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A Global Overview of Exposure Levels and Biological Effects of Trace Elements in Penguins

  • Winfred Espejo
  • José E. CelisEmail author
  • Daniel GonzÃlez-Acuña
  • Andiranel Banegas
  • Ricardo Barra
  • Gustavo Chiang
Chapter
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 245)

Abstract

Trace elements are chemical contaminants that can be present almost anywhere on the planet. The study of trace elements in biotic matrices is a topic of great relevance for the implications that it can have on wildlife and human health. Penguins are very useful, since they live exclusively in the Southern Hemisphere and represent about 90% of the biomass of birds of the Southern Ocean. The levels of trace elements (dry weight) in different biotic matrices of penguins were reviewed here. Maps of trace element records in penguins were included. Data on exposure and effects of trace elements in penguins were collected from the literature. The most reported trace elements in penguins are aluminum, arsenic, cadmium, lead, mercury, copper, zinc, and manganese. Trace elements have been measured in 11 of the 18 species of penguins. The most studied biotic matrices are feathers and excreta. Most of the studies have been performed in Antarctica and subantarctic Islands. Little is known about the interaction among metals, which could provide better knowledge about certain mechanisms of detoxification in penguins. Future studies of trace elements in penguins must incorporate other metals such as vanadium, cobalt, nickel, and chromium. Data of metals in the species such as Eudyptes pachyrhynchus, Eudyptes moseleyi, Eudyptes sclateri, Eudyptes robustus, Eudyptes schlegeli, Spheniscus demersus, Spheniscus mendiculus, and Megadyptes antipodes are urged. It is important to correlate levels of metals in different biotic matrices with the effects on different species and in different geographic locations.

Notes

Acknowledgments

Winfred E. Espejo is a graduate student at the Universidad de Concepción, Chile, who is sponsored by the CONICYT-Chile to pursue PhD research. This study was financially supported by the project INACH RG 09-14 (J. Celis), INACH T31-11 (G. Chiang), and FONDAP CRHIAM 15 13 0015 (R. Barra). Thanks also are given to project 216.153.025-1.0 of the Research Division of the Universidad de Concepción. Many thanks are also given to Dr. Evelyn Habit, Liseth Chaura, and peer reviewers for their useful suggestions. Finally, the authors also thank Diane Haughney for the English revision.

References

  1. Agusa T, Matsumoto T, Ikemoto T, Anan Y, Kubota R, Yasunaga G, Kunito T, Tanabe S, Ogi H, Shibata Y (2005) Body distribution of trace elements in black-tailed gulls from Rishiri island, Japan: age-dependent accumulation and transfer to feathers and eggs. Environ Toxicol Chem 24:2107–2120CrossRefGoogle Scholar
  2. Anan Y, Kunito T, Watanabe I, Sakai H, Tanabe S (2001) Trace element accumulation in hawksbill turtle (Eretmochelys imbricata) and green turtle (Chelonia mydas) from Yaeyama Islands, Japan. Environ Toxicol Chem 20:2802–2814CrossRefGoogle Scholar
  3. Ancora S, Volpi V, Olmastroni S, Focardi S, Leonzio C (2002) Assumption and elimination of trace elements in Adélie penguins from Antarctica: a preliminary study. Mar Environ Res 54:341–344CrossRefGoogle Scholar
  4. Arcos JM, Ruiz X, Bearhop S, Furness RW (2002) Mercury levels in seabirds and their fish prey at the Ebro Delta (NW Mediterranean): the role of trawler discards as a source of contamination. Mar Ecol Prog Ser 232:281–290CrossRefGoogle Scholar
  5. ATSDR (2004) Toxicological profile for copper. Agency for Toxic Substances and Disease Registry US Department of Health and Human Services, Public Health Service, Atlanta, GA. http://www.atsdr.cdc.gov/ToxProfiles/tp132.pdf. Accessed 19 May 2016
  6. ATSDR (2007) Toxicological profile for arsenic. Agency for Toxic Substances and Disease Registry US Department of Health and Human Services, Public Health Service, Atlanta, GA. http://www.atsdr.cdc.gov/toxprofiles/tp2.pdf. Accessed 19 May 2016
  7. ATSDR (2008) Toxicological profile for manganese. Agency for Toxic Substances and Disease Registry US Department of Health and Human Services, Public Health Service, Atlanta, GA. http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=102&tid=23. Accessed 19 May 2016
  8. Ballatori N (2002) Transport of toxic metals by molecular mimicry. Environ Health Perspect 110:689–694CrossRefGoogle Scholar
  9. Barbieri E, de Andrade PE, Filippini A, Souza dos Santos I, Borges CA (2010) Assessment of trace metal concentration in feathers of seabird (Larus dominicanus) sampled in the Florianópolis, SC, Brazilian coast. Environ Monit Assess 169:631–638CrossRefGoogle Scholar
  10. Barbosa A, De Mas E, Benzal J, Diaz J, Motas M, Jerez S, Pertierra L, Benayas J, Justel A, Lauzurica P, Garcia-Peña F, Serrano T (2013) Pollution and physiological variability in gentoo penguins at two rookeries with different levels of human visitation. Antarct Sci 25:329–338CrossRefGoogle Scholar
