Abstract
Nitrification of the environment has resulted from tremendous increases in the use of fertilizers for crop plants. This has increased runoff to coastal marine areas with consequences for primary production, benthos and upper trophic-level consumers, including sea ducks such as eiders Somateria mollissima. This species primarily relies on filter-feeding bivalves, especially blue mussels Mytilus edulis. Stable isotopes of nitrogen (measured as δ15N) are incorporated in the feathers of eiders during molt at a constant rate reflecting the amount in food eaten. We examined if δ15N values in feathers can link eiders to the nitrogen loads in the marine waters surrounding Denmark, which is the main wintering grounds for the Baltic/Wadden Sea eider population. We also assessed how the abundance of eiders is related to nutrients and dead zones with oxygen deficit. During 2014–2018 we collected samples from 489 eiders, and of these 100 were analyzed for stable isotopes δ15N. Eider feather δ15N was positively related to nitrogen abundance in marine waters. Local aggregations of eiders in late summer (the molting period) and in winter increased with the amount of nitrogen in the marine environment. Large eiders took longer to molt, they molted later and the daily growth increments of feathers were larger. Finally, larger eiders and eiders in higher numbers occurred in areas with hypoxia. These findings show that anthropogenic inputs to the coastal marine environment positively influence the abundance and aggregations of eiders.
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References
Belliure J, Sorci G, Møller AP, Clobert J. 2000. Dispersal distances predict subspecies richness in birds. J Evol Biol 13:480–7.
Burger M, Jackson LE. 2003. Microbial immobilization of ammonium and nitrate in relation to nitrification rates in organic and conventional cropping systems. Soil Biol Biochem 35:29–36.
Bustnes JO, Erikstad KE, Bjørn TH. 2002. Body condition and brood abandonment in common eiders breeding in the high arctic. Waterbirds 25:63–6.
Cabana G, Rasmussen JB. 1996. Comparison of aquatic food chains using nitrogen isotopes. Proc Natl Acad Sci USA 93:10844–7.
Camargo JA, Alonso Á. 2006. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems. Environ Int 32:831–49.
Cervencl A, Troost K, Dijkman E, de Jong M, Smit CJ, Leopold MF, Ens BJ. 2014. Distribution of wintering Common Eider Somateria mollissima in the Dutch Wadden Sea in relation to available food stocks. Mar Biol 162:153–68.
Cramp S, Ed. 1977. Handbook of the birds of Europe, the Middle East and North Africa, Vol. 1Oxford, UK: Oxford University Press.
Conley DJ, Carstensen J, Ærtebjerg G, Christensen PB, Dalsgaard T, Hansen JL, Josefson AB. 2007. Long-term changes and impacts of hypoxia in Danish coastal waters. Ecol Appl 17(5 Supplement):165–84.
Diaz RJ, Rosenberg R. 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr Mar Biol Ann Rev 33:245–303.
Duus K, Zinglersen E. 2000. Geografistatistik 2000. Copenhagen (in Danish): Geografforlaget.
Ekroos J, Fox AD, Christensen TK, Petersen IK, Kilpi M, Jonsson JE, Green M, Laursen K, Cervencl A, de Boer P, Nilsson L, Meissner W, Garthe S, Öst M. 2012. Declines amongst breeding Eider Somateria mollissima numbers in the Baltic/Wadden Sea flyway. Ornis Fenn 89:81–90.
Eurostat. 2018. Consumption estimate of manufactured fertilizers. http://epp.eurostat.ec.europa.eu/tgm/table.do?tab=table&init=1&language=en&pcode=tag00090&plugin=1.
Falconer DS, Mackay TFC. 1996. Introduction to quantitative genetics. 4th edn. New York, NJ: Longman.
Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN et al. 2013. The global nitrogen cycle in the twenty-first century. Phil Trans R Soc B Biol Sci 368:20130164.
Galloway JN, Cowling EB. 2002. Reactive nitrogen and the world: 200 years of change. Ambio 31:64–71.
Grubb TC Jr. 2006. Ptilochronology. New York, NY: Oxford University Press.
Guillemette M, Himmelman JH, Barette C. 1993. Habitat selection by common eiders in winter and its interaction with flock size. Can J Zool 71:1259–66.
