Skip to main content

Advertisement

Log in

Inter- and intraspecific variation of carbon and nitrogen stable isotope ratios in freshwater bivalves

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Freshwater bivalves provide important ecosystem functions and services, yet many of their ecological traits such as feeding mechanisms and resource use are largely ignored. In this study, we aimed to evaluate the potential overlap in resource use by bivalve species living in sympatry in European freshwater ecosystems. This was accomplished by analyzing the stable isotope ratios of carbon (C) and nitrogen (N) values of six bivalve species (five native species plus the invasive species Corbicula fluminea) in six distinct aquatic ecosystems. Results showed significant inter- and intraspecific differences in both stable isotope ratios. The interspecific variability suggests differences in the food sources consumed, which can be related to differences in feeding behavior. At the intraspecific level, there was a gradient in the stable isotope ratios from the oligotrophic River Paiva (15N-depleted and 13C-enriched) to the eutrophic Mira Lagoon (15N-enriched and 13C-depleted), suggesting a change in the resources used from benthic to pelagic food sources, respectively, and/or differences in the stable isotopic baseline in each ecosystem. Thus, flexible feeding strategies combined with size selectivity may decrease the possible competition for food sources by native and invasive species living in sympatry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.

    Google Scholar 

  • Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth.

    Google Scholar 

  • Angradi, T. R., 1994. Trophic linkages in the lower Colorado River: multiple stable isotope evidence. Journal of the North American Benthological Society 13: 479–495.

    Article  Google Scholar 

  • Atkinson, C. L., S. W. Golladay, S. P. Opsahl & A. P. Covich, 2009. Stream discharge and floodplain connections affect seston quality and stable isotopic signatures in a coastal plain stream. Journal of the North American Benthological Society 28: 360–370.

    Article  Google Scholar 

  • Atkinson, C. L., S. P. Opsahl, A. P. Covich, S. W. Golladay & L. M. Conner, 2010. Stable isotopic signatures, tissue stoichiometry, and nutrient cycling (C and N) of native and invasive freshwater bivalves. Journal of the North American Benthological Society 29: 496–505.

    Article  Google Scholar 

  • Atkinson, C. L., M. R. First, A. P. Covich, S. P. Opsahl & S. W. Golladay, 2011. Suspended material availability and filtration-biodeposition processes performed by a native and invasive bivalve species in streams. Hydrobiologia 667: 191–204.

    Article  CAS  Google Scholar 

  • Atkinson, C. L., A. D. Christian, D. E. Spooner & C. C. Vaughn, 2014. Long-lived organisms provide an integrative footprint of agricultural land use. Ecological Applications 24: 375–384.

    Article  PubMed  Google Scholar 

  • Boltovskoy, D., I. Izaguirre & N. Correa, 1995. Feeding selectivity of Corbicula fluminea (Bivalvia) on natural phytoplankton. Hydrobiologia 312: 171–182.

    Article  Google Scholar 

  • Cabana, G. & J. B. Rasmussen, 1996. Comparison of aquatic food chains using nitrogen isotopes. Proceedings of the National Academy of Sciences 93: 10844–10847.

    Article  CAS  Google Scholar 

  • Clarke, K. R. & R. M. Warwick, 2001. Change in marine communities: an approach to statistical analysis and interpretation. Plymouth Marine Laboratory, Plymouth.

    Google Scholar 

  • Cloern, J. E., E. A. Canuel & D. Harris, 2002. Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnology and Oceanography 47: 713–729.

    Article  CAS  Google Scholar 

  • Dame, R. F., 1996. Ecology of marine bivalves: an ecosystem approach. CRC, New York.

    Book  Google Scholar 

  • DeNiro, M. J. & S. Epstein, 1977. Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197: 261–263.

    Article  CAS  PubMed  Google Scholar 

  • DeNiro, M. J. & S. Epstein, 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica Cosmochimica Acta 42: 495–506.

    Article  CAS  Google Scholar 

  • Dias, E., P. Morais, C. Antunes & J. C. Hoffman, 2014. Linking terrestrial and benthic estuarine ecosystems: organic matter sources supporting the high secondary production of a non-indigenous bivalve. Biological Invasions 16: 2163–2179.

    Article  Google Scholar 

  • Dillon Jr, R. T., 2000. The ecology of freshwater mollusks. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Ferreira, J. G., T. Simas, A. Nobre, M. C. Silva, K. Schifferegger & J. Lencart-Silva, 2003. Identification of sensitive areas and vulnerable zones in transitional and coastal Portuguese systems. Application of the United States National Estuarine Eutrophication Assessment to the Minho, Lima, Douro, Ria de Aveiro, Mondego, Tagus, Sado, Mira, Ria Formosa and Guadiana systems, INAG/IMAR Technical Report.

