algae: Foodweb implications. Marine Ecology Progress Series 124: 307–312.
Fry, B. 2002. Conservative mixing of stable isotopes across estuarine salinity gradients: A conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries 25 (2): 264–271.
Galván, K., J.W. Fleeger, and B. Fry. 2008. Stable isotope addition reveals dietary importance of phytoplankton and microphytobenthos to saltmarsh infauna. Marine Ecology Progress Series 359: 37–49.
Gaudron, S.M., K. Grangeré, and S. Lefebvre. 2016. The comparison of δ13C values of a deposit- and a suspension-feeder bio-indicates benthic vs. pelagic couplings and trophic status in contrasted coastal ecosystems. Estuaries and Coasts 39 (3): 731–741.
Hall, P.O.J., and R.C. Aller. 1992. Rapid, small-volume, flow injection analysis for ∑CO2 and NH4 + in marine and freshwaters. Limnology and Oceanography 37 (5): 1113–1119.
Hall, S.J., S.R. Weintraub, and D.R. Bowling. 2016. Scale-dependent linkages between nitrate isotopes and denitrification in surface soils: Implications for isotope measurements and models. Oecologia 181 (4): 1221–1231.
Hansman, R.L., and A.L. Sessions. 2016. Measuring the in situ carbon isotopic composition of distinct marine plankton populations sorted by flow cytometry. Limnology and Oceanography: Methods 14: 87–99.
Hemminga, M.A., and M.A. Mateo. 1996. Stable carbon isotopes in seagrasses: Variability in ratios and use in ecological studies. Marine Ecology Progress Series 140: 285–298.
Hoeinghaus, D.J., J.P. Vieira, C.S. Costa, C.E. Bemvenuti, K.O. Winemiller, and A.M. Garcia. 2011. Estuary hydrogeomorphology affects carbon sources supporting aquatic consumers within and among ecological guilds. Hydrobiologia 673 (1): 79–92.
Jarvie, H.P., C. Neal, D.V. Leach, G.P. Ryland, W.A. House, and A.J. Robson. 1997. Major ion concentrations and the inorganic carbon chemistry of the Humber rivers. Science of the Total Environment 194 (195): 285–302.
de Jonge, V.N., and F. Colijn. 1994. Dynamics of microphytobenthos biomass in the Ems estuary. Marine Ecology Progress Series 104: 185–196.
Kanaya, G., S. Takagi, E. Nobata, and E. Kikuchi. 2007. Spatial dietary shift of macrozoobenthos in a brackish lagoon revealed by carbon and nitrogen stable isotope ratios. Marine Ecology Progress Series 345: 117–127.
Koed, A., G. Rasmussen, and E.B. Rasmussen. 1997. Havørredbestandene i Odense Å og Stavids Å systemerne i relation til Fynsværket. DFU-Rapport 29–97.
Kopecky, A.L., and K.H. Dunton. 2006. Variability in drift macroalgal abundance in relation to biotic and abiotic factors in two seagrass dominated estuaries in the western Gulf of Mexico. Estuaries and Coasts 29 (4): 617–629.
Kristensen, E., M. Delefosse, C.O. Quintana, G.T. Banta, H.C. Petersen, and B. Jørgensen. 2013. Distribution patterns of benthic invertebrates in Danish estuaries; the use of Taylor's power law as an indicator of interactions and behavior. Journal of Sea Research 77: 70–78.
Kristensen, E., S.Y. Lee, P. Mangion, C.O. Quintana, and T. Valdemarsen. 2017. Trophic discrimination of stable isotopes and potential food source partitioning by leaf-eating crabs in mangrove environments. Limnology and Oceanography 62 (5): 2097–2112.
Lautenschlager, A.D., T.G. Matthews, and G.P. Quinn. 2014. Utilization of organic matter by invertebrates along an estuarine gradient in an intermittently open estuary. Estuarine, Coastal and Shelf Science 149: 232–243.
Laws, E.A., B.N. Popp, R.R. Bidigare, M.C. Kennicutt, and S.A. Macko. 1995. Dependence of phytoplankton carbon isotopic composition on growth rate and [CO2]aq: Theoretical considerations and experimental results. Geochimica et Cosmochimica Acta 59 (6): 1131–1138.
Lions, J., P. Humez, H. Pauwels, W. Kloppmann, and I. Czernichowski-Lauriol. 2014. Tracking leakage from a natural CO2 reservoir (Montmiral, France) through the chemistry and isotope signatures of shallow groundwater. Greenhouse Gases: Science and Technology 4 (2): 225–243.
