Environmental Science and Pollution Research

, Volume 24, Issue 14, pp 13025–13035 | Cite as

Presence of persistent organic pollutants in a breeding common tern (Sterna hirundo) population in Ireland

  • Heidi Acampora
  • Philip White
  • Olga Lyashevska
  • Ian O’Connor
Research Article

Abstract

Persistent organic pollutants (POPs) are chemical compounds of environmental concern due to their toxic, persistent nature and their ability to bio-accumulate in biological tissue. Seabirds, for often being at the top of the food web, have been used as monitors of environmental pollutants. Adverse effects caused by POPs have been reported in common terns (Sterna hirundo) since the 1970s. Egg shell thinning, embryo and hatchling deformities have been reported for this species. Environmental legislation, such as the Oslo-Paris Convention (OSPAR), has agreed on the monitoring of concentration of POPs in common terns. This study set out to investigate contemporary concentrations of polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), organochlorine pesticides (OCPs) and brominated flame retardants (BFRs) in common terns breeding in Ireland, along with congener profiles. Investigation was conducted in live (n = 15) and dead birds (n = 20) to test for the efficiency of different methodologies using preen oil and feathers versus liver and preen gland. Mean concentrations of POPs followed the order: PCB (36.48 ng/g ww feather) > PAH (30.01 ng/g ww feather) > OCP (13.36 ng/g ww feather) > BFR (1.98 ng/g ww feather) in live birds; and PAH (46.65 ng/g ww preen gland) > PCB (44.11 ng/g ww preen gland) > OCP (15.15 ng/g ww liver) > BFR (5.07 ng/g ww liver) in dead birds. Comparison of contaminant results with toxicity pre-established levels concluded that this population of common terns in Ireland is not at risk of anomalies caused by POPs. However, some levels are higher in comparison to the ones established by OSPAR’s EcoQO and must be monitored periodically.

Keywords

Common tern Sterna hirundo Persistent organic pollutants PCB PAH OCP BFR 

Notes

Acknowledgments

This work was supported by Science Without Borders (CAPES, Brazil, BEX: 1269-13-5). Many thanks to all at BirdWatch Ireland. Thanks to Steve Newton. Special thanks to Rockabill wardens Brian Burke and Andrew Power. Thanks to Niall Keogh for assistance in the field. Thanks to Danilo Hirota, Killian Coakley and Bill Delee for assistance in the lab. Thanks to anonymous reviewers for improving the quality of this manuscript.