  • Ferreiro, N., 2007. Caracterização da qualidade ecológica do rio Tua. Master thesis, University of Porto, Portugal.

  • Finlay, J. C., M. E. Power & G. Cabana, 1999. Effects of water velocity on algal carbon isotope ratios: implications for river food web studies. American Society of Limnology and Oceanography 44: 1198–1203.

    Article  Google Scholar 

  • France, R. L., 1995. Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Marine Ecology Progress Series 124: 307–312.

    Article  Google Scholar 

  • Fry, B., 1991. Stable isotope diagrams of freshwater food webs. Ecology 72: 2293–2297.

    Article  Google Scholar 

  • Galbraith, H. S., S. E. Frazier, B. Allison & C. C. Vaughn, 2009. Comparison of gill surface morphology across a guild of suspension-feeding unionid bivalves. Journal of Molluscan Studies 75: 103–107.

    Article  Google Scholar 

  • Garcia, C. M. T., 2001. Isolamento, cultura e avaliação de toxicidade de estirpes de cianobactérias da Lagoa de Mira. Master thesis, University of Porto, Portugal.

  • Goedkoop, W., N. Akerblom & M. H. Demandt, 2006. Trophic fractionation of carbon and nitrogen stable isotopes in Chironomus riparius reared on food of aquatic and terrestrial origin. Freshwater Biology 51: 878–886.

    Article  CAS  Google Scholar 

  • Hakenkamp, C. C. & M. A. Palmer, 1999. Introduced bivalves in freshwater ecosystems: the impact of Corbicula on organic matter dynamics in a sandy stream. Oecologia 119: 445–451.

    Article  Google Scholar 

  • Hoffman, J. C. & D. A. Bronk, 2006. Interannual variation in stable carbon and nitrogen isotope biogeochemistry of the Mattaponi River, Virginia. Limnology & Oceanography 51: 2319–2332.

    Article  CAS  Google Scholar 

  • Howard, J. K., K. M. Cuffey & M. Solomon, 2005. Toward using Margaritifera falcata as an indicator of base level nitrogen and carbon isotope ratios: insights from two California Coast Range rivers. Hydrobiologia 541: 229–236.

    Article  Google Scholar 

  • Kreitler, C. W. & L. A. Browning, 1983. Nitrogen-isotope analysis of groundwater nitrate and carbonate aquifers: natural sources versus human pollution. Journal of Hydrology 61: 285–301.

    Article  CAS  Google Scholar 

  • Layman, C. A., M. S. Araujo, R. Boucek, C. M. Hammerschlag-Peyer, E. Harrison, Z. R. Jud, P. Matich, A. E. Rosenblatt, J. J. Vaudo, L. A. Yeager, D. M. Post & S. Bearhop, 2012. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews 87: 545–562.

    Article  PubMed  Google Scholar 

  • Logan, J. M., T. D. Jardine, T. J. Miller, S. E. Bunn, R. A. Cunjak & M. E. Lutcavage, 2008. Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. Journal of Animal Ecology 77: 838–846.

    Article  PubMed  Google Scholar 

  • Lopes-Lima, M., A. Teixeira, E. Froufe, A. Lopes, S. Varandas & R. Sousa, 2014a. Biology and conservation of freshwater bivalves: past, present and future perspectives. Hydrobiologia 735: 1–13.

    Article  Google Scholar 

  • Lopes-Lima, M., P. Lima, M. Hinzmann, A. Rocha & J. Machado, 2014b. Selective feeding by Anodonta cygnea (Linnaeus, 1771): the effects of seasonal changes and nutritional demands. Limnologica 44: 18–22.

    Article  Google Scholar 

  • Lopez, G. R. & I. J. Holopainen, 1987. Interstitial suspension-feeding by Pisidium spp. (Pisidiidae: Bivalvia): a new guild in the lentic benthos? American Malacological Bulletin 5: 21–30.

    Google Scholar 

  • McCutchan Jr, J. H., W. M. Lewis, C. Kendall & C. C. McGrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378–390.

    Article  CAS  Google Scholar 

  • McKinney, R. A., J. L. Lake, R. A. Charpentier & S. Ryba, 2002. Using mussel isotope ratios to assess anthropogenic inputs to freshwater ecosystems. Environmental Monitoring and Assessment 74: 167–192.

