Pollution and Its Impact on Wild Animals: A Meta-Analysis on Oxidative Stress Authors
First Online: 24 September 2010 Received: 12 March 2010 Revised: 25 June 2010 Accepted: 06 July 2010 DOI:
Cite this article as: Isaksson, C. EcoHealth (2010) 7: 342. doi:10.1007/s10393-010-0345-7 Abstract
Oxidative stress is the unifying feature underlying the toxicity of anthropogenic pollution (e.g., heavy metals, polycyclic aromatic hydrocarbons, and nitrogen-oxides) and the ultimate culprit in the development of many diseases. Yet, there has been no attempt to summarize the published data on wild terrestrial animals to reveal general trends regarding the effects of pollution on oxidative stress. The main findings of this meta-analysis reveal that, as predicted, there is an overall increase in oxidative stress when exposed to pollution. This is mainly due to a weak overall increase of oxidative damages, although there is some variation across taxa. The reduced form of glutathione (GSH) and its associated enzymes are the most reliable biomarkers. This result is important when choosing biomarkers and when using less-invasive sampling of endangered species, or for longitudinal approaches. To be able to predict future population outcomes, possible treatments, but also evolutionary responses to a changing environment, a greater integration of biotic factors such as temperature, bioavailability of toxic elements, and species-specific responses are needed.
Keywords antioxidants oxidative damage reactive oxygen species urbanization vertebrates wildlife Electronic supplementary material
The online version of this article (doi:
) contains supplementary material, which is available to authorized users. 10.1007/s10393-010-0345-7 References
Beelen R, Hoek G, van den Brandt PA, Goldbohm RA, Fischer P, Schouten LJ, et al. (2008) Long-term effects of traffic-related air pollution on mortality in a Dutch cohort (NLCS-AIR study).
Environmental Health Perspectives
Bel’skii EA, Stepanova ZL (1995) On industrial contamination effect on the state of nestlings of the hole-nesting birds.
Chteniya pamyati professora V.V. Stanchinskogo (Professor V.V. Stanchinskii Memorial Lectures), Smolensk, 2:96–99
Berglund ÅMM, Sturve J, Förlin L, Nyholm NEI (2007) Oxidative stress in pied flycatcher
nestlings from metal contaminated environments in northern Sweden.
Bouwhuis S, Sheldon BC, Verhulst S, Charmantier A (2009) Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle.
Proceedings of the Royal Society of London. Series B: Biological Sciences
Brown AR, Hosken DJ, Balloux F, Bickley LK, LePage G, Owen SF, et al. (2009) Genetic variation, inbreeding and chemical exposure—combined effects in wildlife and critical considerations for ecotoxicology.
Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences
Carpenter DO, Arcaro K, Spink DC (2002) Understanding the human health effects of chemical mixtures.
Environmental Health Perspectives
Chamberlain DE, Cannon AR, Toms MP, Leech DI, Hatchwell BJ, Gaston KJ (2009) Avian productivity in urban landscapes: a review and meta-analysis.
Cornwallis CK, West SA, Griffin AS (2009) Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal.
Journal of Evolutionary Biology
Costantini D, Verhulst S (2009) Does high antioxidant capacity indicate low oxidative stress?
Doherty RM, Heal MR, Wilkinson P, Pattenden S, Vieno M, Armstrong B, et al. (2009) Current and future climate- and air pollution-mediated impacts on human health.
Eeva T, Tanhuanpää S, Råbergh C, Airaksinen S, Nikinmaa M, Lehikoinen E (2000) Biomarkers and fluctuating asymmetry as indicators of pollution-induced stress in two hole-nesting passerines.
Eeva T, Ahola M, Lehikoinen E (2009a) Breeding performance of blue tits (
) and great tits (
) in a heavy metal polluted area.
Eeva T, Hakkarainen H, Bel’skii E (2009b) Local survival of pied flycatcher males and females in a pollution gradient of a Cu smelter.
Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress, part I: mechanisms involved in metal induced oxidative damage.
Current Topics of Medicinal Chemistry
Evers DC, Savoy LJ, DeSorbo CR, Yates DE, Hanson W, Taylor KM, et al. (2008) Adverse effects from environmental mercury loads on breeding common loons.
Fossi MC, Leonzio C, Focardi S, Lari L, Renzoni A (1991) Modulation of mixed-function oxidase activity in black-headed gulls living in anthropic environments—biochemical acclimatization or adaptation.
