Skip to main content

Advertisement

Log in

Biomonitoring of heavy metals (Cd, Hg, and Pb) and metalloid (As) with the Portuguese common buzzard (Buteo buteo)

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

The accumulation of heavy metals in the environment may have a wide range of health effects on animals and humans. Thus, in this study, the concentrations of arsenic (As), cadmium (Cd), lead (Pb), and mercury (Hg) in the blood and tissues (liver and kidney) of Portuguese common buzzards (Buteo buteo) were determined by inductively coupled plasma-mass spectrometer (ICP-MS) in order to monitor environmental pollution to these elements. In general, Hg and As were the elements which appeared in the highest and lowest concentrations, respectively. A highest percentage of non-detected concentration was found for blood Cd (94.6 %) but, in turn, it was the only metal that was detected in all kidney samples. The kidney was the analyzed sample which showed the highest concentrations of each element evaluated. Statistically, significant differences among blood, liver, and kidney samples were observed for As and Cd (P < 0.05). Cd concentrations in kidney and liver varied significantly with age: Adults showed higher hepatic and renal Cd concentrations than juveniles. Blood Pb concentration seems to show an association with the hunting season. Although raptors are at the top of the food chain and are thus potentially exposed to any biomagnification processes that may occur in a food web, the individuals evaluated in this study generally had low levels of heavy metals in blood and tissues. However, chronic exposure to these metals was verified. The results presented here lend weight to arguments in favor of continuous biomonitoring of metals and metalloids, since heavy metals may accumulate to levels that will pose a risk to both human health and the environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Alleva, E., Francia, N., Pandolfi, M., De Marinis, A. M., Chiarotti, F., & Santucci, D. (2006). Organochlorine and heavy-metal contaminants in wild mammals and birds of Urbino-Pesaro Province, Italy: an analytic overview for potential bioindicators. Archives of Environmental Contamination and Toxicology, 51, 123–134.

    Article  CAS  Google Scholar 

  • Baos, R., Jovani, R., Forero, M. G., Tella, J. L., Gómez, G., Jiménez, B., González, M. J., & Hiraldo, F. (2006a). Relationships between T-cell-mediated immune response and Pb, Zn, Cu, Cd, and As concentrations in blood of nestling white storks (Ciconia ciconia) and black kites (Milvus migrans) from Doñana (southwestern Spain) after the Aznalcóllar toxic spill. Environmental Toxicology and Chemistry, 25(4), 1153–1159.

    Article  CAS  Google Scholar 

  • Baos, R., Jovani, R., Pastor, N., Tella, J. L., Jiménez, B., Gómez, G., González, M. J., & Hiraldo, F. (2006b). Evaluation of genotoxic effects of heavy metals and arsenic in wild nestling white storks (Ciconia ciconia) and black kites (Milvus migrans) from southwestern Spain after a mining accident. Environmental Toxicology and Chemistry, 25(10), 2794–2803.

    Article  CAS  Google Scholar 

  • Battaglia, A., Ghidini, S., Campanini, G., & Spaggiari, R. (2005). Heavy metal contamination in little owl (Athene noctua) and common buzzard (Buteo buteo) from northern Italy. Ecotoxicology and Environmental Safety, 60, 61–66.

    Article  CAS  Google Scholar 

  • Blanco, G., Frías, O., Jiménez, B., & Gómez, G. (2003). Factors influencing variability and potential uptake routes of heavy metals in black kites exposed to emissions from a solid-waste incinerator. Environmental Toxicology and Chemistry, 22(11), 2711–2718.

    Article  CAS  Google Scholar 

  • Braune, B. M., & Gaskin, D. E. (1987). Mercury levels in Bonaparte’s gulls (Larus philadelphia) during autumn molt in the Quoddy Region, New Brunswick, Canada. Archives of Environmental Contamination and Toxicology, 16, 539–549.

    Article  CAS  Google Scholar 

  • Burger, J., & Gochfeld, M. (1997). Age differences in metals in the blood of herring (Larus argentatus) and Franklin’s (Larus pipixcan) gulls. Archives of Environmental Contamination and Toxicology, 33, 436–440.

    Article  CAS  Google Scholar 

  • Burger, J., & Gochfeld, M. (2000). Effects of lead on birds (Laridae): a review of laboratory and field studies. Journal of Toxicology and Environmental Health. Part B, Critical Reviews, 3(2), 59–78.