Hansen JW (ed.) 2016. Marine områder 2015. Scientific report from DCE: National Centre of Environment and Energy, No. 208. Department of Bioscience, Aarhus University, Aarhus, Denmark. Danish).
Helcom. 2018. State of the Baltic Sea—second HELCOM holistic assessment 2011–2016. Baltic Sea Environment Proceedings 155.
Hjort M, Josefson AB (ed.) 2010. Marine områder 2008. Technical report from DMU No. 760. Danish Environmental Research Institute, Aarhus University, Aarhus, Denmark (in Danish).
Hobson KA. 1999. Stable-carbon and nitrogen isotope ratios of songbird feathers grown in two terrestrial biomes: implications for evaluating trophic relationships and breeding origins. Condor 101:799–805.
Jaatinen K, Öst M, Hobson KA. 2016. State-dependent capital and income breeding: a novel approach to evaluating individual strategies with stable isotopes. Front Zool 13:24.
Jovani R, Rohwer S. 2017. Fault bars in bird feathers: Mechanisms, and ecological and evolutionary causes and consequences. Biol Rev 92:1113–27.
Kelly JF. 2000. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27.
Laursen K, Asferg K, Frikke J, Sunde P. 2009. Mussel fishery affects diet and reduces body condition of Eiders Somateria mollissima in the Wadden Sea. J Sea Res 62:22–30.
Laursen K, Kristensen PS, Clausen P. 2010. Assessment of blue mussels Mytilus edulis fisheries and waterbird shell-predator management in the Danish Wadden Sea. AMBIO 39:476–85.
Laursen K, Møller AP. 2014. Long-term changes in nutrients and mussel stocks are related to numbers of breeding eiders Somateria mollissima at a large Baltic Colony. PLoS One 9(4):e95851.
Laursen K, Møller AP, Holm TE. 2016. Dynamic group size and displacement as avoidance strategies by eiders in response to hunting. Wildl Biol 22:174–81.
Laursen K, Møller AP, Haugaard L, Öst M, Vainio J. 2019. Allocation of body reserves during winter in eider Somateria mollissima as preparation for spring migration and reproduction. J Sea Res 49:49–56.
Laursen K, Møller AP, Öst M. 2018. Body condition of eiders at Danish wintering grounds and at pre-breeding grounds in Åland. J Ornithol. https://doi.org/10.1007/s10336-018-1609-1.
Lehikoinen A, Kilpi M, Öst M. 2006. Winter climate affects subsequent breeding success of common eiders. Global Change Biol 12:1355–65.
McClave JT, Sincich T. 2003. Statistics. 9th edn. Englewood Cliffs, NJ: Prentice-Hall.
McCutchan JH, Lewis WM, Kendall C, McGrath CC. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–90.
Møller AP, Laursen K, Hobson KA. 2018. Retrospectively analysing condition in historical samples of birds. J Zool https://doi.org/10.1111/jzo.12551.
Nehls G, Ketzenberg CA. 2002. Do common eiders Somateria mollissima exhaust their food resources? A study on natural mussels Mytilus edulis beds in the Wadden Sea. Dan Rev Game Biol 16:47–61.
Noer H. 1991. Distributions and movements of eider Somateria mollissima populations wintering in Danish waters analysed from ringing recoveries. Dan Rev Game Biol 14:1–32.
Nielsen E, Richardson K. 1996. Can changes in the fisheries yield in the Kattegat be linked to changes in primary productions? ICES Mar Sci 53:988–94.
Öst M, Kilpi M. 1998. Blue mussels Mytilus edulis in the Baltic: good news for foraging eiders Somateria mollissima. Wildl Biol 4:81–9.
Öst M, Wickman M, Matulionis E, Steele BB. 2008. Habitat-specific clutch size and cost of incubation in eiders reconsidered. Oecologia 158:205–16.
Öst M, Steele BB. 2010. Age-specific nest site preference and success in Eider. Oecologia 162:59–69.
Pearson TH, Rosenberg R. 1978. Microbenthic succession in relation to organic enrichment and pollution of the marine environment. Mar Biol Ann Rev 16:229–311.