References

  1. Arnold JM, Hatch JJ, Nisbet ICT (2004) Seasonal declines in reproductive success of the common tern Sterna hirundo: timing or parental quality? J Avian Biol 35(1):33–45CrossRefGoogle Scholar
  2. Austin OL (1953) The migration of the common tern (Sterna hirundo) in the western hemisphere. Bird-Banding:39–55Google Scholar
  3. Barron MG, Galbraith H, Beltman D (1995) Comparative reproductive and developmental toxicology of PCBs in birds. Comp Biochem Physiol C: Pharmacol Toxicol Endocrinol 112(1):1–14Google Scholar
  4. Becker PH, Schuhmann S, Koepff C (1993) Hatching failure in common terns (Sterna hirundo) in relation to environmental chemicals. Environ Pollut 79:207–213CrossRefGoogle Scholar
  5. Bosveld ATC, Van den Berg M (1994) Effects of polychlorinated biphenyls, dibenzo-p-dioxins, and dibenzofurans on fish-eating birds. Environ Rev 2(2):147–166CrossRefGoogle Scholar
  6. Bosveld ATC, Gradener J, Murk AJ, Brouwer A, Van Kampen M, Evers EHG, Van den Berg M (1995) Effects of PCBs, PCDDs and PCDFs in common tern (Sterna hirundo) breeding in estuarine and coastal colonies in the Netherlands and Belgium. Environ Toxicol Chem 14(1):99–115CrossRefGoogle Scholar
  7. Broman D, Näuf C, Lundbergh I, Zebühr Y (1990) An in situ study on the distribution, biotransformation and flux of polycyclic aromatic hydrocarbons (pahs) in an aquatic food chain (seston-Mytilus edulis L.-Somateria mollissima L.) from the baltic: an ecotoxicological perspective. Environ Toxicol Chem 9(4):429–442Google Scholar
  8. Brunström B, Andersson L, Nikolaidis E, Dencker L (1990) Non-ortho-and mono-ortho-chlorine-substituted polychlorinated biphenyls—embryotoxicity and inhibition of lymphoid development. Chemosphere 20(7–9):1125–1128CrossRefGoogle Scholar
  9. Burke B, Kinchin-Smith D, Somers S, Newton S (2016) Rockabill Tern Report 2016. BirdWatch Ireland Seabird Conservation Report. BirdWatch Ireland Seabird Conservation ReportGoogle Scholar
  10. Cabot D, Nisbet I (2013) Terns. In: Corbet SA, West R, Streeter D, Silvertown J (eds) Journal of Field Ornithology (Vol. 85). HarperCollins Publishers, LondonGoogle Scholar
  11. Custer TW, Custer CM, Dickerson K, Allen K, Melancon MJ, Schmidt LJ (2001) Polycyclic aromatic hydrocarbons, aliphatic hydrocarbons, trace elements, and monooxygenase activity in birds nesting on the North Platte River, Casper, Wyoming, USA. Environ Toxicol Chem 20(3):624–631CrossRefGoogle Scholar
  12. Derraik JGB (2002) The pollution of the marine environment by plastic debris: a review. Mar Pollut Bull 44(9):842–852. doi:10.1016/S0025-326X(02)00220-5 CrossRefGoogle Scholar
  13. Dittmann T, Becker PH, Bakker J, Bignert A, Nyberg E, Pereira MG et al (2012) Large-scale spatial pollution patterns around the North Sea indicated by coastal bird eggs within an EcoQO programme. Environ Sci Pollut Res 19(9):4060–4072CrossRefGoogle Scholar
  14. Elliott JE, Butler RW, Norstrom RJ, Whitehead PE (1989) Environmental contaminants and reproductive success of great blue herons Ardea herodias in British Columbia, 1986–1987. Environ Pollut 59(2):91–114CrossRefGoogle Scholar
  15. Elliott J, Wilson LK, Wakeford B (2005) Polybrominated diphenyl ether trends in eggs of marine and freshwater birds from British Columbia, Canada, 1979–2002. Environmental Science & Technology 39(15):5584–5591CrossRefGoogle Scholar
  16. Falkowska L, Reindl AR, Grajewska A, Lewandowska AU (2016) Organochlorine contaminants in the muscle, liver and brain of seabirds (Larus) from the coastal area of the southern Baltic. Ecotoxicol Environ Saf 133:63–72. doi:10.1016/j.ecoenv.2016.06.042 CrossRefGoogle Scholar
  17. Fox GA (1976) Eggshell quality: its ecological and physiological significance in a DDE-contaminated common tern population. The Wilson Bulletin 88(3):459–477Google Scholar
  18. Giesy JP, Ludwig JP, Tillitt DE (1994) Dioxins, dibenzofurans, PCBs and colonial, fish-eating water birds. In: Schecter A (ed) Dioxins and health. Springer US, Boston, pp 249–307. doi:10.1007/978-1-4899-1462-0_9 CrossRefGoogle Scholar
  19. Gilbertson M, Fox GA (1977) Pollutant-associated embryonic mortality of Great Lakes herring gulls. Environmental Pollution (1970) 12(3):211–216CrossRefGoogle Scholar
  20. Gilbertson MMRD, Morris RD, Hunter RA (1976) Abnormal chicks and PCB residue levels in eggs of colonial birds on the lower Great Lakes (1971-73). Auk 93(3):434–442Google Scholar
  21. Ginn HB, Melville DS (1983) Moult in birds: BTO guide. British Trust for OrnithologyGoogle Scholar
  22. Hall RJ, Coon NC (1988) Interpreting residues of petroleum hydrocarbons in wildlife tissues. US Fish and Wildlife ServiceGoogle Scholar
