Environmental Science and Pollution Research

, Volume 26, Issue 10, pp 9640–9648 | Cite as

Trace element concentrations in feathers of seven petrels (Pterodroma spp.)

  • Susan M. Philpot
  • Jennifer L. LaversEmail author
  • Dayanthi Nugegoda
  • Morgan E. Gilmour
  • Ian Hutton
  • Alexander L. Bond
Research Article


Gadfly petrels (Pterodroma spp.) are one of the most threatened and poorly studied seabird groups, and as marine predators, are exposed to biomagnified and bioaccumulated chemical pollutants from their prey. We quantified trace element concentrations in breast feathers of seven petrel species that breed in the southern hemisphere to quantify current concentrations. Selenium (Se) concentrations were significantly lower in chicks than adults; this was not observed for zinc (Zn) or lead (Pb). Overall, the species examined here exhibited similar concentrations of Se, with Pb and Zn concentrations more variable among species. The mean Se concentration in adult birds exceeded those thought to be potentially deleterious, and three species had concentrations that were above the assumed threshold for Pb toxicity. Further investigation of potentially toxic trace elements in gadfly petrels is warranted.


Feathers Lead Petrels Procellariiformes Selenium Zinc 



This research was undertaken with approval from the University of Tasmania Animal Ethics Committee (permit no. A13836 and A150319). The 2015 Henderson Island expedition was funded by the David & Lucille Packard Foundation, the Darwin Initiative, the Farallon Islands Foundation, British Birds and several private donors. We thank the Pitcairn Islands Environmental, Conservation, and Natural Resources Division for permission to work on Henderson Island, and S. Oppel for generous support in the field. Our thanks to Ovenstone Agencies (Pty) Ltd. and the South African Department of Environmental Affairs (South African National Antarctic Program, SANAP) for logistical support and transport to Tristan da Cunha. The Royal Society for the Protection of Birds, the UK partner in BirdLife International, funded the Tristan da Cunha component of this research. We thank the Tristan da Cunha Conservation Department for granting permission for sample collection, and D. Fox and C. Taylor (Tristan Conservation Department) for assisting with sample collection. Finally, we thank the Western Australian Department of Parks and Wildlife for assistance on Breaksea Island and A. Finger, P. Morrison and C. Trestrail for analytical support. Comments from two anonymous reviewers improved on earlier versions of this manuscript.


  1. Ackerman JT, Eagles-Smith CA, Herzog MP, Yee JL, Hartman CA (2016) Egg-laying sequence influences egg mercury concentrations and egg size in three bird species: implications for contaminant monitoring programs. Environ Toxicol Chem 35:1458–1469CrossRefGoogle Scholar
  2. Afshan S, Ali S, Ameen US, Farid M, Bharwana SA, Hannan F, Ahmad R (2014) Effect of different heavy metal pollution on fish. Res J Chem Environ Sci 2:74–79Google Scholar
  3. Anderson ORJ, Phillips RA, Shore RF, McGill RAR, McDonald RA, Bearhop S (2010) Element patterns in albatrosses and petrels: influence of trophic position, foraging range, and prey type. Environ Pollut 158:98–107CrossRefGoogle Scholar
  4. Anderson ORJ, Small CJ, Croxall JP, Dunn EK, Sullivan BJ, Yates O, Black A (2011) Global seabird bycatch in longline fisheries. Endanger Species Res 14:91–106CrossRefGoogle Scholar
  5. Australian Government (2012) Species group report card—seabirds. supporting the marine bioregional plan for the South-west Marine Region, Department of Sustainability, Environment, Water, Population, and Communities, Canberra, ACTGoogle Scholar