    Article  CAS  PubMed  Google Scholar 

  • McNeely, C., S. M. Clinton & J. M. Erbe, 2006. Landscape variation in C sources of scraping primary consumers in streams. Journal of the North American Benthological Society 25: 787–799.

    Article  Google Scholar 

  • Minagawa, M. & E. Wada, 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica Cosmochimica Acta 48: 1135–1140.

    Article  CAS  Google Scholar 

  • Oliveira, J. M., P. Segurado, J. M. Santos, A. Teixeira, M. T. Ferreira & R. V. Cortes, 2012. Modelling stream-fish functional traits in reference conditions: regional and local environmental correlates. PLoS ONE 9: e45787.

    Article  Google Scholar 

  • Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293–320.

    Article  Google Scholar 

  • Raikow, D. F. & S. K. Hamilton, 2001. Bivalves diets in a midwestern U.S. stream: a stable isotope enrichment study. American Society of Limnology and Oceanography 46: 514–522.

    Article  Google Scholar 

  • Régnier, C., B. Fontaine & P. Bouchet, 2009. Not knowing, not recording, not listing: numerous unnoticed mollusk extinctions. Conservation Biology 23: 1214–1221.

    Article  PubMed  Google Scholar 

  • Reid, R. G. B., R. F. McMahon, D. O. Foighil & R. Finnigan, 1992. Anterior inhalant currents and pedal-feeding in bivalves. Veliger 35: 93–104.

    Google Scholar 

  • Rolston, D. E., G. E. Fogg, D. L. Decker, D. J. Louie & M. E. Grimser, 1996. Nitrogen isotope ratios identify nitrate contamination sources. California Agriculture 50: 32–36.

    Article  Google Scholar 

  • Silverman, H., E. E. Archberger, J. W. Lynn & T. H. Dietz, 1995. Filtration and utilization of laboratory-cultured bacteria by Dreissena polymorpha, Corbicula fluminea and Carunculina texasensis. Biological Bulletin 189: 308–319.

    Article  Google Scholar 

  • Silverman, H., S. J. Nichols, J. S. Cherry, E. Achberger, J. W. Lynn & T. H. Dietz, 1997. Clearance of laboratory-cultured bacteria by freshwater bivalves: differences between lentic and lotic unionids. Canadian Journal of Zoology 75: 1857–1866.

    Article  Google Scholar 

  • Sousa, R., L. Guilhermino & C. Antunes, 2005. Molluscan fauna in the freshwater tidal area of the River Minho estuary, NW of Iberian Peninsula. Annales de Limnologie—International Journal of Limnology 41: 141–147.

    Article  Google Scholar 

  • Sousa, R., C. Antunes & L. Guilhermino, 2008a. Ecology of the invasive Asian clam Corbicula fluminea (Müller, 1774) in aquatic ecosystems: an overview. Annales de Limnologie—International Journal of Limnology 44: 85–94.

    Article  Google Scholar 

  • Sousa, R., M. Rufino, M. Gaspar, C. Antunes & L. Guilhermino, 2008b. Abiotic impacts on spatial and temporal distribution of Corbicula fluminea (Müller, 1774) in the River Minho estuary, Portugal. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 98–110.

    Article  Google Scholar 

  • Sousa, R., P. Morais, C. Antunes & L. Guilhermino, 2008c. Factors affecting Pisidium amnicum (Müller, 1774; Bivalvia: Sphaeriidae) distribution in the River Minho estuary: consequences for its conservation. Estuaries and Coasts 31: 1198–1207.

    Article  Google Scholar 

  • Sousa, R., A. J. A. Nogueira, C. Antunes & L. Guilhermino, 2008d. Growth and production of Pisidium amnicum (Müller, 1774) in the freshwater tidal area of the River Minho estuary. Estuarine, Coastal and Shelf Science 79: 467–474.

    Article  Google Scholar 

  • Sousa, R., M. Ilarri, A. T. Souza, C. Antunes & L. Guilhermino, 2011. Rapid decline of the greater European peaclam at the periphery of its distribution. Annales de Limnologie—International Journal of Limnology 47: 211–219.

    Article  Google Scholar 

  • Sousa, R., S. Varandas, R. Cortes, A. Teixeira, M. Lopes-Lima, J. Machado & L. Guilhermino, 2012. Massive die-offs of freshwater bivalves as resource pulses. Annales de Limnologie—International Journal of Limnology 48: 105–112.