    Article  CAS  Google Scholar 

  • Castro, I., Aboal, J. R., Fernández, J. A., & Carballeira, A. (2011). Use of raptors for biomonitoring of heavy metals: Gender, age and tissue selection. Bulletin of Environmental Contamination and Toxicology, 86, 347–351.

    Article  CAS  Google Scholar 

  • Catry, P., Costa, H., Elias, G., & Matias, R. (2010). Aves de Portugal, Ornitologia do território continental. Lisboa: Assírio & Alvim.

    Google Scholar 

  • Clarke, J. U. (1998). Evaluation of censored data methods to allow statistical comparisons among very small samples with below detection limits observations. Environmental Science and Technology, 32(1), 177–183.

    Article  CAS  Google Scholar 

  • 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? Archives of Environmental Contamination and Toxicology, 39(4), 541–546.

    Article  CAS  Google Scholar 

  • Dauwe, T., Bervoets, L., Pinxten, R., Blust, R., & Eens, M. (2003). Variation of heavy metals within and among feathers of birds of prey: Effects of molt and external contamination. Environmental Pollution, 124(3), 429–436.

    Article  CAS  Google Scholar 

  • Dmowski, K. (1999). Birds as bioindicators of heavy metal pollution: Review and examples concerning European species. Acta Ornithologica, 341, 1–25.

    Google Scholar 

  • Eisler, R. (1987). Mercury hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish and Wildlife Service Biological Report, 85(1.10), 32.

    Google Scholar 

  • Eisler, R. (1998). Arsenic hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish and Wildlife Service Biological Report, 85(1.12), 2.

    Google Scholar 

  • Erry, B. V., Macnair, M. R., Meharg, A. A., Shore, R. F., & Newton, I. (1999). Arsenic residues in predatory birds from an area of Britain with naturally and anthropogenically elevated arsenic levels. Environmental Pollution, 106(1), 91–95.

    Article  CAS  Google Scholar 

  • Esteban, M., & Castano, A. (2009). Non-invasive matrices in human biomonitoring: a review. Environment International, 35(2), 438–449.

    Article  CAS  Google Scholar 

  • Evers, D. C., Burgess, N. M., Champoux, L., Hoskins, B., Major, A., Goodale, W. M., Taylor, R. J., Poppenga, R., & Daigle, T. (2005). Patterns and interpretation of mercury exposure in freshwater avian communities in northeastern north America. Ecotoxicology, 14(1–2), 193–221.

    Article  CAS  Google Scholar 

  • Florea, A. M., & Busselberg, D. (2006). Occurrence, use and potential toxic effects of metals and metal compounds. Biometals, 19(4), 419–427.

    Article  CAS  Google Scholar 

  • Franson, J. C. (1996). Interpretation of tissue lead residues in birds other than waterfowl. In W. N. Beyer, G. H. Heinz, & A. W. Redmon-Norwood (Eds.), Environmental contaminants in wildlife: Interpreting tissue concentrations (1st ed., pp. 265–279). Boca Raton: Lewis.

    Google Scholar 

  • Furness, R. W. (1993). Birds as monitors of pollutants. In R. W. Furness & J. J. D. Greenwood (Eds.), Birds as monitors of environmental change (pp. 86–143). London: Chapman and Hall.

    Chapter  Google Scholar 

  • Furness, R. W. (1996). Cadmium in birds. In W. N. Beyer, G. H. Heinz, & A. W. Redmon-Norwood (Eds.), Environmental contaminants in wildlife: Interpreting tissue concentrations (1st ed., pp. 389–404). Boca Raton: Lewis.

    Google Scholar 

  • García-Fernández, A. J., Sanchez-Garcia, J. A., Jimenez-Montalban, P., & Luna, A. (1995). Lead and cadmium in wild birds in southeastern Spain. Environmental Toxicology and Chemistry, 14, 2049–2058.

    Article  Google Scholar 

  • García-Fernández, A. J., Sanchez-Garcia, J. A., Gomez-Zapata, M., & Luna, A. (1996). Distribution of cadmium in blood and tissues of wild birds. Archives of Environmental Contamination and Toxicology, 30, 252–258.