  11. Bargagli R (2001) Trace metals in Antarctic organisms and the development of circumpolar biomonitoring networks. Rev Environ Contam Toxicol 171:53–110CrossRefGoogle Scholar
  12. Bargagli R (2008) Environmental contamination in Antarctic ecosystems. Sci Total Environ 400:212–226CrossRefGoogle Scholar
  13. Bargagli R, Monaci F, SÃnchez-HernÃndez J, Cateni D (1998) Biomagnification of mercury in an Antarctic marine coastal food web. Mar Ecol Prog Ser 169:65–76CrossRefGoogle Scholar
  14. Barjaktarovic L, Elliott JE, Scheuhammer AM (2002) Metal and metallothionein concentrations in scoter (Melanitta spp.) from the Pacific northwest of Canada, 1989–1994. Arch Environ Contam Toxicol 43:486–491CrossRefGoogle Scholar
  15. Becker PH, GonzÃlez-Solís J, Behrends B, Croxall J (2002) Feather mercury levels in seabirds at South Georgia: influence of trophic position, sex and age. Mar Ecol Prog Ser 243:261–269CrossRefGoogle Scholar
  16. Beyer WN, Heinz GH, Redmon-Norwood AW (1996) Environmental contaminants in wildlife: interpreting tissue concentrations. Lewis, Boca Raton, FL, p 512Google Scholar
  17. Beyer NW, Spalding M, Morrison D (1997) Mercury concentrations in feathers of wading birds from Florida. Ambio 26:97–100Google Scholar
  18. Beyer WN, Franson JC, Locke LN, Stroud RK, Sileo L (1998) Retrospective study of the diagnostic criteria in a lead-poisoning survey of waterfowl. Arch Environ Contam Toxicol 35:506–512CrossRefGoogle Scholar
  19. Boersma PD (2008) Penguins as marine sentinels. Bioscience 58:597–607CrossRefGoogle Scholar
  20. Brasso RL, Polito MJ (2013) Trophic calculations reveal the mechanism of population-level variation in mercury concentrations between marine ecosystems: case studies of two polar seabirds. Mar Pollut Bull 75:244–249CrossRefGoogle Scholar
  21. Brasso RL, Polito MJ, Emslie SD (2014) Multi-tissue analyses reveal limited inter-annual and seasonal variation in mercury exposure in an Antarctic penguin community. Ecotoxicology 23:1494–1504CrossRefGoogle Scholar
  22. Braune BM, Gaston AJ, Hobson KA, Gilchrist HG, Mallory ML (2014) Changes in food web structure alter trends of mercury uptake at two seabird colonies in the Canadian Arctic. Environ Sci Technol 48:13246–13252CrossRefGoogle Scholar
  23. Bryan GW, Langston WJ (1992) Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review. Environ Pollut 76:89–131CrossRefGoogle Scholar
  24. Burger J (2008) Assessment and management of risk to wildlife from cadmium. Sci Total Environ 389:37–45CrossRefGoogle Scholar
  25. Burger J, Gochfeld M (1997) Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ Res 75:160–172CrossRefGoogle Scholar
  26. Burger J, Gochfeld M (2000a) Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health B Crit Rev 3:59–78CrossRefGoogle Scholar
  27. Burger J, Gochfeld M (2000b) Metal levels in feathers of 12 species of seabirds from midway atoll in the northern Pacific Ocean. Sci Total Environ 257:37–52CrossRefGoogle Scholar
  28. Burger J, Gochfeld M, Sullivan K, Irons D, McKnight A (2008) Arsenic, cadmium, chromium, lead, manganese, mercury, and selenium in feathers of black-legged kittiwake (Rissa tridactyla) and black oystercatcher (Haematopus bachmani) from Prince William sound, Alaska. Sci Total Environ 398:20–25CrossRefGoogle Scholar
  29. Burger J, Tsipoura N, Newhouse M, Jeitner C, Gochfeld M, Mizrahi D (2011) Lead, mercury, cadmium, chromium, and arsenic levels in eggs, feathers, and tissues of Canada geese of the New Jersey meadowlands. Environ Res 111:775–784CrossRefGoogle Scholar
  30. Bustamante P, Bocher P, Cherel Y, Miramand P, Caurant F (2003) Distribution of trace elements in the tissues of benthic and pelagic fish from the Kerguelen Islands. Sci Total Environ 313:25–39CrossRefGoogle Scholar
  31. Byrns MC, Penning TM (2011) Environmental toxicology. Carcinogens and heavy metals. In: Brunton L, Chabner B, Knollman B (eds) The pharmacological basis of therapeutics. McGraw Hill, New York, pp 1853–1878Google Scholar
  32. Calle P, Alvarado O, Monserrate L, Cevallos JM, Calle N, Alava JJ (2015) Mercury accumulation in sediments and seabird feathers from the Antarctic peninsula. Mar Pollut Bull 91:410–417CrossRefGoogle Scholar
  33. Campbell LM, Norstrom RJ, Hobson KA, Muir D, Backus S, Fisk AT (2005) Mercury and other trace elements in a pelagic Arctic marine food web (Northwater polynya, Baffin Bay). Sci Total Environ 351-352:247–263CrossRefGoogle Scholar
  34. Carlini AR, Coria NR, Santos MM, Negrete J, Juares MA, Daneri GA (2009) Responses of Pygoscelis adeliae and P. papua populations to environmental changes at Isla 25 de Mayo (king George Island). Polar Biol 32:1427–1433CrossRefGoogle Scholar
  35. Carravieri A, Bustamante P, Churlaud C, Cherel Y (2013) Penguins as bioindicators of mercury contamination in the Southern Ocean: birds from the Kerguelen Islands as a case study. Sci Total Environ 454-455:141–148CrossRefGoogle Scholar
