Skip to main content
SpringerLink
Log in

High levels of perfluoroalkyl acids in eggs and embryo livers of great cormorant (Phalacrocorax carbo sinensis) and herring gull (Larus argentatus) from Lake Vänern, Sweden

  • Nordic Research on Perfluoroalkyl and Polyfluoroalkyl Substances (PFASs)
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In the eggs and developing chick livers in the two wild bird species, great cormorant and herring gull, the concentrations of a range of 15 perfluoroalkyl acids (PFAAs) were determined. Eggs of the two species were collected from Lake Vänern, Sweden, and analysed either as undeveloped egg (whole egg or separated into yolk and albumen) or incubated until start of the hatching process when the chick liver was removed and analysed. High levels of PFAAs were found in all matrixes except albumen. The predominant PFAA was perfluorooctane sulfonate (PFOS), which was found in the μg/g wet weight (ww) range in some samples of cormorant whole egg, yolk and liver and herring gull egg yolk and liver. The average concentration in yolk was 1,506 ng/g ww in cormorant and 589 ng/g ww in herring gull. The average liver concentrations of PFOS were 583 ng/g ww in cormorant and 508 ng/g ww in herring gull. At these concentrations, biochemical effects in the developing embryo or effects on embryo survival cannot be ruled out. For perfluoroalkyl carboxylates (PFCAs), the liver/egg and liver/yolk concentration ratios increased with PFCA chain length in cormorant but not in herring gull, indicating that chain length could possibly affect egg-to-liver transfer of PFCAs and that species differences may exist.

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
Fig. 4

Similar content being viewed by others

References

  • Boulanger B, Vargo J, Schnoor JL, Hornbuckle KC (2004) Detection of Perfluorooctane Surfactants in Great Lakes Water. Environ Sci Technol 38:4064–4070. doi:10.1021/es0496975

    Article  CAS  Google Scholar 

  • Bregnballe T, Frederiksen M, Gregersen J (1997) Seasonal distribution and timing of migration of Cormorants Phalacrocorax carbo sinensis breeding in Denmark. Bird Study 44:257. doi:10.1080/00063659709461062

    Article  Google Scholar 

  • Buck RC, Franklin J, Berger U, Conder JM, Cousins IT, de Voogt P, Jensen AA, Kannan K, Mabury SA, van Leeuwen SP (2011) Perfluoroalkyl and polyfluoroalkyl substances in the environment: terminology, classification, and origins. Integr Environ Assess Manag 7:513–541. doi:10.1002/ieam.258

    Article  CAS  Google Scholar 

  • Bukacińska M, Bukaciński D, Spaans AL (1996) Attendance and diet in relation to breeding success in herring gulls (Larus argentatus). Auk 113:300–309

    Article  Google Scholar 

  • Bylin K (1978) Sveriges faglar: aktuell oversikt over deras utbredning, numerar och flyttning samt nagot om svensk ornitologi Sveriges ornitologiska forening, Stockholm

  • Engström H (2001) Long term effects of cormorant predation on fish communities and fishery in a freshwater lake. Ecography 24:127–138. doi:10.1034/j.1600-0587.2001.240203.x

    Article  Google Scholar 

  • Gebbink WA, Letcher RJ (2012) Comparative tissue and body compartment accumulation and maternal transfer to eggs of perfluoroalkyl sulfonates and carboxylates in Great Lakes herring gulls. Environ Pollut 162:40–47. doi:10.1016/j.envpol.2011.10.011

    Article  CAS  Google Scholar 

  • Gebbink WA, Hebert CE, Letcher RJ (2009) Perfluorinated Carboxylates and Sulfonates and Precursor Compounds in Herring Gull Eggs from Colonies Spanning the Laurentian Great Lakes of North America. Environ Sci Technol 43:7443–7449. doi:10.1021/es901755q

    Article  CAS  Google Scholar 

  • Gebbink WA, Letcher RJ, Hebert CE, Chip Weseloh DV (2011) Twenty years of temporal change in perfluoroalkyl sulfonate and carboxylate contaminants in herring gull eggs from the Laurentian Great Lakes. J Environ Monit 13:3365–3372. doi:10.1039/c1em10663e

    Article  CAS  Google Scholar 

  • Giesy JP, Kannan K (2001) Global Distribution of Perfluorooctane Sulfonate in Wildlife. Environ Sci Technol 35:1339–1342. doi:10.1021/es001834k