Environmental Toxicology and Chemistry
Fritsch C, Cosson RP, Coeurdassier M, Raoul F, Giraudoux P, Crini N, et al. (2010) Responses of wild small mammals to a pollution gradient: host factors influence metal and metallothionein levels.
Halliwell B, Gutteridge JMC (2007)
Free Radicals in Biology and Medicine, New York: Oxford University Press.
Holmes D, Martin K (2009) A bird’s-eye view of aging: what’s in it for ornithologists?
Isaksson C, Örnborg J, Stephensen E, Andersson S (2005) Plasma glutathione and carotenoid coloration as potential biomarkers of environmental stress in great tits.
Isaksson C, Sturve J, Almrot BC, Andersson S (2009) The impact of urban environment on oxidative damage (TBARS) and enzymatic and non-enzymatic defence system in lungs and liver of great tits,
Koivula MJ, Eeva T (2010) Metal related oxidative stress in wild birds.
Komarnicki GJK (2000) Tissue, sex and age specific accumulation of heavy metals (Zn, Cu, Pb, Cd) by populations of the mole (
Talpa europaea L.
) in a central urban area.
Kelly FJ (2003) Oxidative stress: its role in air pollution and adverse health effects.
Occupational and Environmental Medicine
Knowles SCL, Nakagawa S, Sheldon BC (2009) Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach.
Lajeunesse ML, Forbes MR (2003) Variable reporting and quantitative reviews: a comparison of three meta-analytical techniques.
Laurance WF, Useche DC (2009) Environmental synergisms and extinctions of tropical species.
Limón-Pacheco J, Gonsebatt ME (2009) The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress.
Mutation Research 674:137–147.
Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006)
SAS for Mixed Models, Cary, NC: SAS Publishing.
Migula P, Laszczyca P, Augustyniak M, Wilczek G, Rozpedek K, Kafel A, et al. (2004) Antioxidative defence enzymes in beetles from a metal pollution gradient.
Møller AP, Jennions MD (2001) Testing and adjusting for publication bias.
Trends in Ecology and Evolution
Møller AP, Jennions MD (2002) How much variance can be explained by ecologists and evolutionary biologists?
Mussi MA, Calcaterra NB (2010) Paraquat-induced oxidative stress response during amphibian early embryonic development.
Comparative Biochemistry and Physiology. Part C: Toxicology and Pharmacology 151:240–247.
Nakagawa S, Ockendon N, Gillespie DOS, Hatchwell BJ, Burke T (2007) Assessing the function of house sparrows’ bib size using a flexible meta-analysis method.
Nunes AC, Auffray JC, Mathias ML (2001) Developmental instability in a riparian population of the Algerian mouse (
) associated with a heavy metal-polluted area in central Portugal.
Archives of Environmental Contamination and Toxicology
Rosenberg MS, Adams DC, Gurevitch J (2000)
MetaWin. Statistical Software for Meta- analysis. Version 2.0, Sunderland, MA: Sinauer Associates, p 15.
Sánchez-Chardi A, Marques CC, Gabriel SI, Capela-Silva F, Cabrita AS, López-Fuster MJ, et al. (2008) Haematology, genotoxicity, enzymatic activity and histopathology as biomarkers of metal pollution in the shrew
Surai PF (2003)
Natural Antioxidants in Avian Nutrition and Reproduction, Nottingham, UK: Nottigham University Press, pp 511–542.
Temple HJ, Terry A (2009) European mammals: Red List status, trends, and conservation priorities.
Folia Zoologica 58:248–269.
Terhivuo J, Pankakoski E, Hyvärinen H, Koivisto I (1994) Pb uptake by ecological dissimilar earthworm (Lumbricidae) species near a lead smelter in south Finland.
Velickovic M (2004) Chromosomal aberrancy and the level of fluctuating asymmetry in black-striped mouse (
): effects of disturbed environment.
Viegas-Crespo AM, Lopes PA, Pinheiro MT, Santos MC, Rodrigues PD, Nunes AC, et al. (2003) Hepatic elemental contents and antioxidant enzyme activities in Algerian mice (
) inhabiting a mine area in central Portugal.
Science of the Total Environment
Yang W, Omaye ST (2009) Air pollutants, oxidative stress and human health.
Mutation Research 31:45–54.
Zvereva EL, Kozlov MV (2010) Responses of terrestrial arthropods to air pollution: a meta-analysis.
Environmental Science and Pollution Research
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