  36. 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
  37. Carravieri A, Cherel Y, Jaeger A, Churlaud C (2016) Penguins as bioindicators of mercury contamination in the southern Indian Ocean: geographical and temporal tends. Environ Pollut 213:195–205CrossRefGoogle Scholar
  38. Casini S, Fossi M, Gavilan J, Barra R, Parra O, Leonzio C, Focardi S (2001) Porphyrin levels in excreta of seabirds of the Chilean coasts as nondestructive biomarker of exposure to environmental pollutants. Arch Environ Contam Toxicol 4:65–72CrossRefGoogle Scholar
  39. Casini S, Fossi M, Leonzio C, Renzoni A (2003) Review: porphyrins as biomarkers for hazard assessment of bird populations: destructive and non-destructive use. Ecotoxicology 12:297–305CrossRefGoogle Scholar
  40. Celis J, Jara S, GonzÃlez-Acuña D, Barra R, Espejo W (2012) A preliminary study of trace metals and porphyrins in excreta of gentoo penguins (Pygoscelis papua) at two locations of the Antarctic peninsula. Arch Med Vet 44:311–316CrossRefGoogle Scholar
  41. Celis JE, Espejo W, GonzÃlez-Acuña D, Jara S, Barra R (2014) Assessment of trace metals and porphyrins in excreta of Humboldt penguins (Spheniscus humboldti) in different locations of the northern coast of Chile. Environ Monit Assess 186:1815–1824CrossRefGoogle Scholar
  42. Celis JE, Espejo W, Barra R, Gonzalez-Acuña D, Gonzalez F, Jara S (2015a) Assessment of trace metals in droppings of Adélie penguins (Pygoscelis adeliae) from different locations of the Antarctic peninsula area. Adv Polar Sci 26:1–7Google Scholar
  43. Celis JE, Barra R, Espejo W, GonzÃlez-Acuña D, Jara S (2015b) Trace element concentrations in biotic matrices of gentoo penguins (Pygoscelis papua) and coastal soils from different locations of the Antarctic peninsula. Water Air Soil Pollut 226:1–12CrossRefGoogle Scholar
  44. Chen CY, Serrell N, Evers DC, Fleishman BJ, Lambert KF, Weiss J, Mason RP, Bank MS (2008) Meeting report: methylmercury in marine ecosystems—from sources to seafood consumers. Environ Health Perspect 116:1706–1712CrossRefGoogle Scholar
  45. Cifuentes JM, Becker PH, Sommer U, Pacheco P, Schlatter R (2003) Seabird eggs as bioindicators of chemical contamination in Chile. Environ Pollut 126:123–137CrossRefGoogle Scholar
  46. Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted bray–Curtis coefficient for denuded assemblages. J Exp Mar Biol Ecol 330:55–80CrossRefGoogle Scholar
  47. Cooper J, Crawford RJM, De Villiers M, Dyer BM, Hofmeyr GJG, Jonker A (2009) Disease outbreaks among penguins at sub-Antarctic Marion Island: a conservation concern. Mar Ornithol 37:193–196Google Scholar
  48. Croxall JP, Prince PA, Reid K (1997) Dietary segregation of krill eating South Georgia seabirds. J Zool 242:531–556CrossRefGoogle Scholar
  49. Custer T, Custer C, Eichhorst B, Warburton D (2007) Selenium and metal concentrations in waterbird eggs and chicks at Agassiz National Wildlife Refuge, Minnesota. Arch Environ Contam Toxicol 53:103–109CrossRefGoogle Scholar
  50. Daso AP, Okonkwo JO, Jansen R, Brandao JD, Kotzé A (2015) Mercury concentrations in eggshells of the southern ground-hornbill (Bucorvus leadbeateri) and Wattled crane (Bugeranus carunculatus) in South Africa. Ecotoxicol Environ Saf 114:61–66CrossRefGoogle Scholar
  51. Dauwe T, Bervoets L, Blust R, Pinxten R, Eens M (2000) Can excrement and feathers of nestling songbirds be used as biomonitors for heavy metal pollution? Arch Environ Contam Toxicol 39:541–546CrossRefGoogle Scholar
  52. Dauwe T, Janssens E, Bervoets L, Blust R, Eens M (2005) Heavy-metal concentrations in female laying great tits (Parus major) and their clutches. Arch Environ Contam Toxicol 49:249–256CrossRefGoogle Scholar
  53. De Matos R (2008) Calcium metabolism in birds. Vet Clin Exot Anim 11:59–82CrossRefGoogle Scholar
  54. De Matteis F, Lim CK (1994) Porphyrins as nondestructive indicators of exposure to environmental pollutants. In: Fossi MC, Leoncio C (eds) Nondestructive biomarkers in vertebrates. Lewis, Boca Raton, FL, pp 93–128Google Scholar
  55. De Moreno JEA, Gerpe MS, Moreno VJ, Vodopivez C (1997) Heavy metals in Antarctic organisms. Polar Biol 17:131–140CrossRefGoogle Scholar
  56. Debacker V, Jauniaux T, Coignoul F, Bouquegneau JM (2000) Heavy metals contamination and body condition of wintering guillemots (Uria Aalge) at the Belgian coast from 1993 to 1998. Environ Res 84(3):310–317CrossRefGoogle Scholar
  57. Deheyn DD, Gendreau P, Baldwin RJ, Latz MI (2005) Evidence for enhanced bioavailability of trace elements in the marine ecosystem of Deception Island, a volcano in Antarctica. Mar Environ Res 60:1–33CrossRefGoogle Scholar
  58. Dehn L, Follmann E, Thomas D, Sheffield G, Rosa C, Duffy L, O'Hara T (2006) Trophic relationships in an Arctic food web and implications for trace metal transfer. Sci Total Environ 362:103–123CrossRefGoogle Scholar
