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Environmental Science and Pollution Research

, Volume 26, Issue 19, pp 19646–19654 | Cite as

Metal content in the liver, kidney, and feathers of Northern gannets, Morus bassanus, sampled on the Spanish coast

  • Veronica Nardiello
  • Luis Eusebio Fidalgo
  • Ana López-Beceiro
  • Alessia Bertero
  • Salomé Martínez-Morcillo
  • María Prado Míguez
  • Francisco Soler
  • Francesca Caloni
  • Marcos Pérez-LópezEmail author
Research Article
  • 194 Downloads

Abstract

The value of birds as bioindicators for monitoring the environmental inorganic elements has been globally recognized. In this context, due to its well-known ecology and population stability, the Northern gannet (Morus bassanus) could be particularly useful. Dead Northern gannets (n = 30) were collected and samples from the liver, kidney, and feathers were taken, dried, mineralized, and finally analyzed via ICP-MS. Metals and metalloids, namely As, Cd, Hg, Pb, and Zn, associated with environmental pollution and toxicity on living organisms, were evaluated. The mean highest concentrations of As, Hg, and Zn were found in the liver (0.916, 7.026, and 89.81 mg/kg dry weight, respectively). For Cd, the kidney showed the highest mean concentration (17.51 mg/kg dry weight), whereas for Pb, this value corresponded to the feathers (0.399 mg/kg dry weight). Significant differences were found between the age classes in terms of contaminant concentrations, with the adults exhibiting higher metal levels. This difference was significantly relevant for Pb and Hg, where the effect of age was observed for all the considered tissues. When considering the effect of gender, no significant differences were observed, in agreement with similar studies performed in other geographical regions. Finally, positive correlations between the concentrations of Hg and Pb in the feathers and in the liver (r = 0.688, p < 0.001 and r = 0.566, p < 0.001, respectively) were observed, as well as between the feather and kidney concentrations (r = 0.685, p < 0.001) indicating the possibility to use feathers, a non-invasive biomonitoring tissue, for better understanding Hg and Pb exposure in seabirds.

Keywords

Bioindicators Birds Environment Metals Pollution Feather Liver Kidney 

Notes

Acknowledgements

The authors wish to thank to the Wildlife Recovery Centers from Galicia, and to Dirección Xeral de Patrimonio Natural (Consellería de Medio Ambiente e Ordenación do Territorio, Xunta de Galicia), for authorizing the use and transfer of corpses/specimens of wild fauna.

