Skip to main content

Advertisement

SpringerLink
Log in

Decreasing δ13C and δ15N values in four coastal species at different trophic levels indicate a fundamental food-web shift in the southern North and Baltic Seas between 1988 and 2016

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Marine ecosystems are exposed to increasing human pressures and climatic change worldwide. It has therefore become essential to describe ecosystem statuses with respect to multinational protection schemes, often necessitating long-term monitoring programmes. Changes in the food-web structure, which can be monitored via stable isotope measurements, represent an important descriptor of the status of marine ecosystems. We investigated long-term changes (29 years) in isotopic values (δ13C and δ15N) in four indicative organisms at different trophic levels in the southern North and Baltic Seas: bladderwrack (Fucus vesiculosus), blue mussel (Mytilus ssp.), eelpout (Zoarces viviparus), and herring gull (Larus argentatus). Time series analyses using generalised additive models revealed largely consistent declines in δ13C and δ15N throughout all trophic levels of the coastal food web at all study sites, indicating a clear change in these coastal regions from 1988 to 2016. There were no clear long-term patterns in egg biometrics for herring gulls, except for a consistent increase in eggshell thickness. The declines in stable isotope values were in line with the results of previous long-term studies of single higher-trophic-level species, which suggested that the noted changes were mainly caused by altered foraging patterns of the studied species. The current results demonstrate that declines in δ13C and δ15N have occurred throughout the whole food web, not just in particular species. We discuss the possible reasons for the decrease in stable isotope values, including decreasing eutrophication and an increase in terrestrial carbon sources.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In B. N. Petrov & F. Caski (Eds.), Proceeding of the Second International Symposium on Information Theory (pp. 267–281). Budapest: Akademiai Kiado.

    Google Scholar 

  • Almroth, E., & Skogen, M. D. (2010). A North Sea and Baltic Sea model ensemble eutrophication assessment. Ambio, 39, 59–69.

    Article  CAS  Google Scholar 

  • Amer, H. (1997). Application of multielement techniques for the fingerprinting of elemental contents in Fucus vesiculosus from the North Sea. Chemosphere, 34, 2123–2131.

    Article  CAS  Google Scholar 

  • Andersen, J. H., Carstensen, J., Conley, D. J., Dromph, K., Fleming-Lehtinen, V., Gustafsson, B. G., Josefson, A. B., Norkko, A., Villnäs, A., & Murray, C. (2015). Long-term temporal and spatial trends in eutrophication status of the Baltic Sea. Biological Reviews, 92, 135–149. https://doi.org/10.1111/brv.12221.

    Article  Google Scholar 

  • Bao, J., Sherwood, S. C., Alexander, L. V., & Evans, J. P. (2017). Future increases in extreme precipitation exceed observed scaling rates. Nature Climate Change, 7, 128–132.

    Article  Google Scholar 

  • Baretta, J. W., Ruardij, P., Vested, H. J., & Baretta-Bekker, J. G. (1994). Eutrophication modelling of the North Sea: two different approaches. Ecological Modelling, 75–76, 471–483.

    Article  Google Scholar 

  • Barrett, R. T., Nilsen, E. B., & Anker-Nilssen, T. (2012). Long-term decline in egg size of Atlantic puffins Fratercula arctica is related to changes in forage fish stocks and climate conditions. Marine Ecological Progress Series, 457, 1–10.

    Article  Google Scholar 

  • Becker, P. H. & Muñoz Cifuentes, J. (2004). Contaminants in bird eggs: recent spatial and temporal trends. Wadden Sea Ecosystem No.18: 5–25. Common Wadden Sea Secretariat, Trilateral Monitoring and Assessment Group, Wilhelmshaven, Germany. http://www.waddensea-secretariat.org/sites/default/files/downloads/wse-18-cont-eggs-01.03.05.pdf. Accessed 17 November 2017.

  • Bezzel, E., & Prinzinger, R. (1990). Ornithologie. Stuttgart: Ulmer.