  59. Del Hoyo J, Elliott A, Sargatal J (1992) Handbook of the birds of the world. Volume 1: ostrich to ducks. Lynx Edicions. Barcelona, Spain, p 696Google Scholar
  60. Dos Santos IR, Silva-Filho EV, Schaefer CE, Albuquerque-Filho MR, Campos LS (2005) Heavy metal contamination in coastal sediments and soils near the Brazilian Antarctic Station, king George Island. Mar Pollut Bull 50:185–194CrossRefGoogle Scholar
  61. Eisler R (1985) Selenium hazards to fish, wildlife and invertebrates. A synoptic review. U.S. Fish and Wildlife Service, Washington DC. https://nrm.dfg.ca.gov/FileHandler.ashx?DocumentID=7297. Accessed 31 May 2016
  62. Eisler R (1987) Mercury hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish and WildlifeService, Washington DC. https://www.pwrc.usgs.gov/eisler/CHR_10_Mercury.pdf
  63. Eisler R (1988) Lead hazards to fish, wildlife, and invertebrates. A synoptic review. U.S. Fish and Wildlife Service, Washington DC. https://www.pwrc.usgs.gov/eisler/CHR_14_Lead.pdf. Accessed 31 May 2016
  64. Eisler R (1993) Zinc hazards to fish, wildlife and invertebrates. A synoptic review. U.S. Fish and Wildlife Service, Washington DC. https://www.pwrc.usgs.gov/eisler/CHR_26_Zinc.pdf. Accessed 31 May 2016
  65. Eisler R (1998) Copper hazards to fish, wildlife, and invertebrates. A synoptic review. U.S. Fish and Wildlife Service, Washington DC. https://www.pwrc.usgs.gov/eisler/CHR_33_Copper.pdf. Accessed 31 May 2016
  66. Elliot 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
  67. Erikson KM, Aschner M (2003) Manganese neurotoxicity and glutamate-GABA interaction. Neurochem Int 43:475–480CrossRefGoogle Scholar
  68. Espejo W, Celis J, GonzÃlez-Acuña D, Jara S, Barra R (2014) Concentration of trace metals in excrements of two species of penguins from different locations of the Antarctic peninsula. Polar Biol 37:675–683CrossRefGoogle Scholar
  69. Evers DC, Savoy LJ, DeSorbo CR, Yates DE, Hanson W, Taylor KM, Siegel LS, Cooley JH Jr, Bank MS, Major A, Munney K, Mower BF, Vogel HS, Schoch N, Pokras M, Goodale MW, Fair J (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17:69–81CrossRefGoogle Scholar
  70. Falkowska L, Reindl AR, Szumilo E, Kwaśniak J, Staniszewska M, Bełdowska M, Lewandowska A, Krause I (2013) Mercury and chlorinated pesticides on the highest level of the food web as exemplified by herring from the southern Baltic and African penguins from the zoo. Water Air Soil Pollut 224:1549CrossRefGoogle Scholar
  71. Fimreite N (1974) Mercury contamination of aquatic birds in northwestern Ontario. J Wildl Manag 38:120–131CrossRefGoogle Scholar
  72. 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
  73. Fitzgerald WF, Lamborg CH, Hammerschmidt CR (2007) Marine biogeochemical cycling of mercury. Chem Rev 107:641–662CrossRefGoogle Scholar
  74. Franson JC (1996) Interpretation of tissue lead residues in birds other than waterfowl. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife. Interpreting tissue concentrations. Lewis, Boca Raton, FL, pp 264–279Google Scholar
  75. Franson JC, Hollmén TE, Flint PL, Grand JB, Lanctot RB (2003) Contaminants in molting long-tailed ducks and nesting common eiders in the Beaufort Sea. Mar Pollut Bull 45:504–513Google Scholar
  76. Franson JC, Hoffman DJ, Wells-Berlin A, Perry MC, Shearn-Bochsler V, Finley DL, Flint PL, Hollmén T (2007) Effects of dietary selenium on tissue concentrations, pathology, oxidative stress, and immune function in common eiders (Somateria mollissima). J Toxicol Environ Health A 70:861–874CrossRefGoogle Scholar
  77. Frias JE, Gil MN, Esteves JL, Borboroglu PG, Kane OJ, Smith JR, Boersma PD (2012) Mercury levels in feathers of Magellanic penguins. Mar Pollut Bull 64:1265–1269CrossRefGoogle Scholar
  78. Furness RW (1996) Cadmium in birds. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife. Interpreting tissue concentrations. Lewis, Boca Raton, FL, pp 389–404Google Scholar
  79. Furness RW, Muirhead SJ, Woodburn M (1986) Using bird feathers to measure mercury in the environment: relationships between mercury content and molt. Mar Pollut Bull 17:27–30CrossRefGoogle Scholar
  80. García P, Boersma PD (2013) Penguins: natural history and conservation. University of Washington Press, Seattle & London, p 328Google Scholar
  81. Gasparik J, Vladarova D, Capcarova M, Smehyl P, Slamecka J, Garaj P, Stawarz R, Massanyi P (2010) Concentration of lead, cadmium, mercury and arsenic in leg skeletal muscles of three species of wild birds. J Environ Sci Health A 45:818–823CrossRefGoogle Scholar
  82. Gibbs PJ (1995) Heavy metal and organochlorine concentrations in tissues of the little penguin Eudyptula minor. In: Dann P, Norman I, Reilly P (eds) The penguins. Surrey Beatty & Sons, Australia, pp 393–419Google Scholar
  83. Gilani SH, Alibhai Y (1990) Teratogenicity of metals to chick embryos. Toxicol Environ Health 30:23–31CrossRefGoogle Scholar
  84. Gochfeld M (1997) Spatial patterns in a bioindicator: heavy metal and selenium concentration in eggs of herring gulls (Larus argentatus) in the New York bight. Arch Environ Contam Toxicol 33:63–70CrossRefGoogle Scholar
