Elsevier

Environmental Pollution

Volume 267, December 2020, 115629
Environmental Pollution

Concentration and origin of lead (Pb) in liver and bone of Eurasian buzzards (Buteo buteo) in the United Kingdom

https://doi.org/10.1016/j.envpol.2020.115629Get rights and content

Highlights

  • Within-year variation in buzzard liver Pb matched the UK gamebird hunting season.

  • Pb isotope ratios in high-concentration buzzard livers matched shotgun ammunition.

  • 89% of the mass of Pb in livers of buzzards with acute exposure was from ammunition.

  • Pb isotope ratios differed among commercial shotgun cartridge brands.

Abstract

Ingestion of lead (Pb) derived from ammunition used in the hunting of game animals is recognised to be a significant potential source of Pb exposure of wild birds, including birds of prey. However, there are only limited data for birds of prey in Europe regarding tissue concentrations and origins of Pb. Eurasian buzzards (Buteo buteo) found dead in the United Kingdom during an 11-year period were collected and the concentrations of Pb in the liver and femur were measured. Concentrations in the liver consistent with acute exposure to Pb were found in 2.7% of birds and concentration in the femur consistent with exposure to lethal levels were found in 4.0% of individuals. Pb concentration in the femur showed no evidence of consistent variation among or within years, but was greater for old than for young birds. The Pb concentration in the liver showed no effect of the birds’ age, but varied markedly among years and showed a consistent tendency to increase substantially within years throughout the UK hunting season for gamebirds. The resemblance of the stable isotope composition of Pb from buzzard livers to that of Pb from the types of shotgun ammunition most widely-used in the UK increased markedly with increasing Pb concentration in the liver. Stable isotope results were consistent with 57% of the mass of Pb in livers of all of the buzzards sampled being derived from shotgun pellets, with this proportion being 89% for the birds with concentrations indicating acute exposure to Pb. Hence, most of the Pb acquired by Eurasian buzzards which have liver concentrations likely to be associated with lethal and sublethal effects is probably obtained when they prey upon or scavenge gamebirds and mammals shot using Pb shotgun pellets.

Introduction

Lead (Pb) is toxic to vertebrates and has adverse effects on most body systems (EFSA, 2010). Wild birds are exposed to environmental Pb from several sources, including that occurring naturally in soil and water, emitted from smelters, residues from leaded petrol and paint, lost or discarded fishing weights and spent ammunition (Franson and Pain, 2011; Grade et al., 2018; Pain et al., 2019). Current exposure of wild animals to Pb derives partly from residues remaining from historical activities, but because anthropogenic emissions have been reduced substantially by recent regulation (EFSA, 2010), ammunition is now a frequent source of Pb exposure of birds (see recent review by Pain et al. (2019)). Some species, such as gamebirds and waterfowl, mistake spent shotgun pellets deposited during hunting on soil or in wetlands for food items or grit. The frequency of pellet ingestion varies considerably among species, especially waterfowl, and Pb poisoning causes high mortality in some species (Mateo, 2009; Green and Pain, 2016). Scavenging and predatory birds can be poisoned when lead shotgun pellets and fragments of shot or lead-based bullets embedded in tissue are ingested after they kill or scavenge from shot game animals (Finkelstein et al., 2012; Pain et al., 2019). While studies from North America and Europe indicate that a proportion of predatory and scavenging birds die from Pb poisoning (Pain et al., 2019), there have been few studies of Pb exposure of these taxa in the UK (Pain and Green, 2015).