    Google Scholar 

  • Brendel, C. & Deutschländer, T. (2017). Temporal development of extreme precipitation in Germany projected by EURO-CORDEX simulations. Geophysical Research Abstracts 19:EGU2017–7881. http://meetingorganizer.copernicus.org/EGU2017/EGU2017-7881.pdf. Accessed 17 November 2017.

  • Christensen, J. T., & Richardson, K. (2008). Stable isotope evidence of long-term changes in the North Sea food web structure. Marine Ecology Progress Series, 368, 1–8. https://doi.org/10.3354/meps07635.

    Article  Google Scholar 

  • Cloern, J. E. (2001). Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series, 210, 223–253. https://doi.org/10.3354/meps210223.

    Article  CAS  Google Scholar 

  • Corman, A.-M., Mendel, B., Voigt, C. C., & Garthe, S. (2015). Varying foraging patterns in response to competition? A multicolony approach in a generalist seabird. Ecology and Evolution. https://doi.org/10.1002/ece3.1884.

    Article  Google Scholar 

  • Corsolini, S., Borghesi, N., Ademollo, N., & Focardi, S. (2011). Chlorinated biphenyls and pesticides in migrating and resident seabirds from East and West Antarctica. Environment International, 37, 1329–1335. https://doi.org/10.1016/j.envint.2011.05.017.

    Article  CAS  Google Scholar 

  • Elliott, M., & Griffiths, A. H. (1986). Mercury contamination in components of an estuarine ecosystem. Water Science & Technology, 18, 161–170.

    Article  CAS  Google Scholar 

  • European Commission (2008). Marine Strategy Framework Directive 2008/56/EC. http://ec.europa.eu/environment/marine/eu-coast-and-marine-policy/marine-strategy-framework-directive/index_en.htm. Accessed 17 November 2017.

  • Farmer, R. G., & Leonard, M. L. (2011). Long-term feeding ecology of Great Black-backed Gulls (Larus marinus) in the northwest Atlantic: 110 years of feather isotope data. Canadian Journal of Zoology, 89, 125–133.

    Article  CAS  Google Scholar 

  • Fliedner, A., Rüdel, H., Jürling, H., Müller, J., Neugebauer, F., & Schröter-Kermani, C. (2012). Levels and trends of industrial chemicals (PCBs, PFCs, PBDEs) in archived herring gull eggs from German coastal regions. Environmental Sciences Europe, 24, 7. https://doi.org/10.1186/2190-4715-24-7.

    Article  Google Scholar 

  • Fox, G. A. (1976). Eggshell quality: its ecological and physiological significance in a DDE-contaminated Common Tern population. Wilson Bulletin, 88, 459–477.

    Google Scholar 

  • Fry, B. (2006). Stable isotope ecology. New York: Springer.

    Book  Google Scholar 

  • Furness, R. W., & Camphuysen, C. J. (1997). Seabirds as monitors of the marine environment. ICES Journal of Marine Science, 54, 726–737.

    Article  Google Scholar 

  • Furness, R. W., & Monaghan, P. (1987). Seabird ecology. New York: Chapman & Hall.

    Google Scholar 

  • Green, N., Bjerkeng, B., Hylland, K., Ruus, A., & Rygg, B. (2003). Hazardous substances in the European marine environment: trends in metals and persistent organic pollutants (pp. 6–60). Copenhagen: European Environment Agency.

    Google Scholar 

  • Inger, R., & Bearhop, S. (2008). Applications of stable isotope analyses to avian ecology. Ibis, 150, 447–461.

    Article  Google Scholar 

  • Isaksson, N., Evans, N. J., Shamoun-Baranes, J., & Åkesson, S. (2016). Land or sea? Foraging area choice during breeding by an omnivorous gull. Movement Ecology. https://doi.org/10.1186/s40462-016-0078-5.