Petersen IK, Pihl S, Hounisen JP, Holm TE, Clausen, P, Therkildsen OR, Christensen TK. 2006. Landsdækkende optælling af vandfugle januar-februar 2004. Scientific report from DMU nr. 606, Danish Environmental Institute, Aarhus University, Denmark (in Danish).
Pihl S, Clausen P, Petersen IK, Nielsen RD, Laursen K, Bregnballe T, Holm TE, Søgaard B. 2013. Fugle 2004–2011. Scientific report from DCE, National Centre of Environment and Energy, No. 49. Department of Bioscience, Aarhus University, Denmark (in Danish).
Phil S, Holm TE, Clausen P, Petersen IK, Nielsen RD, Laursen K, Bregnballe T, Søgaard B. 2015. Fugle 2012–2013. Scientific report from DCE, National Centre of Environment and Energy, No. 125. Department of Bioscience, Aarhus University, Denmark (in Danish).
Philippart CJM, Beukema JJ, Cadee GC, Dekker R, Goedhart PW, van Iperen JM, Leopold MF, Herman PMJ. 2007. Impacts of nutrient reduction on coastal communities. Ecosystems 10:95–118.
Post DM. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–18.
Richardson K, Jørgensen BB. 2013. Eutrophication: Definition, history and effects. In: Jørgensen BB, Richardson K, Eds. Eutrophication in marine coastal ecosystems. Washington, DC: American Geophysical Union. p 1–19.
SAS. 2012. JMP version 10.2. SAS Institute, Inc., Cary, NC.
Svendsen, LM, Windolf J, Ellermann T. 2012. Tilførsel af næringsstoffer og organiske stoffer. Notat 2.8. DCE-National Center for Environment and Energy, Aarhus University. Denmark (in Danish).
Svendsen LM, Maar M, Hansen JW. 2014. Nogle faglige aspekter ved anvendelse af HELCOMS reduktionsmål til national regulering af havbrug—Fase 1. Technical report from DCE, National Centre of Environment and Energy. Aarhus University. Denmark (in Danish).
Thomsen H, Nielsen TG, Richardson K. 2002. Udvalget om Miljøpåvirkninger og fiskeriressourcer. Delrapport om eutrofiering. Technical report. DFU—rapport nr. 110-02, Danmarks Fiskeriundersøgelser., Denmark (in Danish).
Van Stralen MR. 1995. De groei en aanvoer van gekweekte mosselen (Mytilus edulis) na 1952 en de ontwikkeling van het kokkelbestand (Cerastoderme edule) in relatie tot het voedselaanbod, eutrofiëring en andrere milieufactoren in de Waddenzee. DLO-Rijksinstituut voor Visserijonderzoek 95:016 (in Dutch).
Vágási CI, Pap PL, Barta Z. 2010. Haste makes waste: Accelerated molt adversely affects the expression of melanin-based and depigmented plumage ornaments in house sparrows. PLoS One 5(12):e14215.
Vanderklift MA, Ponsard S. 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–82.
Vitousek PM, Aber J, Howarth RW, Tilman GD, Matson PA, Schindler DW, Schlesinger WH, Tilman DG. 1997a. Human alteration of the global nitrogen cycle: causes and consequences. Ecol Appl 7:737–50.
Vitousek PM, Mooney HA, Lubchenko J, Melillo JM. 1997b. Human domination of earth’s ecosystems. Science 277:494–9.
Acknowledgements
We thank the hunters who collected birds for the study and Ako Osman Mirza who assisted in the laboratory. We also thank two anonymous reviewers for valuable comments and suggestions. This study received financial support from the 15 June Foundation (Ref.: 2015-B-132) in Denmark and an operating grant from Environment Canada to KAH. Chantel Gryba assisted with sample preparation and Geoff Koehler of the Environment Canada stable isotope facility in Saskatoon, Canada, assisted with stable isotope measurements.
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APM conceived the project, KL and KAH collected the data, APM and KL analyzed the data, APM, KL and KAH wrote the manuscript.
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Laursen, K., Møller, A.P. & Hobson, K.A. N-Isotopes in Feathers and Abundance of Eiders Respond to Nutrients in Seawater. Ecosystems 22, 1271–1279 (2019). https://doi.org/10.1007/s10021-018-00334-w
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DOI: https://doi.org/10.1007/s10021-018-00334-w