Metals in Feathers of African Penguins (Spheniscus demersus): Considerations for the Welfare and Management of Seabirds Under Human Care

  • S. Squadrone
  • M. C. Abete
  • P. Brizio
  • D. Pessani
  • L. Favaro
Article

Abstract

Bird feathers have been proven to be reliable indicators of metal exposure originating from contaminated food and polluted environments. The concentrations of 15 essential and non-essential metals were investigated in African penguins (Spheniscus demersus) feathers from a Northwestern Italian zoological facility. These birds are exclusively fed with herring from the northeast Atlantic Ocean. Certain elements, such as Hg and Cd, reflected the bioaccumulation phenomena that occur through the marine food chain. The levels of Cr, Mn, and Ni were comparable to those registered in feathers of birds living in polluted areas. These results are important for comparative studies regarding the health, nutrition and welfare of endangered seabirds kept under human care.

Keywords

Metal accumulation Biomonitoring Penguins Feathers 

Notes

Acknowledgements

The authors would like to thank Zoom Torino S.p.A. (http://www.zoomtorino.it), and in particular Dr. Daniel Sanchez, Dr. Valentina Isaja, Dr. Laura Ozella, and Dr. Sara Piga for their help during collection of samples. Kim Maciej is acknowledged for providing holding data for the genus Spheniscus. Livio Favaro was supported during the writing of this manuscript by the University of Torino through a MIUR co-financed postdoctoral fellowship. The authors also thank the editor and the anonymous reviewers for useful suggestions and comments on an earlier version of this manuscript.

Compliance with Ethical Standards

Ethical Approval

This research was carried out with the approval of the Ethical Committee of the Istituto Zooprofilattico Sperimentale del Piemonte Liguria e Valle d’Aosta (11168; 14 July 2014).

Research Involving with Human and Animal Participants

This research conformed to the Ethical Guidelines for the Conduct of Research on Animals by Zoos and Aquariums (WAZA 2005).