    Article  CAS  Google Scholar 

  • Holmström KE, Berger U (2008) Tissue Distribution of Perfluorinated Surfactants in Common Guillemot (Uria aalge) from the Baltic Sea. Environ Sci Technol 42:5879–5884. doi:10.1021/es800529h

    Article  Google Scholar 

  • Holmström KE, Järnberg U, Bignert A (2005) Temporal Trends of PFOS and PFOA in Guillemot Eggs from the Baltic Sea, 1968–2003. Environ Sci Technol 39:80–84. doi:10.1021/es049257d

    Article  Google Scholar 

  • Holmström KE, Johansson A-K, Bignert A, Lindberg P, Berger U (2010) Temporal Trends of Perfluorinated Surfactants in Swedish Peregrine Falcon Eggs (Falco peregrinus), 1974–2007. Environ Sci Technol 44:4083–4088. doi:10.1021/es100028f

    Article  Google Scholar 

  • Jones PD, Hu W, De Coen W, Newsted JL, Giesy JP (2003) Binding of perfluorinated fatty acids to serum proteins. Environ Toxicol Chem 22:2639–2649. doi:10.1897/02-553

    Article  CAS  Google Scholar 

  • Kärrman A, Ericson I, van Bavel B, Darnerud PO, Aune M, Glynn A, Lignell S, Lindström G (2007) Exposure of Perfluorinated Chemicals through Lactation: Levels of Matched Human Milk and Serum and a Temporal Trend, 1996–2004, in Sweden. Environ Health Perspect 115:226–230. doi:10.1289/ehp.9491

    Article  Google Scholar 

  • Kissa E (2001) Fluorinated Surfactants and Repellents, 2nd edn. CRC Press, New York

    Google Scholar 

  • Lau C (2003) Exposure to Perfluorooctane Sulfonate during Pregnancy in Rat and Mouse. II: Postnatal Evaluation. Toxicol Sci 74:382–392. doi:10.1093/toxsci/kfg122

    Article  CAS  Google Scholar 

  • Lau C, Thibodeaux JR, Hanson RG, Narotsky MG, Rogers JM, Lindstrom AB, Strynar MJ (2006) Effects of perfluorooctanoic acid exposure during pregnancy in the mouse. Toxicol Sci 90:510

    Article  CAS  Google Scholar 

  • Molina ED, Balander R, Fitzgerald SD, Giesy JP, Kannan K, Mitchell R, Bursian SJ (2006) Effects of air cell injection of perfluorooctane sulfonate before incubation on development of the white leghorn chicken (Gallus domesticus) embryo. Environ Toxicol Chem 25:227–232. doi:10.1897/04-414R.1

    Article  CAS  Google Scholar 

  • Newsted JL, Beach SA, Gallagher SP, Giesy JP (2006) Pharmacokinetics and Acute Lethality of Perfluorooctanesulfonate (PFOS) to Juvenile Mallard and Northern Bobwhite. Arch Environ Contam Toxicol 50:411–420. doi:10.1007/s00244-005-1137-x

    Article  CAS  Google Scholar 

  • Newsted JL, Coady KK, Beach SA, Butenhoff JL, Gallagher S, Giesy JP (2007) Effects of perfluorooctane sulfonate on mallard and northern bobwhite quail exposed chronically via the diet. Environ Toxicol Pharmacol 23:1–9

    Article  CAS  Google Scholar 

  • Nordén M, Westman O, Venizelos N, Engwall M (2012) Perfluorooctane sulfonate increases β-oxidation of palmitic acid in chicken liver. Environ Sci Pollut Res 19:1859–1863. doi:10.1007/s11356-012-0869-1

    Article  Google Scholar 

  • O’Brien JM, Crump D, Mundy LJ, Chu S, McLaren KK, Vongphachan V, Letcher RJ, Kennedy SW (2009) Pipping success and liver mRNA expression in chicken embryos exposed in ovo to C8 and C11 perfluorinated carboxylic acids and C10 perfluorinated sulfonate. Toxicol Lett 190:134–139. doi:10.1016/j.toxlet.2009.07.004

    Article  Google Scholar 

  • Peden-Adams MM, Keller JM, EuDaly JG, Berger J, Gilkeson GS, Keil DE (2008) Suppression of Humoral Immunity in Mice following Exposure to Perfluorooctane Sulfonate. Toxicol Sci 104:144–154. doi:10.1093/toxsci/kfn059