  23. Hays H, Risebrough RW (1972) Pollutant concentrations in abnormal young terns from Long Island sound. Auk 89(1):19–35CrossRefGoogle Scholar
  24. Hoffman DJ, Smith GJ, Rattner BA (1993) Biomarkers of contaminant exposure in common terns and black-crowned night herons in the Great Lakes. Environ Toxicol Chem 12(6):1095–1103. doi:10.1002/etc.5620120615 CrossRefGoogle Scholar
  25. Hoffman DJ, Rice CP, Kubiak TJ (1996) PCBs and dioxins in birds. Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations, 165–207Google Scholar
  26. Hoffman DJ, Melancon MJ, Klein PN, Eisemann JD, Spann JW (1998) Comparative developmental toxicity of planar polychlorinated biphenyl congeners in chickens, american krestels, and common terns. Environ Toxicol Chem 17(4):747–757CrossRefGoogle Scholar
  27. Jacob J, Ziswiler V (1982) The uropygial gland. Avian Biology 6:199–324CrossRefGoogle Scholar
  28. Janke AK, Anteau MJ, Markl N, Stafford JD (2015) Is income breeding an appropriate construct for waterfowl? J Ornithol 156(3):755–762. doi:10.1007/s10336-015-1200-y CrossRefGoogle Scholar
  29. Jaspers VLB, Oorspoels S, Covaci A, Eens M (2006) Can predatory bird feathers be used as a non-destructive biomonitoring tool of organic pollutants? Biol Lett 2(2):283–285. doi:10.1098/rsbl.2006.0450 CrossRefGoogle Scholar
  30. Jaspers VLB, Voorspoels S, Covaci A, Lepoint G, Eens M (2007) Evaluation of the usefulness of bird feathers as a non-destructive biomonitoring tool for organic pollutants: a comparative and meta-analytical approach. Environ Int 33(3):328–337. doi:10.1016/j.envint.2006.11.011 CrossRefGoogle Scholar
  31. Jaspers VLB, Covaci A, Deleu P, Neels H, Eens M (2008) Preen oil as the main source of external contamination with organic pollutants onto feathers of the common magpie (Pica pica). Environ Int 34(6):741–748. doi:10.1016/j.envint.2007.12.002 CrossRefGoogle Scholar
  32. Jaspers VLB, Rodriguez FS, Boertmann D, Sonne C, Dietz R, Rasmussen LM et al (2011) Body feathers as a potential new biomonitoring tool in raptors: a study on organohalogenated contaminants in different feather types and preen oil of West Greenland white-tailed eagles (Haliaeetus albicilla). Environ Int 37(8):1349–1356CrossRefGoogle Scholar
  33. Jenssen BM, Sørmo EG, Bæk K, Bytingsvik J, Gaustad H, Ruus A, Skaare JU (2007) Brominated flame retardants in north-East Atlantic marine ecosystems. Environ Health Perspect 115(SUPPL1):35–41. doi:10.1289/ehp.9355 CrossRefGoogle Scholar
  34. Jones KC, de Voogt P (1999) Persistent organic pollutants (POPs): state of the science. Environ Pollut 100(1–3):209–221. doi:10.1016/S0269-7491(99)00098-6 CrossRefGoogle Scholar
  35. Koeman JH, Oskamp AAG, Veen J, Brouwer E, Rooth J, Zwart P et al (1967) Insecticides as a factor in the mortality of the sandwich tern (Sterna sandvicensis). Meded Rijksfac Landbouwwetenschappen Gent 32:841Google Scholar
  36. Kubiak TJ, Harris HJ, Smith LM, Schwartz TR, Stalling DL, Trick JA et al (1989) Microcontaminants and reproductive impairment of the Forster’s tern on Green Bay, Lake Michigan-1983. Arch Environ Contam Toxicol 18(5):706–727. doi:10.1007/BF01225009 CrossRefGoogle Scholar
  37. Lemmetyinen R, Rantamäki P, Karlin A (1982) Levels of DDT and PCB’s in different stages of life cycle of the Arctic tern Sterna paradisaea and the herring gull Larus argentatus. Chemosphere 11(10):1059–1068CrossRefGoogle Scholar
  38. MacRae JD, Hall KJ (1998) Biodegradation of polycyclic aromatic hydrocarbons (PAH) in marine sediment under denitrifying conditions. Water Sci Technol 38(11):177–185CrossRefGoogle Scholar
  39. Massias A, Becker PH (1990) Nutritive value of food and growth in common tern Sterna hirundo chicks. Ornis Scand:187–194Google Scholar
  40. Mitchell PI, Newton SF, Ratcliffe N, Eds TED, Dunn TE, Poyser AD, May L (2004) Seabird populations of Britain and Ireland: results of the Seabird 2000 census. JNCC, Poyser, London., (August)Google Scholar
  41. Moore NW, Tatton J (1965) Organochlorine insecticide residues in the eggs of sea birdsGoogle Scholar
  42. Mora MA, Durgin B, Hudson LB, Jones E (2016) Temporal and latitudinal trends of p,p’-DDE in eggs and carcass of North American birds from 1980-2005. Environ Toxicol Chem 35(6):1340–1348. doi:10.1002/etc.3360 CrossRefGoogle Scholar
  43. Nfon E, Cousins IT, Broman D (2008) Biomagnification of organic pollutants in benthic and pelagic marine food chains from the Baltic Sea. Sci Total Environ 397(1):190–204CrossRefGoogle Scholar
  44. OSPAR (2010) The Ospar system of ecological quality objectives for the North sea, 16Google Scholar