  6. Ayres RU (1992) Toxic heavy metals: materials cycle optimization. Proc Natl Acad Sci 89:815–820CrossRefGoogle Scholar
  7. Becker PH, Goutner V, Ryan PG, González-Solís J (2016) Feather mercury concentrations in Southern Ocean seabirds: variation by species, site and time. Environ Pollut 216:253–263CrossRefGoogle Scholar
  8. Bester A, Priddel D, Klomp N (2010) Diet and foraging behaviour of the Providence Petrel Pterodroma solandri. Mar Ornithol 39:163–172Google Scholar
  9. Birdlife International (2017) IUCN Red List for birds. Birdlife International, CambridgeGoogle Scholar
  10. Bocher P, Caurant F, Miramand P, Cherel Y, Bustamante P (2003) Influence of the diet on the bioaccumulation of heavy metals in zooplankton-eating petrels at Kerguelen archipelago, Southern Indian Ocean. Polar Biol 26:759–767CrossRefGoogle Scholar
  11. Bond AL, Diamond AW (2008) High within-individual variation in total mercury concentration in seabird feathers. Environ Toxicol Chem 27:2375–2377CrossRefGoogle Scholar
  12. Bond AL, Lavers JL (2011) Trace element concentrations in feathers of flesh-footed shearwaters (Puffinus carneipes) from across their breeding range. Arch Environ Contam Toxicol 61:318–326CrossRefGoogle Scholar
  13. Borgå K, Campbell L, Gabrielsen GW, Norstrom RJ, Muir DC, Fisk AT (2006) Regional and species specific bioaccumulation of major and trace elements in Arctic seabirds. Environ Toxicol Chem 25:2927–2936CrossRefGoogle Scholar
  14. Boye M, Wake BD, Garcia PL, Bown J, Baker AR, Achterberg EP (2012) Distributions of dissolved trace metals (Cd, Cu, Mn, Pb, Ag) in the southeastern Atlantic and the Southern Ocean. Biogeosciences 9:3231–3246CrossRefGoogle Scholar
  15. Braune BM, Gaskin DE (1987) Mercury levels in Bonaparte’s gulls (Larus philadelphia) during autumn molt in the Quoddy Region, New Brunswick, Canada. Arch Environ Contam Toxicol 16:539–549CrossRefGoogle Scholar
  16. Brooke ML, O’Connell TC, Wingate D, Madeiros J, Hilton GM, Ratcliffe N (2010) Potential for rat predation to cause decline of the globally threatened Henderson petrel Pterodroma atrata: evidence from the field, stable isotopes and population modelling. Endanger Species Res 11:47–59CrossRefGoogle Scholar
  17. Burger J (1993) Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 5:203–311Google Scholar
  18. Burger J, Gochfeld M (1995) Biomonitoring of heavy metals in the Pacific basin using avian feathers. Environ Toxicol Chem 14:1233–1239CrossRefGoogle Scholar
  19. Burger J, Gochfeld M (1997) Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ Res 75:160–172CrossRefGoogle Scholar
  20. Burger J, Gochfeld M (2000a) Metals in albatross feathers from Midway Atoll: influence of species, age, and nest location. Environ Res 82:207–221CrossRefGoogle Scholar
  21. Burger J, Gochfeld M (2000b) Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health B Crit Rev 3:59–78CrossRefGoogle Scholar
  22. Burger J, Gochfeld M (2004) Marine birds as sentinels of environmental pollution. EcoHealth 1:263–274CrossRefGoogle Scholar
  23. Burger J, Nisbet ICT, Gochfeld M (1994) Heavy metal and selenium levels in feathers of known-aged common terns (Sterna hirundo). Arch Environ Contam Toxicol 26:351–355CrossRefGoogle Scholar
  24. Bustamante P, Carravieri A, Goutte A, Barbraud C, Delord K, Chastel O, Weimerskirch H, Cherel Y (2016) High feather mercury concentrations in the wandering albatross are related to sex, breeding status and trophic ecology with no demographic consequences. Environ Res 144:1–10CrossRefGoogle Scholar
  25. Caravaggi A, Cuthbert RJ, Ryan PG, Cooper J, Bond AL (2018) The impacts of introduced house mice on the breeding success of nesting seabirds on Gough Island. Ibis.