    Article  CAS  Google Scholar 

  • Pierotti R, Annett CA (1991) Diet Choice in the Herring Gull: Constraints Imposed by Reproductive and Ecological Factors. Ecology 72:319–328

    Article  Google Scholar 

  • Prevedouros K, Cousins IT, Buck RC, Korzeniowski SH (2006) Sources, Fate and Transport of Perfluorocarboxylates. Environ Sci Technol 40:32–44. doi:10.1021/es0512475

    Article  CAS  Google Scholar 

  • Rüdel H, Müller J, Jürling H, Schröter-Kermani C (2010) Retrospective monitoring of perfluorinated compounds in archived herring gull eggs. Interdisciplinary Studies on Environmental Chemistry-Environmental Specimen Bank Eds: T Isobe, K Nomiyama, A Subramanian and S Tanabe:81–86

  • Rüdel H, Müller J, Jürling H, Bartel-Steinbach M, Koschorreck J (2011) Survey of patterns, levels, and trends of perfluorinated compounds in aquatic organisms and bird eggs from representative German ecosystems. Environ Sci Pollut Res 18:1457–1470. doi:10.1007/s11356-011-0501-9

    Article  Google Scholar 

  • van Leeuwen SPJ, Swart CP, van der Veen I, de Boer J (2009) Significant improvements in the analysis of perfluorinated compounds in water and fish: Results from an interlaboratory method evaluation study. J Chromatogr A 1216:401–409. doi:10.1016/j.chroma.2008.11.029

    Article  Google Scholar 

  • Verreault J, Houde M, Gabrielsen GW, Berger U, Haukås M, Letcher RJ, Muir DCG (2005) Perfluorinated Alkyl Substances in Plasma, Liver, Brain, and Eggs of Glaucous Gulls (Larus hyperboreus) from the Norwegian Arctic. Environ Sci Technol 39:7439–7445. doi:10.1021/es051097y

    Article  CAS  Google Scholar 

  • Verreault J, Berger U, Gabrielsen GW (2007) Trends of Perfluorinated Alkyl Substances in Herring Gull Eggs from Two Coastal Colonies in Northern Norway: 1983–2003. Environ Sci Technol 41:6671–6677. doi:10.1021/es070723j

    Article  CAS  Google Scholar 

  • Wang Y, Yeung L, Yamashita N, Taniyasu S, So M, Murphy M, Lam P (2008) Perfluorooctane sulfonate (PFOS) and related fluorochemicals in chicken egg in China. Chin Sci Bull 53:501–507. doi:10.1007/s11434-008-0128-5

    Article  CAS  Google Scholar 

  • Yoo H, Guruge KS, Yamanaka N, Sato C, Mikami O, Miyazaki S, Yamashita N, Giesy JP (2009) Depuration kinetics and tissue disposition of PFOA and PFOS in white leghorn chickens (Gallus gallus) administered by subcutaneous implantation. Ecotoxicol Environ Saf 72:26–36. doi:10.1016/j.ecoenv.2007.09.007

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Funding for this project was provided by The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas). We would like to thank Sten-Gunnar Steensson and Ola Westman for help with egg collection and Maria Larsson, Katrin Holmström and Anne-Sofie Kärsrud for help with analysis and result interpretation.

Author information

Authors and Affiliations

  1. Man-Technology-Environment Research Centre (MTM), School of Science and Technology, Örebro University, 701 82, Örebro, Sweden

    Marcus Nordén & Magnus Engwall

  2. Department of Applied Environmental Science (ITM), Stockholm University, 106 91, Stockholm, Sweden

    Urs Berger

Authors
  1. Marcus Nordén
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Urs Berger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Magnus Engwall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Magnus Engwall.

Additional information

Responsible editor: Ester Heath

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 35.7 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nordén, M., Berger, U. & Engwall, M. High levels of perfluoroalkyl acids in eggs and embryo livers of great cormorant (Phalacrocorax carbo sinensis) and herring gull (Larus argentatus) from Lake Vänern, Sweden. Environ Sci Pollut Res 20, 8021–8030 (2013). https://doi.org/10.1007/s11356-013-1567-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-1567-3

Keywords

Search

Navigation