    Article  Google Scholar 

  • García-Fernández, A. J., Motas-Guzmán, M., Navas, I., María-Mojica, P., Luna, A., & Sánchez-Garcia, J. A. (1997). Environmental exposure and distribution of lead in four species of raptors in Southeastern Spain. Archives of Environmental Contamination and Toxicology, 33, 76–82.

    Article  Google Scholar 

  • Gochfeld, M., & Burger, J. (1987). Heavy metal concentrations in the liver of three duck species: Influence of species and sex. Environmental Pollution, 45, 1–15.

    Article  CAS  Google Scholar 

  • Goutte, A., Bustamante, P., Barbraud, C., Delord, K., Weimerskirch, H., & Chastel, O. (2014). Demographic responses to mercury exposure in two closely related Antarctic top predators. Ecology, 95(14), 1075–1086.

    Article  CAS  Google Scholar 

  • Henny, C. J., Rudis, D. D., Roffe, T. J., & Robinson-Wilson, E. (1995). Contaminants and sea ducks in Alaska and the circumpolar region. Environmental Health Perspectives, 103(4), 41–49.

    Article  CAS  Google Scholar 

  • Hernández, M., & Margalida, A. (2009). Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population. Environmental Research, 109, 837–842.

    Article  Google Scholar 

  • Honda, K., Min, B. Y., & Tatsukawa, R. (1985). Heavy metal distribution in organs and tissues of the eastern great white egret Egretta alba modesta. Bulletin of Environmental Contamination and Toxicology, 35(6), 781–789.

    Article  CAS  Google Scholar 

  • Honda, K., Nasu, T., & Tatsukawa, R. (1986). Seasonal changes in mercury accumulation in the black-eared kite, Milvus migrans lineatus. Environmental Pollution, 42, 325–334.

    Article  CAS  Google Scholar 

  • Jager, L. P., Rijnierse, F. V. J., Esselink, H., & Baars, A. J. (1996). Biomonitoring with the Buzzard Buteo buteo in the Netherlands: Heavy metals and sources of variation. Journal of Ornithology, 137, 295–318.

    Article  Google Scholar 

  • Lebedeva, N. V. (1997). Accumulation of heavy metals by birds in the southwest of Russia. Russian Journal of Ecology, 28(1), 41–46.

    Google Scholar 

  • Licata, P., Naccari, F., Lo Turco, V., Rando, R., Di Bella, G., & Dugo, G. (2010). Levels of Cd (II), Mn (II), Pb (II), Cu (II), and Zn (II) in Common Buzzard (Buteo buteo) from Sicily (Italy) by Derivative Stripping Potentiometry. International Journal of Ecology, 1-7.

  • López-Alonso, M., Miranda, M., García-Partida, P., Cantero, F., Hernández, J., & Benedito, J. L. (2007). Use of dogs as indicators of metal exposure in rural and urban habitats in NW Spain. Science of the Total Environment, 372, 668–675.

    Article  Google Scholar 

  • Lucia, M., Bocher, P., Cosson, R. P., Churlaud, C., & Bustamante, P. (2012a). Evidence of species-specific detoxification processes for trace elements in shorebirds. Ecotoxicology, 21(8), 2349–2362.

    Article  CAS  Google Scholar 

  • Lucia, M., Bocher, P., Cosson, R. P., Churlaud, C., Robin, F., & Bustamante, P. (2012b). Insight on trace element detoxification in the Black-tailed Godwit (Limosa limosa) through genetic, enzymatic and metallothionein analyses. Science of the Total Environment, 423, 73–83.

    Article  CAS  Google Scholar 

  • Monteiro, L. R., & Furness, R. W. (2001). Kinetics, dose–response, and excretion of methylmercury in free-living adult Cory’s shearwaters. Environmental Science and Technology, 35(4), 739–746.

    Article  CAS  Google Scholar 

  • Naccari, C., Cristani, M., Cimino, F., Arcoraci, T., & Trombetta, D. (2009). Common buzzards (Buteo buteo) bio-indicators of heavy metals pollution in Sicily (Italy). Environment International, 35, 594–598.

    Article  CAS  Google Scholar 

  • Pain, D. J., & Amiard-Triquet, C. (1993). Lead poisoning of raptors in France and elsewhere. Ecotoxicology and Environmental Safety, 25, 183–192.

    Article  CAS  Google Scholar 

  • Pain, D. J., Sears, J., & Newton, I. (1995). Lead concentrations in birds of prey in Britain. Environmental Pollution, 87, 173–180.