  26. Carravieri A, Bustamante P, Churlaud C, Fromant A, Cherel Y (2014) Moulting patterns drive within-individual variations of stable isotopes and mercury in seabird body feathers: implications for monitoring of the marine environment. Mar Biol 161:963–968CrossRefGoogle Scholar
  27. Carvalho PC, Bugoni L, McGill RA, Bianchini A (2013) Metal and selenium concentrations in blood and feathers of petrels of the genus Procellaria. Environ Toxicol Chem 32:1641–1648CrossRefGoogle Scholar
  28. Chapman PM, Adams WJ, Brooks M, Delos CG, Luoma SN, Maher WA, Ohlendorf HM, Presser TS, Shaw P (2010) Ecological assessment of selenium in the aquatic environment, SETAC Pellston Workshop on Selenium in the Aquatic Environment. CRC Press, PensacolaCrossRefGoogle Scholar
  29. Cherel Y, Bocher P, Trouve C, Weimerskirch H (2002) Diet and feeding ecology of blue petrels Halobaena caerulea at Iles Kerguelen, Southern Indian Ocean. Mar Ecol Prog Ser 228:283–299CrossRefGoogle Scholar
  30. Cherel Y, Barbraud C, Lahournat M, Jaeger A, Jaquemet S, Wanless RM, Phillips RA, Thompson DR, Bustamante P (2018) Accumulate or eliminate? Seasonal mercury dynamics in albatrosses, the most contaminated family of birds. Environ Pollut 241:124–135CrossRefGoogle Scholar
  31. Cipro CVZ, Cherel Y, Caurant F, Miramand P, Méndez-Fernandez P, Bustamante P (2014) Trace elements in tissues of white-chinned petrels (Procellaria aequinoctialis) from Kerguelen waters, Southern Indian Ocean. Polar Biol 37:763–771CrossRefGoogle Scholar
  32. Clark R (2001) Marine pollution. Oxford University Press, New YorkGoogle Scholar
  33. Croxall JP, Butchart SHM, Lascelles B, Stattersfield AJJ, Sullivan BJJ, Symes A, Taylor P (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34CrossRefGoogle Scholar
  34. Cuthbert RJ, Louw H, Lurling J, Parker GH, Rexer-Huber K, Sommer E, Visser P, Ryan PG (2013) Low burrow occupancy and breeding success of burrowing petrels at Gough Island: a consequence of mouse predation. Bird Conserv Int 23:113–124CrossRefGoogle Scholar
  35. Elliott JE, Scheuhammer AM, Leighton FA, Pearce PA (1992) Heavy metal and metallothionein concentrations in Atlantic Canadian seabirds. Arch Environ Contam Toxicol 22:63–73CrossRefGoogle Scholar
  36. Finger A, Lavers JL, Dann P, Nugegoda D, Orbell JD, Robertson B, Scarpaci C (2015) The little penguin (Eudyptula minor) as an indicator of coastal trace metal pollution. Environ Pollut 205:365–377CrossRefGoogle Scholar
  37. Finger A, Lavers JL, Dann P, Nugegoda D, Orbell JD, Scarpaci C (2016) Seasonal variation and annual trends of metals and metalloids in the blood of the little penguin (Eudyptula minor). Mar Pollut Bull 110:261–273CrossRefGoogle Scholar
  38. Franson JC, Hoffman DJ, Wells-Berlin A, Perry MC, Shearn-Bochsler V, Finley DL, Flint PL, Hollmen T (2007) Effects of dietary selenium on tissue concentrations, pathology, oxidative stress, and immune function in common eiders (Somateria mollissima). J Toxicol Environ Health 70:861–874CrossRefGoogle Scholar
  39. Furness RW, Camphuysen K (1997) Seabirds as monitors of the marine environment. ICES J Mar Sci 54:726–737CrossRefGoogle Scholar
  40. Furness RW, Muirhead SJ, Woodburn M (1986) Using bird feathers to measure mercury in the environment: relationships between mercury content and moult. Mar Pollut Bull 17:27–30CrossRefGoogle Scholar
  41. Gasaway WC, Buss IO (1972) Zinc toxicity in the mallard duck. J Wildl Manag 36:1107–1117CrossRefGoogle Scholar
  42. Gochfeld M, Gochfeld DJ, Minton D, Murray BG, Pyle P, Seto N, Smith D, Burger J (1999) Metals in feathers of Bonin petrel, Christmas shearwater, wedge-tailed shearwater, and red-tailed tropicbird in the Hawaian Islands, Northern Pacific. Environ Monit Assess 59:343–358CrossRefGoogle Scholar