  85. Gochfeld M, Belant JL, Shukla T, Benson T, Burger J (1996) Heavy metals in laughing gulls: gender, age and tissue differences. Environ Toxicol Chem 15:2275–2283CrossRefGoogle Scholar
  86. Goutner V, Furness R, Papakonstantinou K (2000) Mercury in feathers of Audouin’s Gull (Larus audouinii) chicks from northeastern Mediterranean colonies. Arch Environ Contam Toxicol 39:200–204CrossRefGoogle Scholar
  87. Goutte A, Barbraud C, Herzke D, Bustamante P, Angelier F, Tartu S, Clément-Chastel C, Moe B, Bech C, Gabrielsen GW, Bustnes JO, Chastel O (2015) Survival rate and breeding outputs in a high Arctic seabird exposed to legacy persistent organic pollutants and mercury. Environ Pollut 200:1–9CrossRefGoogle Scholar
  88. Goyer RA (1997) Toxic and essential metal interactions. Annu Rev Nutr 17:37–50CrossRefGoogle Scholar
  89. Hoffman DJ (2002) Role of selenium toxicity and oxidative stress in aquatic birds. Aquat Toxicol 57:11–26CrossRefGoogle Scholar
  90. Honda K, Yamamoto Y, Hidaka H, Tatsukawa R (1986) Heavy metal accumulation in Adélie penguin, Pygoscelis adeliae, and their variations with the reproductive process. Mem Natl Inst Polar Res 40:443–453Google Scholar
  91. 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
  92. Iavicoli I, Fontana L, Bergamaschi A (2009) The effects of metals as endocrine disruptors. J Toxicol Environ Health B 12:206–223CrossRefGoogle Scholar
  93. Ikemoto T, Kunito T, Tanaka H, Baba N, Miyazaki N, Tanabe S (2004) Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, copper, zinc, and cadmium in liver. Arch Environ Contam Toxicol 47:402–413CrossRefGoogle Scholar
  94. Jerez S, Motas M, Palacios MJ, Valera F, Cuervo JJ, Barbosa A (2011) Concentration of trace elements in feathers of three Antarctic penguins: geographical and interspecific differences. Environ Pollut 159:2412–2419CrossRefGoogle Scholar
  95. Jerez S, Motas M, Benzal J, Diaz J, Vidal V, D’Amico V, Barbosa A (2013a) Distribution of metals and trace elements in adult and juvenile penguins from the Antarctic peninsula area. Environ Sci Pollut R 20:3300–3311CrossRefGoogle Scholar
  96. Jerez S, Motas M, Benzal J, Diaz J, Barbosa A (2013b) Monitoring trace elements in Antarctic penguin chicks from south Shetland Islands, Antarctica. Mar Pollut Bull 69:67–75CrossRefGoogle Scholar
  97. Jin S, Seo S, Shin Y, Bing K, Kang T, Paek W, Lee D (2012) Heavy metal accumulations of 4 species of Anseriformes in Korea. J Korean Nat 5:345–349CrossRefGoogle Scholar
  98. Kaur N, Dhanju CK (2013) Heavy metals concentration in excreta of free living wild birds as indicator of environmental contamination. Bioscan 8:1089–1093Google Scholar
  99. Kehrig HA, Hauser-Davis RA, Seixas TG, Fillmann G (2015) Trace-elements, methylmercury and metallothionein levels in Magellanic penguin (Spheniscus magellanicus) found stranded on the southern Brazilian coast. Mar Pollut Bull 96:450–455CrossRefGoogle Scholar
  100. Khan A, Hussain H, Sattar A, Khan M, Abbas R (2014) Toxico-pathological aspects of arsenic in birds and mammals: a review. Int J Agric Biol 16:1213–1224Google Scholar
  101. Kim J, Koo T (2007) Heavy metal concentrations in diet and livers of black-crowned night heron Nycticorax nycticorax and grey heron Ardea cinerea chicks from Pyeongtaek, Korea. Ecotoxicology 16:411–416CrossRefGoogle Scholar
  102. Kim J, Oh J (2014a) Trace element concentrations in eggshells and egg contents of black-tailed gull (Larus crassirostris) from Korea. Ecotoxicology 23:1147–1152CrossRefGoogle Scholar
  103. Kim J, Oh J (2014b) Relationships of metals between feathers and diets of black-tailed gull (Larus crassirostris) chicks. Bull Environ Contam Toxicol 92:265–269CrossRefGoogle Scholar
  104. Kim J, Oh J (2014c) Heavy metal concentrations in black-tailed gull (Larus crassirostris) chicks, Korea. Chemosphere 112:370–376CrossRefGoogle Scholar
  105. Kim EY, Murakami T, Saeki K, Tatsukawa R (1996) Mercury levels and its chemical form in tissues and organs of seabirds. Arch Environ Contam Toxicol 30:259–266CrossRefGoogle Scholar
  106. Kim EY, Goto R, Tanabe S, Tanaka H, Tatsukawa R (1998) Distribution of 14 elements in tissues and organs of oceanic seabirds. Arch Environ Contam Toxicol 35:638–645CrossRefGoogle Scholar
  107. Kim M, Park K, Park J, Kwak I (2013) Heavy metal contamination and metallothionein mRNA in blood and feathers of black-tailed gulls (Larus crassirostris) from South Korea. Environ Monit Assess 185:2221–2230CrossRefGoogle Scholar
  108. Kler T, Vashishat N, Kumar M (2014) Heavy metals concentration in excreta of avian species from Ludhiana district. Int J Adv Res 2:873–879Google Scholar
  109. Lalancette A, Morin Y, Measures L, Fournier M (2003) Contrasting changes of sensitivity by lymphocytes and neutrophils to mercury in developing grey seals. Dev Comp Immunol 27:735–747CrossRefGoogle Scholar