  45. Pariatamby A, Kee YL (2016) Persistent organic pollutants management and remediation. Procedia Environmental Sciences 31:842–848. doi:10.1016/j.proenv.2016.02.093 CrossRefGoogle Scholar
  46. Peck LE, Gilchrist HG, Mallory CD, Braune BM, Mallory ML (2016) Persistent organic pollutant and mercury concentrations in eggs of ground-nesting marine birds in the Canadian high Arctic. Sci Total Environ 556(March):80–88. doi:10.1016/j.scitotenv.2016.02.205 CrossRefGoogle Scholar
  47. Perugini M, Visciano P, Giammarino A, Manera M, Di Nardo W, Amorena M (2007) Polycyclic aromatic hydrocarbons in marine organisms from the Adriatic Sea, Italy. Chemosphere 66(10):1904–1910CrossRefGoogle Scholar
  48. R Core Team. (2015) A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Retrieved from https://www.r-project.org
  49. Roscales JL, Gonzalez-Solis J, Calabuig P, Jimenez B (2011) Interspecies and spatial trends in polycyclic aromatic hydrocarbons (PAHs) in Atlantic and Mediterranean pelagic seabirds. Environ Pollut 159(10):2899–2905. doi:10.1016/j.envpol.2011.04.034 CrossRefGoogle Scholar
  50. Scharenberg W (1991) Prefledging terns (Sterna paradisaea, Sterna hirundo) as bioindicators for organochlorine residues in the German Wadden Sea. Arch Environ Contam Toxicol 21(1):102–105CrossRefGoogle Scholar
  51. Smith LM, Schwartz TR, Feltz K, Kubiak TJ (1990) Determination and occurrence of AHH-active polychlorinated biphenyls, 2, 3, 7, 8-tetrachloro-p-dioxin and 2, 3, 7, 8-tetrachlorodibenzofuran in Lake Michigan sediment and biota. The question of their relative toxicological significance. Chemosphere 21(9):1063–1085CrossRefGoogle Scholar
  52. Stockholm Convention, 2001 (2001) Stockholm Convention on Persistent Organic Pollutants (p. http://chm.pops.int/)
  53. Su H, Wu F, Zhang R, Zhao X, Mu Y, Feng C, Giesy JP (2014) Toxicity reference values for protecting aquatic birds in China from the effects of polychlorinated biphenyls. In Reviews of Environmental Contamination and Toxicology volume (pp. 59–82). SpringerGoogle Scholar
  54. Tanabe S, Tanaka H, Tatsukawa R (1984) Polychlorobiphenyls, $Σ$DDT, and hexachlorocyclohexane isomers in the western North Pacific ecosystem. Arch Environ Contam Toxicol 13(6):731–738. doi:10.1007/BF01055937 CrossRefGoogle Scholar
  55. Tanaka K, Takada H, Yamashita R, Mizukawa K, Fukuwaka M, Watanuki Y (2015) Facilitated leaching of additive-derived PBDEs from plastic by seabirds’ stomach oil and accumulation in tissues. Environmental Science & Technology . doi:10.1021/acs.est.5b01376150901174241000Google Scholar
  56. United Nations Environment Programme. Division of Early Warning, and Assessment. UNEP Year Book 2011: Emerging Issues in Our Global Environment. UNEP/Earthprint, 2011Google Scholar
  57. Van Den Brink NW (1997) Directed transport of volatile organochlorine pollutants to polar regions: the effect of the contamination pattern of Antarctic seabirds. Sci Total Environ 198(1):43–50. doi:10.1016/S0048-9697(97)05440-5 CrossRefGoogle Scholar
  58. Van Den Brink NW, Bosveld ATC (2001) PCB concentrations and metabolism patterns in common terns (Sterna hirundo) from different breeding colonies in The Netherlands. Mar Pollut Bull 42(4):280–285. doi:10.1016/S0025-326X(00)00151-X CrossRefGoogle Scholar
  59. Van den Steen E, Covaci A, Jaspers VLB, Dauwe T, Voorspoels S, Eens M, Pinxten R (2007) Experimental evaluation of the usefulness of feathers as a non-destructive biomonitor for polychlorinated biphenyls (PCBs) using silastic implants as a novel method of exposure. Environ Int 33(2):257–264CrossRefGoogle Scholar
  60. Van Franeker JA (2004) Save the North Sea fulmar-Litter-EcoQO manual part 1: collection and dissection procedures., 38. Retrieved from http://edepot.wur.nl/40451
  61. Wan Y, Jin X, Hu J, Jin F (2007) Trophic dilution of polycyclic aromatic hydrocarbons (PAHs) in a marine food web from Bohai Bay, North China. Environmental Science & Technology 41(9):3109–3114CrossRefGoogle Scholar
  62. Wang J, Caccamise SAL, Woodward LA, Li QX (2015) Polychlorinated biphenyls in the plasma and preen oil of black-footed albatross (Diomedea nigripes) chicks and adults on midway atoll, North Pacific Ocean. PLoS One 10(4):e0123041. doi:10.1371/journal.pone.0123041 CrossRefGoogle Scholar
  63. Yamashita R, Takada H, Murakami M, Fukuwaka MA, Watanuki Y (2007) Evaluation of noninvasive approach for monitoring PCB pollution of seabirds using preen gland oil. Environ Sci Technol 41(14):4901–4906. doi:10.1021/es0701863 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Marine & Freshwater Research CentreGalway-Mayo Institute of TechnologyGalwayIreland

Personalised recommendations