  43. Goede AA (1991) The variability and significance of selenium concentrations in shorebird feathers. Environ Monit Assess 18:203–210CrossRefGoogle Scholar
  44. Gulson B, Korsch M, Matisons M, Douglas C, Gillam L, McLaughlin V (2009) Windblown lead carbonate as the main source of lead in blood of children from a seaside community: an example of local birds as “canaries in the mine”. Environ Health Perspect 117:148–154CrossRefGoogle Scholar
  45. Gulson B, Korsch M, Winchester W, Devenish M, Hobbs T, Main C, Smith GC, Rosman K, Howearth L, Burn-Nunes L, Seow J, Oxford C, Yun G, Gillam L, Crisp M (2012) Successful application of lead isotopes in source apportionment, legal proceedings, remediation and monitoring. EnvironRes 112:100–110Google Scholar
  46. Honda K, Marcovecchio JE, Kan S, Tatsukawa R, Ogi H (1990) Metal concentrations in pelagic seabirds from the North Pacific Ocean. Arch Environ Contam Toxicol 19:704–711CrossRefGoogle Scholar
  47. Jones HP et al (2016) Invasive mammal eradication on islands results in substantial conservation gains. Proc Natl Acad Sci 113:4033–4038CrossRefGoogle Scholar
  48. Lavers JL, Bond AL (2016) Ingested plastic as a route for trace metals in Laysan albatross (Phoebastria immutabilis) and Bonin petrel (Pterodroma hypoleuca) from Midway Atoll. Mar Pollut Bull 110:493–500CrossRefGoogle Scholar
  49. Lavers JL, Bond AL, Hutton I (2014) Plastic ingestion by flesh-footed shearwaters (Puffinus carneipes): implications for chick body condition and the accumulation of plastic-derived chemicals. Environ Pollut 187:124–129CrossRefGoogle Scholar
  50. Lehnert K, Ronnenberg K, Weijs L, Covaci A, Das K, Hellwig V, Siebert U (2016) Xenobiotic and immune-relevant molecular biomarkers in harbor seals as proxies for pollutant burden and effects. Arch Environ Contam Toxicol 70:106–120CrossRefGoogle Scholar
  51. Lemly AD (1996) Assessing the toxic threat of selenium to fish and aquatic birds. Environ Monit Assess 43:19–35CrossRefGoogle Scholar
  52. Lyver POB, Aldridge SP, Gormley AM, Gaw S, Webb S, Buxton RT, Jones CJ (2017) Elevated mercury concentrations in the feathers of grey-faced petrels (Pterodroma gouldi) in New Zealand. Mar Pollut Bull 119:195–203CrossRefGoogle Scholar
  53. Markowski M, Kaliński A, Skwarska J, Wawrzyniak J, Bańbura M, Markowski J, Zieliński P, Bańbura J (2013) Avian feathers as bioindicators of the exposure to heavy metal contamination of food. Bull Environ Contam Toxicol 91:302–305CrossRefGoogle Scholar
  54. Marx SK, Kamber BS, McGowan HA, Zawadzki A (2010) Atmospheric pollutants in alpine peat bogs record a detailed chronology of industrial and agricultural development on the Australian continent. Environ Pollut 158:1615–1628CrossRefGoogle Scholar
  55. Monteiro LR, Furness RW (2001) Kinetics, dose−response, and excretion of methylmercury in free-living adult Cory’s shearwaters. Environ Sci Technol Lett 35:739–746CrossRefGoogle Scholar
  56. Mudd GM (2007) An analysis of historic production trends in Australian base metal mining. Ore Geol Rev 32:227–261CrossRefGoogle Scholar
  57. Ohlendorf HM, Heinz GH (2011) Selenium in birds, environmental contaminants in biota: interpreting tissue concentrations. Taylor and Francis, Boca RatonGoogle Scholar
  58. Ohlendorf H, Hoffman D, Saiki M, Aldrich T (1986) Embryonic mortality and abnormalities of aquatic birds: apparent impacts of selenium from irrigation drainwater. Sci Total Environ 52:49–63CrossRefGoogle Scholar
  59. Onley D, Scofield P (2007) Albatrosses, petrels and shearwaters of the world. A&C Black, LondonGoogle Scholar