  110. Larison JR, Likens GE, Fitzpatrick JW, Crock JG (2000) Cadmium toxicity among wildlife in the Colorado Rocky Mountains. Nature 406:181–183CrossRefGoogle Scholar
  111. Lavoie R, Jardine T, Chumchal M, Kidd K, Campbell L (2013) Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis. Environ Sci Technol 47:13385–13394CrossRefGoogle Scholar
  112. Lebedeva NV (1997) Accumulation of heavy metals by birds in the southwest of Russia. Russ J Ecol 28:41–46Google Scholar
  113. Lee DP (1996) Relationship of heavy metal level in birds. Bull Kor Inst Orni 5:59–67Google Scholar
  114. Lemley AD (1993) Guidelines for evaluating selenium data form aquatic monitoring and assessment studies. Environ Monit Assess 28:83–100CrossRefGoogle Scholar
  115. Lescroël A, Ridoux V, Bost CA (2004) Spatial and temporal variation in the diet of the gentoo penguin (Pygoscelis papua) at Kerguelen Islands. Polar Biol 27:206–216CrossRefGoogle Scholar
  116. Lim CK (1991) Porphyrins. In: Hanai T (ed) Liquid chromatography in biomedical analysis. Elsevier, Amsterdam, pp 209–229Google Scholar
  117. Lock JW, Thompson DR, Furness RW (1992) Metal concentrations in seabirds of the New Zealand region. Environ Pollut 75:289–300CrossRefGoogle Scholar
  118. Lucia M, André JM, Gontier K, Diot N, Veiga J, Davail S (2010) Trace element concentrations (mercury, cadmium, copper, zinc, lead, aluminum, nickel, arsenic, and selenium) in some aquatic birds of the Southwest Atlantic Coast of France. Arch Environ Contam Toxicol 58:844–853CrossRefGoogle Scholar
  119. Majer A, Petti M, Corbisier T, Ribeiro A, Theophilo C, de Lima FP, Figueira R (2014) Bioaccumulation of potentially toxic trace elements in benthic organisms of Admiralty Bay (king George Island, Antarctica). Mar Pollut Bull 79:321–325CrossRefGoogle Scholar
  120. Malinga M, Szefer P, Gabrielsen G (2010) Age, sex and spatial dependent variations in heavy metals levels in the glaucous gulls (Larus hyperboreus) from the Bjørnøya and Jan Mayen, Arctic. Environ Monit Assess 169:407–416CrossRefGoogle Scholar
  121. Mansouri B, Babaei H, Hoshyari E (2012) Heavy metal contamination in feathers of western reef heron (Egretta gularis) and Siberian gull (Larus heuglini) from hara biosphere reserve of southern Iran. Environ Monit Assess 184:6139–6145CrossRefGoogle Scholar
  122. Martinez-Haro M, Taggart M, Mateo R (2010) Pb-al relationships in waterfowl feces discriminate between sources of Pb exposure. Environ Pollut 158:2485–2489CrossRefGoogle Scholar
  123. Mateo R, Lacorte S, Taggart M (2016) An overview of recent trends in wildlife ecotoxicology. Curr Trends Wildlife Res 1:125–150CrossRefGoogle Scholar
  124. Mathews T, Fisher N (2008) Trophic transfer of seven trace metals in a four-step marine food chain. Mar Ecol Prog Ser 367:23–33CrossRefGoogle Scholar
  125. Metcheva R, Yurukova L, Teodorova S, Nikolova E (2006) The penguin feathers as bioindicator of Antarctica environmental state. Sci Total Environ 362:259–265CrossRefGoogle Scholar
  126. Metcheva R, Yurukova L, Bezrukov V, Beltcheva M, Yankov Y, Dimitrov K (2010) Trace and toxic elements accumulation in food chain representatives at Livingston Island (Antarctica). Int J biol 2:155CrossRefGoogle Scholar
  127. Metcheva R, Yurukova L, Teodorova SE (2011) Biogenic and toxic elements in feathers, eggs, and excreta of gentoo penguin (Pygoscelis papua ellsworthii) in the Antarctic. Environ Monit Assess 182:571–585CrossRefGoogle Scholar
  128. Monteiro LR, Furness RW (2001) Kinetics, dose-response, and excretion of methylmercury in free-living adult Cory’s shearwaters. Environ Sci Technol 35:739–746CrossRefGoogle Scholar
  129. Morera M, Sanpera C, Crespo S, Jover L, Ruiz X (1997) Inter- and intraclutch variability in heavy metals and selenium levels in Audouin’s gull eggs from the Ebro Delta, Spain. Arch Environ Contam Toxicol 33:71–75CrossRefGoogle Scholar
  130. Nayak P (2002) Aluminum: impacts and disease. Environ Res 89:101–115CrossRefGoogle Scholar
  131. Neff JM (1997) Ecotoxicology of arsenic in the marine environment. Environ Toxicol Chem 16:917–927Google Scholar
  132. Newman MC (2015) Fundamentals of ecotoxicology: the science of pollution. CRC Press, Boca Raton, FL, p 680Google Scholar
  133. Nordberg M, Nordberg GF (2016) Trace element research-historical and future aspects. J Trace Elem Med Biol 38:46–52CrossRefGoogle Scholar
  134. Norheim G, Borch-Iohnsen B (1990) Chemical and morphological studies of liver from eider (Somateria mollissima) in Svalbard with special reference to the distribution of copper. J Comp Pathol 102:457–466CrossRefGoogle Scholar
  135. Nygard T, Lie E, Rov N, Steinnes E (2001) Metal dynamics in an Antarctic food chain. Mar Pollut Bull 42:598–602CrossRefGoogle Scholar
  136. Nyholm NE (1981) Evidence of involvement of aluminum in causation of defective formation of eggshells and of impaired breeding in wild passerine birds. Environ Res 26:363–371CrossRefGoogle Scholar
  137. O’Flaherty EJ (1998) Physiologically based models of metal kinetics. Crit Rev Toxicol 28:271–317CrossRefGoogle Scholar