References

  1. Adrian WJ, Stevens ML (1979) Wet versus dry weights for heavy metal toxicity determinations in duck liver. J Wildl Dis 15(1):125–126.  https://doi.org/10.7589/0090-3558-15.1.125 CrossRefGoogle Scholar
  2. Bond AL, Hobson KA, Branfireun BA (2015) Rapidly increasing methyl mercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record. Proc Biol Sci 282(1805).  https://doi.org/10.1098/rspb.2015.0032
  3. Burger J (2008) Assessment and management of risk to wildlife from cadmium. Sci Total Environ 389(1):37–45.  https://doi.org/10.1016/j.scitotenv.2007.08.037 CrossRefGoogle Scholar
  4. Burger J, Gochfeld M (2000a) Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Sci Total Environ 257(1):37–52.  https://doi.org/10.1016/S0048-9697(00)00496-4 CrossRefGoogle Scholar
  5. Burger J, Gochfeld M (2000b) Metals in albatross feathers from midway atoll: influence of species, age, and nest location. Environ Res 82(3):207–221.  https://doi.org/10.1006/enrs.1999.4015 CrossRefGoogle Scholar
  6. Champoux L, Rail JF, Lavoie RA, Hobson KA (2015) Temporal trends of mercury, organochlorines and PCBs in northern gannet (Morus bassanus) eggs from Bonaventure Island, Gulf of St. Lawrence, 1969–2009. Environ Pollut 197:13–20.  https://doi.org/10.1016/j.envpol.2014.10.030 CrossRefGoogle Scholar
  7. Clarke JU (1998) Evaluation of censored data methods to allow statistical comparisons among very small samples with below detection limit observations. Environ Sci Technol 32(1):177–183.  https://doi.org/10.1021/es970521v CrossRefGoogle Scholar
  8. Espejo W, Celis JE, GonzAlez-Acuna D, Banegas A, Barra R, Chiang G (2018) A global overview of exposure levels and biological effects of trace elements in penguins. Rev Environ Contam Toxicol 245:1–64.  https://doi.org/10.1007/398_2017_5 Google Scholar
  9. Espín S, Martinez-Lopez E, Gomez-Ramirez P, Maria-Mojica P, Garcia-Fernandez AJ (2012) Razorbills (Alca torda) as bioindicators of mercury pollution in the southwestern Mediterranean. Mar Pollut Bull 64(11):2461–2470.  https://doi.org/10.1016/j.marpolbul.2012.07.045 CrossRefGoogle Scholar
  10. Fromant A, Carravieri A, Bustamante P et al (2016) Wide range of metallic and organic contaminants in various tissues of the Antarctic prion, a planktonophagous seabird from the Southern Ocean. Sci Total Environ 544:754–764.  https://doi.org/10.1016/j.scitotenv.2015.11.114 CrossRefGoogle Scholar
  11. Furness RW, Camphuysen K (1997) Seabirds as monitors of the marine environment. ICES J Mar Sci 54(4):726–737.  https://doi.org/10.1006/jmsc.1997.0243 CrossRefGoogle Scholar
  12. García-Fernández AJ (2014) Avian ecotoxicology. In: Wexler P (ed) Encyclopedia of toxicology, vol 2, 3rd edn. Elsevier Inc, Academic Press, Amsterdam, pp 289–294.  https://doi.org/10.1016/B978-0-12-386454-3.00496-6 CrossRefGoogle Scholar
  13. 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(5):704–711.  https://doi.org/10.1007/bf01183988 CrossRefGoogle Scholar
  14. Hutton M (1981) Accumulation of heavy metals and selenium in three seabird species from the United Kingdom. Environ Pollut Ser A, Ecol Biol 26(2):129–145.  https://doi.org/10.1016/0143-1471(81)90043-X CrossRefGoogle Scholar
  15. ICH (2005) International conference on harmonization of technical requirements for registration of pharmaceuticals for human use. Validation of analytical procedures: text and methodology Q2(R1). Geneva, SwitzerlandGoogle Scholar
  16. Jaspers V, Dauwe T, Pinxten R, Bervoets L, Blust R, Eens M (2004) The importance of exogenous contamination on heavy metal levels in bird feathers. A field experiment with free-living great tits, Parus major. J Environ Monit 6(4):356–360.  https://doi.org/10.1039/b314919f CrossRefGoogle Scholar
  17. Jerez S, Motas M, Benzal J, Diaz J, Barbosa A (2013) Monitoring trace elements in Antarctic penguin chicks from South Shetland Islands, Antarctica. Mar Pollut Bull 69(1–2):67–75.  https://doi.org/10.1016/j.marpolbul.2013.01.004 CrossRefGoogle Scholar
  18. 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(1–2):450–455.  https://doi.org/10.1016/j.marpolbul.2015.05.006 CrossRefGoogle Scholar
  19. Kim J, Oh JM (2014) Heavy metal concentrations in Black-tailed Gull (Larus crassirostris) chicks, Korea. Chemosphere 112:370–376.  https://doi.org/10.1016/j.chemosphere.2014.04.059 CrossRefGoogle Scholar
  20. 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(4):638–645.  https://doi.org/10.1007/s002449900426 CrossRefGoogle Scholar
  21. Kojadinovic J, Le Corre M, Cosson RP, Bustamante P (2007) Trace elements in three marine birds breeding on Reunion Island (Western Indian ocean): part 1-factors influencing their bioaccumulation. Arch Environ Contam Toxicol 52(3):418–430.  https://doi.org/10.1007/s00244-005-0225-2 CrossRefGoogle Scholar
  22. Lucia M, Andre 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(3):844–853.  https://doi.org/10.1007/s00244-009-9393-9 CrossRefGoogle Scholar