References

  1. Abbasi NA, Chaudhry VLB, Ali S, Malik RM (2015) Influence of taxa, trophic level, and location on bioaccumulation of toxic metals in bird’s feathers: a preliminary biomonitoring study using multiple bird species from Pakistan. Chemosphere 120:527–537CrossRefGoogle Scholar
  2. Abdullah M, Fasola M, Muhammad A, Malik SA, Bostan N, Bokhari B, Kamran MA, Shafqat MN, Alamdar A, Khan M, Ali N (2015) Avian feathers as a non-destructive bio-monitoring tool of trace metals signatures: a case study from severely contaminated areas. Chemosphere 119:553–561CrossRefGoogle Scholar
  3. Adriano DC (2001) Trace elements in terrestrial environments: biochemistry, bioavailability and risks of metals. Springer, New YorkCrossRefGoogle Scholar
  4. ATSDR (Agency for Toxic Substances and Disease Registry) (2005). Toxicological Profile for Nickel. Agency for Toxic Substances and Disease Registry, U.S. Public Health Service, AtlantaGoogle Scholar
  5. Barbieri E, Passos E, Filippini A, dos Santos IS, Garcia CAB (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
  6. Barton CC, Schmitz SC 2009. Environmental toxicology: wildlife. In: Wexler P (ed), Information resources in toxicology (pp 251–254)Google Scholar
  7. BirdLife International (2013). Spheniscus demersus. The IUCN Red List of Threatened Species. Version 2014.2. http://www.iucnredlist.org. Accessed on 15 Dec 2014
  8. Blay N, Côté IM (2001) Optimal conditions for breeding of captive Humboldt penguins (Spheniscus humboldti): a survey of British zoo. Zoo Biol 20:545–555CrossRefGoogle Scholar
  9. Burger J (1993) Metals in avian feathers: bioindicators of environmental pollution. Rev Envirom Toxicol 5:203–311Google Scholar
  10. Burger J, Gochfeld M (2000) Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Sci TotEnviron 257:37–52Google Scholar
  11. Burger J, Gochfeld M (2009) Comparison of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in feathers in bald eagle (Haliaeetus leucocephalus), and comparison with common eider (Somateria mollissima), glaucous-winged gull (Larus glaucescens), pigeon guillemot (Cepphus columba), and tufted puffin (Fratercula cirrhata) from the Aleutian Chain of Alaska. Environ Monit Assessment 152(1–4):357–367CrossRefGoogle Scholar
  12. 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 Tot Environ 398:20–25CrossRefGoogle Scholar
  13. 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 Tot Environ 454:141–148CrossRefGoogle Scholar
  14. Crawford RJM, Altwegg R, Barham BJ, Barham PJ, Durant JM, Dyer BM, Geldenhuys D, Makhado AB, Pichegru L, Ryan PG, Underhill LG, Upfol L, Waller LJ, Whittington PA (2011) Collapse of South Africa’s penguins in the early 21st century. Afr J Mar Sci 33:139–156CrossRefGoogle Scholar
  15. Das KK (2008) Nickel, its adverse health effects oxidative stress. Indian J Med Res 128:412–425Google Scholar
  16. Dauwe T, Bervoets L, Blust R, Pinxten R, Eens M (2000) Can excrement and feathers of nestling songbirds be used as biomonitors for heavy metals pollution? Arch Environ Contam Toxicol 9:541–546CrossRefGoogle Scholar
  17. Davis LS, Darby JT (1990) Penguin Biology. Academic Press, LondonGoogle Scholar
  18. Deng H, Zhang Z, Chang C, Wang Y (2007) Trace metal concentration in Great Tit (Parus major) and Greenfinch (Carduelis sinica) at the Western Mountains of Beijing, China. Environ Pollut 148:620–626CrossRefGoogle Scholar
  19. Dmowski K (1999) Birds as bioindicators of heavy metal pollution: review and examples concerning European species. Acta Ornithol 34:1–25Google Scholar
  20. Eeva T, Lehikoinen E, Rönkä M (1998) Air pollution fades the plumage of the great tit. Funct Ecol 12:607–612CrossRefGoogle Scholar
  21. Eeva T, Belskii E, Kuranov B (2006) Environmental pollution affects genetic diversity in wild bird populations. Mut Res 608:8–15CrossRefGoogle Scholar
  22. Eisler R (1981) Trace metal concentrations in marine organisms. Pergamon Press, New YorkGoogle Scholar
  23. Eisler R (1987) Mercury hazards to fish, wildlife and invertebrates: a synoptic review. U.S. Fish and Wildlife Service, LaurelGoogle Scholar
  24. Eisler R (1988) Lead hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish and Wildlife Service, LaurelGoogle Scholar
  25. 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
  26. Falkowska L, Szumilo E, Hajdryh J, Grajewska A, Beldowska M, Krause I (2013a). Effect of diet on the capacity to remove mercury from the body of a penguin (Spheniscus demersus) living in the zoo. E3S Web Conf 1:12002.  https://doi.org/10.1051/e3sconf/20130112002 CrossRefGoogle Scholar
  27. Falkowska L, Reindl AR, Szumiło E, Kwaśniak J, Staniszewska M, Bełdowska M, Lewandowska A, Krause I (2013b) 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
  28. Favaro L, Gamba M, Alfieri C, Pessani D, McElligott AG (2016) Vocal individuality cues in the African penguin (Spheniscus demersus): a source-filter theory. Sci Rep 5:17255.  https://doi.org/10.1038/srep17255 CrossRefGoogle Scholar
  29. 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(6):1265–1269CrossRefGoogle Scholar
  30. Gangoso L, Alvarez-Lloret PA, Rodriguez-Navarro AAB, Mateo R, Hiraldo F, Donazar JA (2009) Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ Pollut 157:569–574CrossRefGoogle Scholar