  60. Paritte JM, Kelly JF (2009) Effect of cleaning regime on stable-isotope ratios of feathers in Japanese quail (Coturnix japonica). Auk 126:165–174CrossRefGoogle Scholar
  61. Penicaud V, Lacoue-Labarthe T, Bustamante P (2017) Metal bioaccumulation and detoxification processes in cephalopods: A review. Environ Res 155:123–133Google Scholar
  62. Phillips RA, Croxall J, Silk JRD, Briggs DR (2007) Foraging ecology of albatrosses and petrels from South Georgia: two decades of insights from tracking technologies. Aquat Conserv Mar Freshwat Ecosyst 17:S6–S21CrossRefGoogle Scholar
  63. R Core Team (2018) R: a language and environment for statistical computing. Version 3.5.1 [computer program]. R Foundation for Statistical Computing, ViennaGoogle Scholar
  64. Rainbow PS (1985) The biology of heavy metals in the sea. Int J Environ Stud 25:195–211CrossRefGoogle Scholar
  65. Rejomon G, Dinesh Kumar PK, Nair M, Muraleedharan KR (2010) Trace metal dynamics in zooplankton from the Bay of Bengal during summer monsoon. Environ Toxicol 25:622–633CrossRefGoogle Scholar
  66. Richir J (2016) Trace elements in marine environments: occurrence, threats and monitoring with special focus on the coastal Mediterranean. J Environ Anal Toxicol 6:1–19CrossRefGoogle Scholar
  67. Ruelas-Inzunza J, Páez-Osuna F (2008) Trophic distribution of Cd, Pb, and Zn in a food web from Altata-Ensenada del Pabellón subtropical lagoon, SE Gulf of California. Arch Environ Contam Toxicol 54:584–596CrossRefGoogle Scholar
  68. Serrano O, Davis G, Lavery PS, Duarte CM, Martinez-Cortizas A, Mateo MA, Masqué P, Arias-Ortiz A, Rozaimi M, Kendrick GA (2016) Reconstruction of centennial-scale fluxes of chemical elements in the Australian coastal environment using seagrass archives. Sci Total Environ 541:883–894CrossRefGoogle Scholar
  69. Signa G, Tramati C, Vizzini S (2013) Contamination by trace metals and their trophic transfer to the biota in a Mediterranean coastal system affected by gull guano. Mar Ecol Prog Ser 479:13–24CrossRefGoogle Scholar
  70. Sunde ML (1972) Zinc requirement for normal feathering of commercial leghorn-type pullets. Poult Sci 51:1316–1322CrossRefGoogle Scholar
  71. Surmacki A, Nowakowski JK (2007) Soil and preen waxes influence the expression of carotenoid-based plumage coloration. Naturwissenschaften 94:829–835CrossRefGoogle Scholar
  72. Talbot V (1983) Lead and other trace metals in the sediments and selected biota of Princess Royal Harbour, Albany, Western Australia. Environ Pollut 5:35–49CrossRefGoogle Scholar
  73. USDI (1998) Guidelines for interpretation of the biological effects of selected constituents in biota, water, and sediment. U.S. Department of the Interior, DenverGoogle Scholar
  74. Weimerskirch H, Ancel A, Caloin M, Zahariev A, Spagiari J, Kersten M, Chastel O (2003) Foraging efficiency and adjustment of energy expenditure in a pelagic seabird provisioning its chick. J Anim Ecol 72:500–508CrossRefGoogle Scholar
  75. Wenzel C, Gabrielsen GW (1995) Trace element accumulation in three seabird species from Hornøya, Norway. Arch Environ Contam Toxicol 29:198–206CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute for Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia
  2. 2.School of ScienceRMIT UniversityBundooraAustralia
  3. 3.Ocean Sciences DepartmentUniversity of CaliforniaSanta CruzUSA
  4. 4.Lord Howe Island MuseumLord Howe IslandAustralia
  5. 5.RSPB Centre for Conservation Science, Royal Society for the Protection of Birds, The LodgeSandyUK
  6. 6.Bird Group, Department of Life Sciences, The Natural History MuseumTringUK

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