  23. Malinga M, Szefer P, Gabrielsen GW (2010) Age, sex and spatial dependent variations in heavy metals levels in the Glaucous Gulls (Larus hyperboreus) from the Bjornoya and Jan Mayen, Arctic. Environ Monit Assess 69(1–4):407–416.  https://doi.org/10.1007/s10661-009-1183-3 CrossRefGoogle Scholar
  24. Mansouri B, Pourkhabbaz A, 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(10):6139–6145.  https://doi.org/10.1007/s10661-011-2408-9 CrossRefGoogle Scholar
  25. Mendes P, Eira C, Torres J, Soares AM, Melo P, Vingada J (2008) Toxic element concentration in the Atlantic gannet Morus bassanus (Pelecaniformes, Sulidae) in Portugal. Arch Environ Contam Toxicol 55(3):503–539.  https://doi.org/10.1007/s00244-008-9134-5 CrossRefGoogle Scholar
  26. Mendes P, Eira C, Vingada J, Miquel J, Torres J (2013) The system Tetrabothrius bassani (Tetrabothriidae)/Morus bassanus (Sulidae) as a bioindicator of marine heavy metal pollution. Acta Parasitol 58(1):21–25.  https://doi.org/10.2478/s11686-013-0102-5 CrossRefGoogle Scholar
  27. Montevecchi W, Fifield D, Burke C et al (2012) Tracking long-distance migration to assess marine pollution impact. Biol Lett 8(2):218–221.  https://doi.org/10.1098/rsbl.2011.0880 CrossRefGoogle Scholar
  28. Morton J, Tan E, Suvarna SK (2017) Multi-elemental analysis of human lung samples using inductively coupled plasma mass spectrometry. J Trace Elem Med Biol 43:63–71.  https://doi.org/10.1016/j.jtemb.2016.11.008 CrossRefGoogle Scholar
  29. Mowbray TB (2002) Northern Gannet (Morus bassanus), version 2.0. In Poole AF, Gill FB (eds) The Birds of North America. Cornell Lab of Ornithology, Ithaca, NY, USA.  https://doi.org/10.2173/bna.693
  30. Nam DH, Anan Y, Ikemoto T, Okabe Y, Kim EY, Subramanian A, Saeki K, Tanabe S (2005) Specific accumulation of 20 trace elements in great cormorants (Phalacrocorax carbo) from Japan. Environ Pollut 134(3):503–514.  https://doi.org/10.1016/j.envpol.2004.09.003 CrossRefGoogle Scholar
  31. Ohlendorf HM, Anderson DW, Boellstorff DE, Mulhern BM (1985) Tissue distribution of trace elements and DDE in brown pelicans. Bull Environ Contam Toxicol 35(2):183–192.  https://doi.org/10.1007/BF01636497 CrossRefGoogle Scholar
  32. Orlowski G, Polechonski 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 southwestern Poland. Pol J Ecol 55(4):783–793Google Scholar
  33. Pereira MG, Walker LA, Best J, Shore RF (2009) Long-term trends in mercury and PCB congener concentrations in gannet (Morus bassanus) eggs in Britain. Environ Pollut 157(1):155–163.  https://doi.org/10.1016/j.envpol.2008.07.019 CrossRefGoogle Scholar
  34. Pérez-López M, Cid F, Oropesa AL, Fidalgo LE, Ana López B, Soler F (2006) Heavy metal and arsenic content in seabirds affected by the prestige oil spill on the Galician coast (NW Spain). Sci Total Environ 359(1–3):209–220.  https://doi.org/10.1016/j.scitotenv.2005.04.006 CrossRefGoogle Scholar
  35. Saeki K, Okabe Y, Kim E, Tanabe S, Fukuda M, Tatsukawa R (2000) Mercury and cadmium in common cormorants (Phalacrocorax carbo). Environ Pollut 108(2):249–255.  https://doi.org/10.1016/S0269-7491(99)00181-5 CrossRefGoogle Scholar
  36. 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(1–3):133–158.  https://doi.org/10.1016/s0048-9697(02)00489-8 CrossRefGoogle Scholar
  37. Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295.  https://doi.org/10.1016/0269-7491(87)90173-4 CrossRefGoogle Scholar
  38. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Luch A (ed) Molecular, clinical and environmental toxicology. EXS, vol 101. Springer, Basel, pp 133–164.  https://doi.org/10.1007/978-3-7643-8340-4_6 CrossRefGoogle Scholar
  39. Vega CM, Siciliano S, Barrocas PR, Hacon SS, Campos RC, do Couto Jacob S, Ott PH (2010) Levels of cadmium, mercury, and lead in Magellanic penguins (Spheniscus magellanicus) stranded on the Brazilian coast. Arch Environ Contam Toxicol 58(2):460–468.  https://doi.org/10.1007/s00244-009-9349-0 CrossRefGoogle Scholar
  40. Vizuete J, Pérez-López M, Míguez-Santiyán MP, Hernández-Moreno D (2019) Mercury (Hg), lead (Pb), cadmium (Cd), selenium (Se) and arsenic (As) in liver, kidney and feathers of gulls: a review. Rev Environ Contam Toxicol 247:85–146.  https://doi.org/10.1007/398_2018_16 Google Scholar

Copyright information

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

Authors and Affiliations

  • Veronica Nardiello
    • 1
  • Luis Eusebio Fidalgo
    • 2
  • Ana López-Beceiro
    • 2
  • Alessia Bertero
    • 1
  • Salomé Martínez-Morcillo
    • 3
  • María Prado Míguez
    • 3
    • 4
  • Francisco Soler
    • 3
    • 5
  • Francesca Caloni
    • 1
  • Marcos Pérez-López
    • 3
    • 4
    Email author
  1. 1.Department of Veterinary Medicine (DIMEVET)Università degli Studi di MilanoMilanItaly
  2. 2.Department of Veterinary Clinical Sciences, Faculty of Veterinary Medicine (USC)LugoSpain
  3. 3.Toxicology Area, Faculty of Veterinary Medicine (UEX)CaceresSpain
  4. 4.INBIO G+CCáceresSpain
  5. 5.IPROCAR Research InstitutesCáceresSpain

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