  • Jennings, S., & van der Molen, J. (2015). Trophic levels of marine consumers from nitrogen stable isotope analysis: estimation and uncertainty. ICES Journal of Marine Science, 72(8), 2289–2300. https://doi.org/10.1093/icesjms/fsv120.

    Article  Google Scholar 

  • Keeling, C. D. (1979). The Suess effect: 13Carbon−14Carbon interactions. Environment International, 2, 229–300.

    Article  CAS  Google Scholar 

  • Klein, R., Bartel, M., Paulus, M., Quack, M., Tarricone, K., Teubner, D., Wagner, G. (2010). Guideline for sampling and sample treatment—eelpout (Zoarces viviparus). German Federal Environmental Agency. https://www.umweltprobenbank.de/en/documents/publications/14526 Accessed 17 November 2017.

  • Kubetzki, U., & Garthe, S. (2003). Distribution, diet and habitat selection by four sympatrical gull species in the southeastern North Sea. Marine Biology, 143, 199–207.

    Article  Google Scholar 

  • Layman, C. A., Araujo, M. S., Boucek, R., Hammerschlag-Peyer, C. M., Harrison, E., Jud, Z. R., et al. (2012). Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews of the Cambridge Philosophical Society, 87, 545–562.

    Article  Google Scholar 

  • Lefebvre, A., Guiselin, N., Barbet, F., & Artigas, F. L. (2011). Long-term hydrological and phytoplankton monitoring (1992–2007) of three potentially eutrophic systems in the eastern English Channel and the Southern Bight of the North Sea. ICES Journal of Marine Science, 68, 2029–2043. https://doi.org/10.1093/icesjms/fsr149.

    Article  Google Scholar 

  • Lindenmayer, D. B., Likens, G. E., Andersen, A., Bowman, D., Bull, C. M., Burns, E., Dickman, C.R., Hoffmann, A. A., Keith, D. A., Liddell, M. J., Lowe, A. J., Metcalfe, D. J., Phinn, S. R., Russell-Smith, J., Thurgate, N., & Wardle, G. M. (2012). Value of long-term ecological studies. Austral Ecology, 37(7), 745–757. https://doi.org/10.1111/j.1442-9993.2011.02351.x.

    Article  Google Scholar 

  • Likens, G. E. (Ed.). (1989). Long-term studies in ecology: Approaches and alternatives. New York: Springer.

    Google Scholar 

  • MacKenzie, K. M., Longmore, C., Preece, C., Lucas, C. H., & Trueman, C. N. (2014). Testing the long-term stability of marine isoscapes in shelf seas using jellyfish tissues. Biogeochemistry, 121, 441–454.

    Article  Google Scholar 

  • Magurran, A. E., Baillie, S. R., Buckland, S. T., Dick, J. M., Elston, D. A., Scott, E. M., Smith, R. I., Somerfield, P. J., & Watt, A. D. (2010). Long-term datasets in biodiversity research and monitoring: assessing change in ecological communities through time. Trends in Ecology and Evolution, 25, 574–582.

    Article  Google Scholar 

  • McClelland, J. W., Valiela, I., & Michener, R. H. (1997). Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnology and Oceanography, 42, 930–937.

    Article  CAS  Google Scholar 

  • McGowan, J. A. (1990). Climate and change in oceanic ecosystems: the value of time-series data. Trends in Ecology and Evolution, 5, 293–299.

    Article  CAS  Google Scholar 

  • Michener, R., & Kaufman, L. (2008). Stable isotope ratios as tracers in marine food webs: an update. In R. Michener & K. Lajtha (Eds.), Stable isotopes in ecology and environmental science (pp. 238–282). New York: Blackwell.

    Google Scholar 

  • Paulus, M., Bartel, M., Klein, R., Quack, M., Tarricone, K., Teubner, D., Wagner, G. (2010). Guideline for sampling and sample treatment—herring gull (Larus argentatus). German Federal Environmental Agency. https://www.umweltprobenbank.de/en/documents/publications/11893 Accessed 17 November 2017.