    Article  Google Scholar 

  • Sousa, R., A. Amorim, C. Sobral, E. Froufe, S. Varandas, A. Teixeira & M. Lopes-Lima, 2013. Ecological status of a Margaritifera margaritifera (Linnaeus, 1758) population at the southern edge of its distribution (River Paiva, Portugal). Environmental Management 52: 1230–1238.

    Article  PubMed  Google Scholar 

  • Sousa, R., A. Novais, R. Costa & D. L. Strayer, 2014. Invasive bivalves in fresh waters: impacts from individuals to ecosystems and possible control strategies. Hydrobiologia 735: 233–251.

    Article  Google Scholar 

  • Strayer, D. L., 2010. Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshwater Biology 55: 152–174.

    Article  Google Scholar 

  • Strayer, D., J. A. Downing, W. R. Haag, T. L. King, J. B. Layer, T. J. Newton & S. J. Nichols, 2004. Changing perspectives on pearly mussels, North America’s most imperiled animals. BioScience 54: 429–439.

    Article  Google Scholar 

  • Thorp, J. H., M. D. Delong, K. S. Greenwood & A. F. Casper, 1998. Isotopic analysis of three food web theories in constricted and floodplain regions of a large river. Oecologia 117: 551–563.

    Article  Google Scholar 

  • Vaughn, C. C., 2010. Biodiversity losses and ecosystem function in freshwaters: emerging conclusions and research directions. BioScience 60: 25–35.

    Article  Google Scholar 

  • Vaughn, C. C. & C. C. Hakenkamp, 2001. The functional role of burrowing bivalves in freshwater ecosystems. Freshwater Biology 46: 1431–1446.

    Article  Google Scholar 

  • Vaughn, C. C. & C. M. Taylor, 1999. Impoundments and the decline of freshwater mussels: a case study of an extinction gradient. Conservation Biology 13: 912–920.

    Article  Google Scholar 

  • Vaughn, C. C., S. J. Nichols & D. E. Spooner, 2008. Community and foodweb ecology of freshwater mussels. Journal of the North American Benthological Society 27: 409–423.

    Article  Google Scholar 

  • Way, C. M., D. J. Hornbach, T. Deneka & R. A. Whitehead, 1989. A description of the ultrastructure of the gills of freshwater bivalves, including a new structure, the frontal cirrus. Canadian Journal of Zoology 67: 357–362.

    Article  Google Scholar 

  • Way, C. M., D. J. Hornbach, C. A. Miller-Way, B. S. Payne & A. C. Miller, 1990. Dynamics of filter feeding in Corbicula fluminea (Bivalvia: Corbiculidae). Canadian Journal of Zoology 68: 115–120.

    Article  Google Scholar 

  • West, J. B., G. J. Bowen, T. E. Cerling & J. R. Ehleringer, 2006. Stable isotopes as one of nature’s ecological recorders. Trends in Ecology and Evolution 21: 408–414.

    Article  PubMed  Google Scholar 

  • Zanden, M. J. V. & J. B. Rasmussen, 1999. Primary consumer 13C and 15N and the trophic position of aquatic consumers. Ecology 80: 1395–1404.

    Article  Google Scholar 

  • Zanden, M. J. V. & J. B. Rasmussen, 2001. Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46: 2061–2066.

    Article  Google Scholar 

Download references

Acknowledgments

A. Novais was supported by a Ph.D. Grant (SFRH/BD/86463/2012) from the Portuguese Foundation for Science and Technology—FCT through POPH/FSE funds. This study was conducted in the scope of the project ECO-IAS: ecosystem-level impacts of an invasive alien species, funded by FCT and COMPETE funds (contract: PTDC/AAC-AMB/116685/2010). This study was also partially supported by the European Regional Development Fund (ERDF) through the COMPETE, under the project “PEst-C/MAR/LA0015/2011.” Special thanks are addressed to Francisco Carvalho and Ângela Amorim for help in collecting the organisms in the field, to Sofia Gonçalves for assistance in the stable isotope analyses, to Joel C. Hoffman, Beat Oertli, and two anonymous referees for valuable suggestions on an earlier version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adriana Novais.

Additional information

Handling editor: Beat Oertli

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Novais, A., Dias, E. & Sousa, R. Inter- and intraspecific variation of carbon and nitrogen stable isotope ratios in freshwater bivalves. Hydrobiologia 765, 149–158 (2016). https://doi.org/10.1007/s10750-015-2408-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2408-9

Keywords

Navigation