Marconi, M., M. Giordano, and J.A. Raven. 2011. Impact of taxonomy, geography, and depth on δ13C and δ15N variation in a large collection of macroalgae. Journal of Phycology 47 (5): 1023–1035.
Mariotti, A., J.C. Germon, P. Hubert, P. Kaiser, R. Letolle, A. Tardieux, and P. Tardieux. 1981. Experimental determination of nitrogen kinetic isotope fractionation: Some principles; illustration for the denitrification and nitrification processes. Plant and Soil 62 (3): 413–430.
McClanahan, K., J. Polk, C. Groves, L. Osterhoudt, and S. Grubbs. 2016. Dissolved inorganic carbon sourcing using δ13CDIC from a karst influenced river system. Earth Surface Processes and Landforms 41 (3): 392–405.
McClelland, J.W., and I. Valiela. 1998. Linking nitrogen in estuarine producers to land-derived sources. Limnology and Oceanography 43 (4): 577–585.
McCutchan, J.H., W.M. Lewis, C. Kendall, and C.C. McGrath. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102 (2): 378–390.
McPherson, M.L., R.C. Zimmerman, and V.J. Hill. 2015. Predicting carbon isotope discrimination in eelgrass (Zostera marina L.) from the environmental parameters—light, flow, and [DIC]. Limnology and Oceanography 60 (6): 1875–1889.
Michener, R.H., and D.M. Schell. 1994. Stable isotope ratios as tracers in marine aquatic food webs. In Stable isotopes in ecology and environmental science, ed. K. Lajtha and R.H. Michener, 138–157. Oxford: Blackwell.
Moore, S.K., and I.M. Suthers. 2005. Can the nitrogen and carbon stable isotopes of the pygmy mussel, Xenostrobus securis, indicate catchment disturbance for estuaries in northern New South Wales, Australia? Estuaries 28 (5): 714–725.
Morris, E.P., G. Peralta, J. Benavente, R. Freitas, A.M. Rodrigues, V. Quintino, O. Alvarez, N. Valcárcel-Pérez, J.J. Vergara, I. Hernández, and J.L. Pérez-Lloréns. 2009. Caulerpa prolifera stable isotope ratios reveal anthropogenic nutrients within a tidal lagoon. Marine Ecology Progress Series 390: 117–128.
Naithani, J., B. de Brye, E. Buyze, W. Vyverman, V. Legat, and E. Deleersnijder. 2016. An ecological model for the Scheldt estuary and tidal rivers ecosystem: Spatial and temporal variability of plankton. Hydrobiologia 775 (1): 51–67.
Needoba, J.A., N.A. Waser, P.J. Harrison, and S.E. Calvert. 2003. Nitrogen isotope fractionation in 12 species of marine phytoplankton during growth on nitrate. Marine Ecology Progress Series 255: 81–91.
Nithart, M. 2000. Comparison of stable carbon and nitrogen isotope signatures of the polychaete Nereis diversicolor from different estuarine sites. Journal of the Marine Biological Association of the UK 80 (4): 763–765.
Olsen, Y.S., S.E. Fox, M. Teichberg, M. Otter, and I. Valiela. 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.
Orlandi, L., E. Calizza, G. Careddua, P. Carlino, M.L. Costantini, and L. Rossi. 2017. The effects of nitrogen pollutants on the isotopic signal (δ15N) of Ulva lactuca: Microcosm experiments. Marine Pollution Bulletin 115 (1-2): 429–435.
Oxtoby, L.E., J.T. Mathis, L.W. Juranek, and M.J. Wooller. 2016. Estimating stable carbon isotope values of microphytobenthos in the Arctic for application to food web studies. Polar Biology 39 (3): 473–483.
Petersen, J.D., N. Rask, H.B. Madsen, O.T. Jørgensen, S.E. Petersen, S.V.K. Nielsen, C.B. Pedersen, and M.H. Jensen. 2009. Odense Pilot River Basin: Implementation of the EU Water Framework Directive in a shallow eutrophic estuary (Odense Fjord, Denmark) and its upstream catchment. Hydrobiologia 629 (1): 71–89.
Pitt, K.A., R.M. Connolly, and P. Maxwell. 2009. Redistribution of sewage-nitrogen in estuarine food webs following sewage treatment upgrades. Marine Pollution Bulletin 58 (4): 573–580.
Raven, J.A., D.I. Walker, A.M. Johnston, L.L. Handley, and J.E. Kübler. 1995. Implications of 13C natural abundance measurements for photosynthetic performance by marine macrophytes in their natural environment. Marine Ecology Progress Series 123: 193–205.