  • Phelps, J. J. C. (2015). Modelling large-scale CO2 leakages in the North Sea. International Journal of Greenhouse Gas Control, 38, 210–220.

    Article  CAS  Google Scholar 

  • Pierotti, R., & Annett, C. (1991). Diet choice in the herring gull: constraints imposed by reproductive and ecological factors. Ecology, 72, 319–328.

    Article  Google Scholar 

  • Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83, 703–718.

    Article  Google Scholar 

  • Quack, M., Bartel-Steinbach, T., Klein, R., Paulus, M., Tarricone, K., Teubner, D., Wagner, G. (2010). Richtlinie zur Probenahme und Probenbearbeitung - Blasentang (Fucus vesiculosus). German Federal Environment Agency. https://www.umweltprobenbank.de/en/documents/publications/20550 Accessed 17 November 2017.

  • Quay, P., Sonnerup, R., Stutsman, J., Maurer, J., Körtzinger, J., Padin, X. A., & Robinson, C. (2007). Anthropogenic CO2 accumulation rates in the North Atlantic Ocean from changes in the 13C/12C of dissolved inorganic carbon. Global Biogeochemical Cycles, 21, GB1009. https://doi.org/10.1029/2006GB002761.

    Article  CAS  Google Scholar 

  • Ratcliffe, D. A. (1967). Decrease in eggshell weight in certain birds of prey. Nature, 215, 208–210.

    Article  CAS  Google Scholar 

  • Ratcliffe, D. A. (1970). Changes attributable to pesticides in egg breakage frequency and eggshell thickness in some British birds. Journal of Applied Ecology, 7, 67–115.

    Article  Google Scholar 

  • Rüdel, H., Lepper, P., Steinhanses, J., & Schröter-Kermani, C. (2003). Retrospective monitoring of organotin compounds in marine biota from 1985 to 1999. Results from the German Environmental Specimen Bank. Environment Science & Technology, 37, 1731–1738.

    Article  CAS  Google Scholar 

  • Rüdel, H., Uhlig, S., Weingärtner, M. (2009). Guidelines for sampling and sample processing: pulverisation and homogenisation of environmental samples by cryomilling. German Federal Environment Agency. https://www.umweltprobenbank.de/en/documents/publications/11939 Accessed 17 November 2017.

  • Schuster, U., Watson, A. J., Bates, N. R., Corbiere, A., Gonzales-Davila, M., Metzl, N., Pierrot, D., & Santana-Casiano, M. (2009). Trends in North Atlantic sea-surface CO2 from 1990 to 2006. Deep-Sea Research II, 23. https://doi.org/10.1016/j.dsr2.2008.12.011.

    Article  CAS  Google Scholar 

  • Schwemmer, P., & Garthe, S. (2008). Regular habitat switch as an important feeding strategy of an opportunistic seabird species at the interface between land and sea. Estuarine Coastal Shelf Science, 77, 12–22.

    Article  Google Scholar 

  • Southward, A. J., Langmead, O., Hardman-Mountford, N. J., Aiken, J., Boalch, G. T., Dando, P., et al. (2005). Long-term oceanographic and ecological research in the Western English Channel. Advances in Marine Biology, 47, 1–105.

    Google Scholar 

  • Stevenson, I. R., & Bryant, D. M. (2000). Climate change and constraints on breeding. Nature, 406, 366–367.

    Article  CAS  Google Scholar 

  • Suess, H. E. (1955). Radiocarbon concentration in modern wood. Science, 122(3166), 415–417.

    Article  CAS  Google Scholar 

  • Thompson, D. R., Furness, R. W., & Lewis, S. A. (1995). Diets and long-term changes in δ15N and δ13C values in northern fulmars Fulmarus glacialis from two northeast Atlantic colonies. Marine Ecological Progress Series, 125, 3–11.

    Article  CAS  Google Scholar 

  • Tomassini, L., & Jacob, D. (2009). Spatial analysis of trends in extreme precipitation events in high-resolution climate model results and observations for Germany. Journal of Geophysical Research, 114, D12113. https://doi.org/10.1029/2008JD010652.