  138. Ochoa-Acuña H, Sepúlveda MS, Gross TS (2002) Mercury in feathers from Chilean birds: influence of location: feeding strategy, and taxonomic affiliation. Mar Pollut Bull 44:340–345CrossRefGoogle Scholar
  139. Ohlendorf HM, Kilness AW, Simmons JL, Stroud RK, Hoffman DJ, Moore JF (1988) Selenium toxicosis in wild aquatic birds. Toxicol Environ Health 24:67–92CrossRefGoogle Scholar
  140. Orłowski G, Polechoński R, Dobicki W, Zawada Z (2007) Heavy metal concentrations in the tissues of the black-headed gull Larus ridibundus L. nesting in the dam reservoir in south-western Poland. Pol J Ecol 55:777–787Google Scholar
  141. Outridge PM, Scheuhammer AM (1993) Bioaccumulation and toxicology of chromium: implications for wildlife. Rev Environ Contam Toxicol 130:31–77Google Scholar
  142. Parslow JLF, Jefferies DJ, Hanson HM (1973) Gannet mortality incidents in 1972. Mar Pollut Bull 4:41–43CrossRefGoogle Scholar
  143. Pedro S, Xavier JC, Tavares S, Trathan PN, Ratcliffe N, Paiva VH, Medeiros R, Pereira E, Pardal M (2015) Feathers as a tool to assess mercury contamination in gentoo penguins: variations at the individual level. PLoS One 10:e0137622. doi: 10.1371/journal.pone.0137622 CrossRefGoogle Scholar
  144. Pérez-López M, Cid-GalÃn F, HernÃndez-Moreno D, Oropesa-Jiménez AL, López-Beceiro A, Fidalgo-Álvarez LE, Soler-Rodríguez F (2005) Contenido de metales pesados en hígado y plumas de aves marinas afectadas por el accidente del “Prestige” en la costa de Galicia. Rev Toxicol 22:191–199. (in Spanish)Google Scholar
  145. Prashanth L, Kattapagari KK, Chitturi RT, Baddam VR, Prasad LK (2016) A review on role of essential trace elements in health and disease. J NTR Univ Health Sci 4:75–85Google Scholar
  146. Raidal SR, Shearer PL, Cannell BL, RJDB N (2006) Micromelia in little penguins (Eudyptula minor). J Avian Med Surg 20:258–262CrossRefGoogle Scholar
  147. Rattner BA, Golden NH, Toschik PC, McGowan PC, Custer TW (2008) Concentrations of metals in blood and feathers of nestling ospreys (Pandion haliaetus) in Chesapeake and Delaware bays. Arch Environ Contam Toxicol 54:114–122CrossRefGoogle Scholar
  148. Ribeiro AR, Eira C, Torres J, Mendes P, Miquel J, Soares AMVM, Vingada J (2009) Toxic element concentrations in the razorbill Alca torda (Charadriiformes, Alcidae) in Portugal. Arch Environ Contam Toxicol 56:588–595CrossRefGoogle Scholar
  149. Rodrigue J, Champoux L, Leclair D, Duchesne JF (2007) Cadmium concentrations in tissues of willow ptarmigan (Lagopus lagopus) and rock ptarmigan (Lagopus muta) in Nunavik, northern Québec. Environ Pollut 147:642–647CrossRefGoogle Scholar
  150. Roth JA (2006) Homeostatic and toxic mechanisms regulating manganese uptake, retention, and elimination. Biol Res 39:45–57CrossRefGoogle Scholar
  151. Rothschild RFN, Duffy LK (2005) Mercury concentrations in muscle, brain and bone of western Alaskan waterfowl. Sci Total Environ 349:277–283CrossRefGoogle Scholar
  152. Sagerup K, Savinov V, Savinova T, Kuklin V, Muir D, Gabrielsen G (2009) Persistent organic pollutants, heavy metals and parasites in the glaucous gull (Larus hyperboreus) on Spitsbergen. Environ Pollut 157:2282–2290CrossRefGoogle Scholar
  153. Sanchez-Hernandez JC (2000) Trace element contamination in Antarctic ecosystems. Rev Environ Toxicol 166:83–127Google Scholar
  154. SÃnchez-Virosta P, Espína S, García-FernÃndez AJ, Eeva T (2015) A review on exposure and effects of arsenic in passerine birds. Sci Total Environ 512-513:506–525CrossRefGoogle Scholar
  155. Santos IR, Silva-Filho EV, Schaefer C, Maria S, Silva CA, Gomes V, Passos MJ, Van Ngan P (2006) Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ Pollut 140:304–311CrossRefGoogle Scholar
  156. Šaric M, Lucchini R (2007) Manganese. In: Nordberg GF, Fowler BA, Nordberg M, Friberg L (eds) Handbook on the toxicology of metals. Academic Press, London, pp 645–674Google Scholar
  157. Savinov VM, Gabrielsen GW, Savinova TN (2003) Cadmium, zinc, copper, arsenic, selenium and mercury in seabirds from the Barents Sea: levels, inter-specific and geographical differences. Sci Total Environ 306:133–158CrossRefGoogle Scholar
  158. Scheifler R, Gauthier-Clerc M, Bohec CL, Crini N, Cœurdassier M, Badot PM, Giraudoux P, Maho YL (2005) Mercury concentrations in king penguin (Aptenodytes patagonicus) feathers at Crozet Islands (sub-Antarctic): temporal trend between 1966–1974 and 2000–2001. Environ Toxicol Chem 24:125–128CrossRefGoogle Scholar
  159. Scheuhammer AM (1987) The chronic toxicity aluminium, cadmium, mercury and lead in birds: a review. Environ Pollut 46:263–295CrossRefGoogle Scholar
  160. Scheuhammer AM, Basu N, Burgess NM, Elliot JE, Campbell GD, Wayland M, Champoux L, Rodrigue J (2008) Relationships among mercury, selenium, and neurochemical parameters in common loons (Gavia immer) and bald eagles (Haliaeetus leucocephalus). Ecotoxicology 17:93–101CrossRefGoogle Scholar