Riisgård, H.U. 1991. Suspension feeding in the polychaete Nereis diversicolor. Marine Ecology Progress Series 70: 29–37.
Riisgård, H.U., M.H. Jensen, and N. Rask. 2008. Odense Fjord and Kerteminde Fjord/Kertinge Nor. In Ecology of Baltic Coastal Waters, Ecological Studies 197, ed. U. Schiewer. Berlin: Springer-Verlag.
Sarà, G. 2007. Sedimentary and particulate organic matter: Mixed sources for cockle Cerastoderma glaucum in a shallow pond, Western Mediterranean. Aquatic Living Resources 20 (3): 271–277.
Smith, P.E., J.M. Oakes, and B.D. Eyre. 2016. Recovery of nitrogen stable isotope signatures in the food web of an intermittently open estuary following removal of wastewater loads. Estuarine, Coastal and Shelf Science 182: 170–178.
Strasser, M. 1999. Mya arenaria—an ancient invader of the North Sea coast. Helgoländer Meeresuntersuchungen 52: 309–324.
Sugimoto, R., and A. Kasai. 2016. Key biogeochemical processes evaluated by the stable nitrogen isotopes of dissolved inorganic nitrogen in the Yodo River estuary, Japan: Significance of estuarine nutrient recycling as a possible source for coastal production. Biogeochemistry 128 (1-2): 1–17.
Taupp, T., C. Hellmann, R. Gergs, C. Winkelmann, and M.A. Wetzel. 2017. Life under exceptional conditions—isotopic niches of benthic invertebrates in the estuarine maximum turbidity zone. Estuaries and Coasts 40 (2): 502–512.
Teichberg, M., S.E. Fox, C. Aguila, Y.S. Olsen, and I. Valiela. 2008. Macroalgal responses to experimental nutrient enrichment in shallow coastal waters: Growth, internal nutrient pools, and isotopic signatures. Marine Ecology Progress Series 368: 117–126.
Vadeboncoeur, M.A., S.P. Hamburg, and D. Pryor. 2010. Modeled nitrogen loading to Narragansett Bay: 1850 to 2015. Estuaries and Coasts 33 (5): 1113–1127.
Valdemarsen, T., C.O. Quintana, E. Kristensen, and M.R. Flindt. 2014. Recovery of organic-enriched sediments through microbial degradation: Implications for eutrophic estuaries. Marine Ecology Progress Series 503: 41–58.
Vander Zanden, M.J., and J.B. Rasmussen. 2001. Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnology and Oceanography 46 (8): 2061–2066.
Vermaat, J.E., S. Broekx, B. van Eck, G. Engelen, F. Hellmann, J.L. de Kok, H. van der Kwast, J. Maes, W. Salomons, and W. van Deursen. 2012. Nitrogen source apportionment for the catchment, estuary, and adjacent coastal waters of the River Scheldt. Ecology and Society 17: 30. https://doi.org/10.5751/ES-04889-170230.
Viana, I.G., and A. Bode. 2015. Variability in δ15N of intertidal brown algae along a salinity gradient: Differential impact of nitrogen sources. Science of the Total Environment 512–513: 167–176.
White, D.L., D.E. Porter, and A.J. Lewitus. 2004. Spatial and temporal analyses of water quality and phytoplankton biomass in an urbanized versus a relatively pristine salt marsh estuary. Journal of Experimental Marine Biology and Ecology 298 (2): 255–273.
Winde, V., M.E. Böttcher, P. Escher, P. Böning, M. Beck, G. Liebezeit, and B. Schneider. 2014. Tidal and spatial variations of DI13C and aquatic chemistry in a temperate tidal basin during winter time. Journal of Marine Systems 129: 396–404.
Acknowledgements
We are grateful to Birthe Christensen, Katrine C. Kirkegaard, and Rikke O. Holm for the support with laboratory analyses. This work was supported by grant no. 12-132701 from The Danish Council for Strategic Research and grant no. 12-127012 from the Danish Council for Independent Research/Natural Sciences.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Ken Dunton
Rights and permissions
About this article
Cite this article
Kristensen, E., Quintana, C.O. & Valdemarsen, T. Stable C and N Isotope Composition of Primary Producers and Consumers Along an Estuarine Salinity Gradient: Tracing Mixing Patterns and Trophic Discrimination. Estuaries and Coasts 42, 144–156 (2019). https://doi.org/10.1007/s12237-018-0460-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12237-018-0460-1