    Article  Google Scholar 

  • van Beusekom, J., Bot, P., Göbel, J., Hanslik, M., Lenhart, H.J., Pätsch, J. et al. (2005). Eutrophication. In: K. Essink, C. Dettmann, H. Farke, K. Laursen, G. Lüerßen, H. Marencic, W. Wiersinga (Eds.), Wadden Sea Quality Status Report 2004. Wadden Sea Ecosystem No. 19. Trilateral Monitoring and Assessment Group, Common Wadden Sea Secretariat, Wilhelmshaven, Germany. http://www.waddensea-secretariat.org/sites/default/files/downloads/1_pdfsam_qsr2004.pdf Accessed 17 November 2017.

  • Van der Zanden, M. J., & Rasmussen, J. B. (1999). Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology, 80, 1395–1404.

    Article  Google Scholar 

  • Vander Pol, S. S., & Becker, P. R. (2007). Monitoring contaminants in seabirds: the importance of specimen banking. Marine Ornithology, 35, 113–118.

    Google Scholar 

  • Wagner, G., Bartel, M., Klein, R., Paulus, M., Quack, M., Tarricone, K., Teubner, D. (2011). Richtlinie zur Probenahme und Probenbearbeitung - Miesmuschel (Mytilus edulis). German Federal Environmental Agency. https://www.umweltprobenbank.de/en/documents/publications/20492 Accessed at 17 November 2017.

  • Winde, V., Böttcher, M. E., Voss, M., & Mahler, A. (2017). Bladder wrack (Fucus vesiculosus) as a multi-isotope bio-monitor in an urbanized fjord of the western Baltic Sea. Isotopes in Environmental and Health Studies, 53, 563–579.

    Article  CAS  Google Scholar 

  • Wood, S. N. (2006). Generalized additive models: an introduction with R. London: Chapman and Hall.

    Book  Google Scholar 

Download references

Acknowledgements

S. Furness provided language support.

Funding

This study was funded by the German Federal Environmental Agency (UBA).

Author information

Authors and Affiliations

  1. Research & Technology Centre (FTZ), Kiel University, Hafentörn 1, 25761, Büsum, Germany

    Anna-Marie Corman, Philipp Schwemmer & Stefan Garthe

  2. BIONUM Büro für Biostatistik, Finkenwerder Norderdeich 15 A, 21129, Hamburg, Germany

    Moritz Mercker

  3. Alfred Wegener Institute, Hafenstraße 43, 25992, List/Sylt, Germany

    Harald Asmus

  4. Fraunhofer Institute for Molecular Biology and Applied Ecology IME, Auf dem Aberg 1, 57392, Schmallenberg, Germany

    Heinz Rüdel

  5. Insitute of Biogeography, University of Trier, Universitätsring 15, 54286, Trier, Germany

    Roland Klein

  6. Agroisolab GmbH, Prof.-Rehm-Str. 6, 52428, Jülich, Germany

    Markus Boner & Sabine Hofem

  7. Federal Environmental Agency, Bismarckplatz 1, 14193, Berlin, Germany

    Jan Koschorreck

Authors
  1. Anna-Marie Corman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philipp Schwemmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Moritz Mercker
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Harald Asmus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Heinz Rüdel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Roland Klein
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Markus Boner
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sabine Hofem
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jan Koschorreck
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Stefan Garthe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philipp Schwemmer.

Electronic supplementary material

ESM 1

(DOCX 28 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Corman, AM., Schwemmer, P., Mercker, M. et al. Decreasing δ13C and δ15N values in four coastal species at different trophic levels indicate a fundamental food-web shift in the southern North and Baltic Seas between 1988 and 2016. Environ Monit Assess 190, 461 (2018). https://doi.org/10.1007/s10661-018-6827-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-018-6827-8

Keywords

Search

Navigation