  31. Heath RGM, Randall RM (1985) Growth of Jackass penguin chicks, Spheniscus demersus, hand reared on different diets. J Zool 205:91–105CrossRefGoogle Scholar
  32. Heinz GH (1996) Selenium in birds. In: Beyer WN, Heinz GH, Redmom-Norwood AW (eds) Environmental contaminants in wildlife: interpreting tissues concentrations. Lewis Publishers INC, Boca Raton, pp 447–458Google Scholar
  33. 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
  34. Kemper J, Roux JP, Underhill LG (2008) Effect of age and breeding status on molt phenology of adult African penguins (Spheniscus demersus) in Namibia. Auk 125:809–819CrossRefGoogle Scholar
  35. Lodenious M, Solonen T (2013) The use of feathers of birds of prey as indicators of metal pollution. Ecotoxicology 22:1319–1334CrossRefGoogle Scholar
  36. Lucia M, Andrè JM, Gontier K, Diot N, Veiga J, Davail S (2010) Trace element concentrations (mercury, cadmium, copper, zinc, lead, aluminium, nickel, arsenic, and selenium) in some aquatic birds of the Southwest Atlantic Coast of France. Arch Environ Contam Toxicol 58:844–853CrossRefGoogle Scholar
  37. Markowski M, Banbura M, Kalinski A, Markowski J, Skwarska J, Zielinski P, Wawrzyniak J, Ban J (2013) Avian feathers as bioindicators of the exposure to heavy metal contamination of food. Bull Environ Contam Toxicol 91:302–305CrossRefGoogle Scholar
  38. Metcheva R, Yurukova L, Teodorova S, Nikolova E (2006) The penguin feathers as bioindicator of Antarctica environmental state. Sci Tot Environ 362:259–265CrossRefGoogle Scholar
  39. 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(1–4): 571 – 85Google Scholar
  40. Nyholm NEI (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
  41. Ohlendorf HM, Heinz GH (2009) Selenium in birds. In: Beyer WN, Meador JP (eds), Environmental contaminants in biota: interpreting tissue concentrations. CRC Press, Boca Raton, FL, pp 669–701Google Scholar
  42. Outridge PM, Scheuhammer AM (1993) Bioaccumulation and toxicology of nickel: implications for wild mammals and birds. Environ Rev 1(2):172–197CrossRefGoogle Scholar
  43. Pohl C, Hennings U (2008) Trace metals in Baltic Seawater. In: Feistel R, Nausch G, Wasmund N (eds) State and evolution of the Baltic Sea 1952–2005. John Wiley & Sons, pp 367–393Google Scholar
  44. Polak-Juszczak L (2009) Temporal trends in bioaccumulation of trace metals in herring, sprat, and cod from the southern Baltic Sea in the 1994–2003 period. Chemosphere 76:1334–1339CrossRefGoogle Scholar
  45. Rahman MA, Hasegawa H, Lim RP (2012) Bioaccumulation, biotransformation and trophic transfer of arsenic in the aquatic food chain. Environ Res 116:118–135CrossRefGoogle Scholar
  46. Randall RM, Randall BM, Cooper J, Frost PGH (1986) A new census method for penguins tested on Jackass Penguins (Spheniscus demersus). Ostrich 57:211–215CrossRefGoogle Scholar
  47. Ribeiro AR, Eira C, Torres J, Mendes P, Miquel J, Soares AM, Vingada J (2009) Toxic element concentrations in the razorbill Alca torda (Charadriiformes, Alcidae) in Portugal. Arch Environ Contam Toxicol 56:588–595CrossRefGoogle Scholar
  48. Schreiber EA, Burger J (2002) Biology of marine birds. CRC Press, Boca RatonGoogle Scholar
  49. Snoeijs T, Dauwe T, Pinxten R, Vandesande F, Eens M (2004) Heavy metal exposure affects the humoral immune response in a free-living small songbird, the Great Tit (Parus major). Arch Environ Contam Toxicol 46:399–404CrossRefGoogle Scholar
  50. Spahn SA, Sherry TW (1999) Cadmium and lead exposure associated with reduced growth rates, poorer fledging success of little blue heron chicks (Egretta cerulea). Arch Environ Contam Toxicol 37:377–384CrossRefGoogle Scholar
  51. Sparling DW, Lowe TP, Campbell PGC (1997) Ecotoxicology of aluminum to fish and wildlife. In: Yokel RA, Golub MS (eds) Research issues in aluminum toxicity. Taylor and Frances, Washington, DC, pp 47–68Google Scholar
  52. Squadrone S, Abete MC, Brizio P, Monaco G, Colussi S, Biolatti C, Modesto P, Acutis PL, Pessani D, Favaro L (2016) Sex- and age-related variation in metal content of penguin feathers. Ecotoxicology 25(2):431–438CrossRefGoogle Scholar
  53. Sterner O (2010) Chemistry, health, and environment. Wiley-Blackwell, WeinheimGoogle Scholar
  54. Thomas VG, McGill IR (2008) Dissolution of copper, tin, and iron from sintered tungsten-bronze spheres in a simulated avian gizzard, and an assessment of their potential toxicity to birds. Sci Tot Environ 394:283–289CrossRefGoogle Scholar
  55. Višnjić-Jeftić Ž, Jarić I, Jovanović LJ, Skorić S, Smederevac-Lalić M, Lenhardt M (2010) Heavy metal and trace element accumulation in muscle, liver, and gills of the Pontic shad (Alosa immaculate Bennet 1835) from the Danube River (Serbia). Microchem J 95:341–344CrossRefGoogle Scholar
  56. WAZA (World Association of Zoos and Aquariums) (2005). Ethical guidelines for the conduct of research on animals by zoos and aquariums. 60th Annual Conference of the World Association of Zoos and Aquariums, New York, USA. http://www.waza.org/en/site/conservation/code-of-ethics-and-animal-welfare. Accessed 13 January 2014
  57. Williams TD (1995) The Penguins. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Istituto Zooprofilattico Sperimentale del PiemonteTorinoItaly
  2. 2.Department of Life Sciences and Systems BiologyUniversity of TorinoTorinoItaly

Personalised recommendations