    Article  CAS  Google Scholar 

  • Pain, D. J., Meharg, A. A., Ferrer, M., Taggart, M., & Penteriani, V. (2005). Lead concentrations in bones and feathers of the globally threatened Spanish imperial eagle. Biological Conservation, 121, 603–610.

    Article  Google Scholar 

  • Peakall, D., & Burger, J. (2003). Methodologies for assessing exposure to metals: Speciation, bioavailability of metals, and ecological host factors. Ecotoxicology and Environmental Safety, 56(1), 110–121.

    Article  CAS  Google Scholar 

  • Pérez-López, M., Hermoso de Mendoza, M., López Beceiro, A., & Soler Rodriguez, F. (2008). Heavy metal (Cd, Pb, Zn) and metalloid (As) content in raptor species from Galicia (NW Spain). Ecotoxicology and Environmental Safety, 70, 154–162.

    Article  Google Scholar 

  • Ribeiro, A. R., Eira, C., Torres, J., Mendes, P., Miquel, J., Soares, A. M., & Vingada, J. (2009). Toxic element concentrations in the Razorbill Alca torda (Charadriiformes, Alcidae) in Portugal. Archives of Environmental Contamination and Toxicology, 56, 588–595.

    Article  CAS  Google Scholar 

  • Scheuhammer, A. M. (1987). The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environmental Pollution, 46, 263–295.

    Article  CAS  Google Scholar 

  • Shlosberg, A., Rumbeiha, W. K., Lublin, A., & Kannan, K. (2011). A database of avian blood spot examinations for exposure of wild birds to environmental toxicants: the DABSE biomonitoring project. Journal of Environmental Monitoring, 13(6), 1547–1558.

    Article  CAS  Google Scholar 

  • Stout, J. H., & Trust, K. A. (2002). Elemental and organochlorine residues in bald eagles from Adak Island, Alaska. Journal of Wildlife Diseases, 38(3), 511–517.

    Article  CAS  Google Scholar 

  • Tartu, S., Goutte, A., Bustamante, P., Angelier, F., Moe, B., Clement-Chastel, C., Bech, C., Gabrielsen, G. W., Bustnes, J. O., & Chastel, O. (2013). To breed or not to breed: Endocrine response to mercury contamination by an Arctic seabird. Biology Letters, 9, 1–4.

    Article  Google Scholar 

  • Wayland, M., Neugebauer, E., & Bollinger, T. (1999). Concentrations of lead in liver, kidney, and bone of bald and golden eagles. Archives of Environmental Contamination and Toxicology, 37(2), 267–272.

    Article  CAS  Google Scholar 

  • Wayland, M., García-Fernández, A. J., Neugebauer, E., & Gilchrist, H. G. (2001a). Concentrations of cadmium, mercury and selenium in blood, liver and kidney of common eider ducks from the Canadian arctic. Environmental Monitoring and Assessment, 71, 255–267.

    Article  CAS  Google Scholar 

  • Wayland, M., Gilchrist, H. G., Dickson, D. L., Bollinger, T., James, C., Carreno, R. A., & Keating, J. (2001b). Trace elements in king eiders and common eiders in the Canadian arctic. Archives of Environmental Contamination and Toxicology, 41(4), 491–500.

    Article  CAS  Google Scholar 

  • Wayland, M., Drake, K. L., Alisauskas, R. T., Kellett, D. K., Traylor, J., Swoboda, C., & Mehl, K. (2008). Survival rates and blood metal concentrations in two species of free-ranging North American sea ducks. Environmental Toxicology and Chemistry, 27(3), 698–704.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the fellowship SFRH/BD/62115/2009 provided by the Fundação para a Ciência e Tecnologia. The authors wish to thank all personnel at the Serveis Científics i Tècnics of the University of Barcelona, Spain and especially all personnel from the Servei d’Ecopatologia de Fauna Salvatge of the Autonomous University of Barcelona, Spain.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paula A. Oliveira.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carneiro, M., Colaço, B., Brandão, R. et al. Biomonitoring of heavy metals (Cd, Hg, and Pb) and metalloid (As) with the Portuguese common buzzard (Buteo buteo). Environ Monit Assess 186, 7011–7021 (2014). https://doi.org/10.1007/s10661-014-3906-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-014-3906-3

Keywords

Navigation