  161. Sjögren B, Iregren A, Elinder C-G, Yokel RA (2007) Aluminum. In: Nordberg GF, Fowler BA, Nordberg M, Friberg L (eds) Handbook on the toxicology of metals. Academic Press, London, pp 339–352Google Scholar
  162. Skoric S, Visnjić-Jeftic Z, Jaric I, Djikanovic V, Mickovic B, Nikcevic M, Lenhardt M (2012) Accumulation of 20 elements in great cormorant (Phalacrocorax carbo) and its main prey, common carp (Cyprinus carpio) and Prussian carp (Carassius gibelio). Ecotoxicol Environ Saf 80:244–251CrossRefGoogle Scholar
  163. Smichowski P, Vodopivez C, Muñoz-Olivas R, Gutierrez AM (2006) Monitoring trace elements in selected organs of Antarctic penguin (Pygoscelis adeliae) by plasma-based techniques. Microchem J 82:1–7CrossRefGoogle Scholar
  164. Soria ML, Repetto G, Repetto M (1995) Revisión general de la toxicología de los metales. In: Repetto M (ed) Toxicología avanzada. Ediciones Díaz de Santos, Madrid, pp 293–358 (in Spanish)Google Scholar
  165. Sparling DW, Lowe TP (1996) Environmental hazards of aluminum to plants, invertebrates, fish, and wildlife. Rev Environ Contam Toxicol 145:1–127Google Scholar
  166. Steinhagen-Schneider G (1986) Cadmium and copper levels in seals, penguins and skuas from the Weddell Sea in 1982/1983. Polar Biol 5:139–143CrossRefGoogle Scholar
  167. Stewart FM, Phillips RA, Catry P, Furness RW (1997) Influence of species, age and diet on mercury concentrations in Shetland seabirds. Mar Ecol-Prog Ser 151:237–244CrossRefGoogle Scholar
  168. Suedel BC, Boraczek JA, Peddicord RK, Clifford PA, Dillon TM (1994) Trophic transfer and biomagnification potential of contaminants in aquatic ecosystems. Rev Environ Contam Toxicol 136:21–89CrossRefGoogle Scholar
  169. Sun L, Xie Z (2001) Changes in lead concentration in Antarctic penguin droppings during the past 3,000 years. Environ Geol 40:1205–1208CrossRefGoogle Scholar
  170. Szefer P, Pempkowiak J, Skwarzec B, Bojanowski R, Holm E (1993) Concentration of selected metals in penguins and other representative fauna of the Antarctica. Sci Total Environ 138:281–288CrossRefGoogle Scholar
  171. Szopińska M, Namieśnik J, Polkowska Z (2016) How important is research on pollution levels in Antarctica? Historical approach, difficulties and current trends. Rev Environ Contam Toxicol. doi:  10.1007/398_2015_5008
  172. Tartu S, Goutte A, Bustamante P, Angelier F, Moe B, Clément-Chastel C, Bech C, Gabrielsen GW, Bustnes JO, Chastel O (2013) To breed or not to breed: endocrine response to mercury contamination by an Arctic seabird. Biol Lett 9:20130317. doi: 10.1098/rsbl.2013.0317 CrossRefGoogle Scholar
  173. Tartu S, Bustamante P, Angelier F, Lendvai AZ, Moe B, Blévin P, Bech C, Gabrielsen GW, Bustnes JO, Chastel O (2016) Mercury exposure, stress and prolactin secretion in an Arctic seabird: an experimental study. Funct Ecol 30:596–604CrossRefGoogle Scholar
  174. Thompson DR (1990) Metal levels in marine vertebrates. In: Furness RW, Rainbow PS (eds) Heavy metals in the marine environment. CRC, Boca Raton, FL, pp 143–182Google Scholar
  175. Tin T, Fleming Z, Hughes K, Ainley D, Convey P, Moreno C, Pfeiffer S, Scott J, Snape I (2009) Impacts of local human activities on the Antarctic environment. Antarct Sci 21:3–33CrossRefGoogle Scholar
  176. UICN (2016) The IUCN Red List of Thereatened Species 2014.3. http://www.iucnredlist.org/details/22697817/0. Accessed 2 Jan 2016
  177. Wastney ME, House WA, Barnes RM, Subramanian KN (2000) Kinetics of zinc metabolism: variation with diet, genetics and disease. J Nutr 130:1355–1359CrossRefGoogle Scholar
  178. Williams TD (1990) Annual variation in breeding biology of gentoo penguin, Pygoscelis papua, at Bird Island, South Georgia. J Zool 222:247–258CrossRefGoogle Scholar
  179. Yin X, Xia L, Sun L, Luo H, Wang Y (2008) Animal excrement: a potential biomonitor of heavy metal contamination in the marine environment. Sci Total Environ 399:179–185CrossRefGoogle Scholar
  180. Zamani-Ahmadmahmoodi R, Alahverdi M, Mirzaei R (2014) Mercury concentrations in common tern Sterna hirundo and slender-billed gull Larus genei from the Shadegan marshes of Iran, in north-western corner of the Persian Gulf. Biol Trace Elem Res 159:161–166CrossRefGoogle Scholar
  181. Zhang W, Ma J (2011) Waterbirds as bioindicators of wetland heavy metal pollution. Procedia Environ Sci 10:2769–2774CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Winfred Espejo
    • 1
  • José E. Celis
    • 2
    Email author
  • Daniel GonzÃlez-Acuña
    • 2
  • Andiranel Banegas
    • 1
    • 3
  • Ricardo Barra
    • 1
  • Gustavo Chiang
    • 4
  1. 1.Department of Aquatic Systems, Faculty of Environmental Sciences, EULA-Chile CentreUniversidad de ConcepciónConcepciónChile
  2. 2.Department of Animal Science, Faculty of Veterinary SciencesUniversidad de ConcepciónChillÃnChile
  3. 3.Department of Sciences Biology Unit, Danlí Technological CampusUniversidad Nacional Autónoma de HondurasDanlíHonduras
  4. 4.Melimoyu Ecosystem Research InstituteSantiagoChile

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