The concentration of Pb in the bones of wild birds is usually regarded as the best indicator of exposure over the lifetime of the bird, because Pb accumulates in bone and, once deposited, relatively little of it is remobilised (Scheuhammer, 1987; Franson and Pain, 2011; Krone, 2018), although female birds remobilise some Pb from the skeleton when they form eggshells (Finley and Dieter, 1978). Because Pb is rapidly excreted and transferred to bone from the blood and soft tissues, its concentration in bone is a less useful indicator of recent exposure and absorption than that in soft tissues, such as blood and liver (Franson and Pain, 2011). The half-life of Pb in blood in California condors (Gymnogyps californianus) is 14–17 days (Green et al., 2008; Fry et al., 2009). Reliable estimates of the half-life of Pb in the soft tissues of other birds of prey are not available, so it is uncertain how much it may vary among species, but the half-life of Pb in soft tissues of vertebrates is generally short compared with that for bone (Agency for Toxic Substances and Disease Registry, 2020). Because of the large difference between bone and liver in the lability and accumulation of Pb, we would expect only a weak correlation between bone and liver Pb concentrations across sampled individuals unless there was substantial variation among individuals in their long-term exposure to Pb. Such variation might arise from geographical variation of differences among individuals in behaviour and diet.

In this paper, we analyse data on Pb concentration and isotopic composition in liver and Pb concentration in bones of Eurasian buzzards (Buteo buteo) in the United Kingdom (UK) to test several hypotheses, including that ingestion of Pb from ammunition makes a significant contribution to the Pb exposure of this species. The Eurasian buzzard is a widely-distributed bird of prey (Accipitridae) which breeds in much of Eurasia and has been suggested as a suitable sentinel species for assessing the risks to birds of prey from Pb contamination in Europe (Badry et al., 2020). In the UK, buzzards prey upon and scavenge from carcasses of bird and mammal species including lagomorphs (Leporidae), voles (Cricetidae), gamebirds (Phasianidae and Tetraonidae), pigeons (Columbidae) and shorebirds (Scolopacidae and Charadriidae) (Graham et al., 1995; Francksen et al., 2016, 2017). Some of the species fed upon by buzzards, particularly lagomorphs, pigeons and gamebirds, are the quarry of hunters and farmers, who predominantly use Pb shotgun ammunition to shoot them (Pain et al. 2010). Shotgun pellets and bullet fragments are frequently present in the bodies of unrecovered animals that were shot and killed (Krone, 2018), viscera discarded by hunters (Knott et al., 2010) and live animals that are struck but not killed (Tavecchia et al., 2001; Pain et al., 2015). Hence, by feeding on carrion and preying upon these animals, Eurasian buzzards are potentially exposed to dietary Pb from ammunition to a variable extent, depending on the local type and intensity of shooting and the composition of their diet. Additional non-ammunition sources of exposure also exist, as described above.

We performed quantitative assessments of the following six hypotheses. (1) The mean concentration of Pb in liver is lower than that for bone and more variable among individuals because liver concentrations reflect fluctuations in recent exposure to environmental Pb. (2) The mean concentration of Pb in bone is higher for older than younger buzzards, because Pb accumulates in bone over the bird’s lifetime, but there is no age dependency for liver Pb, which reflects recent short-term exposure. (3) There is greater within-year and among-year variation in the concentration of Pb in buzzard liver than for bone because the composition of the diet of buzzards is known to vary spatially and temporally as a result of variation in the abundance of preferred food items (Graham et al., 1995; Francksen et al., 2016, 2017). (4) Liver Pb concentration is positively correlated with bone Pb concentration across individuals if there is spatial variation and/or consistent individual differences in exposure of buzzards to Pb. (5) If ingestion by buzzards of projectiles or fragments thereof derived from lead-based bullets and lead shotgun pellets is a substantial pathway of Pb exposure relative to other pathways, there will be a consistent pattern of within-year variation in liver Pb concentrations because of the greater level of shooting of game animals in the UK in autumn and winter than in spring and summer. There should not be such variation for bone Pb because its concentration does not reflect short-term exposure. (6) If lead ammunition in the diet of buzzards is a substantial pathway of Pb exposure, relative to other pathways, isotope ratios of Pb from the liver of some individuals should resemble those from widely-used UK shotgun ammunition types, and this resemblance will be strongest in birds with the highest liver Pb concentrations.

Section snippets

Buzzard sample collection and preparation

Specimens (n = 220) were obtained of Eurasian buzzards found dead or dying in the wild in the United Kingdom in the period 2007–2018. Requests were made to the public, birdwatchers and wildlife managers through bird journals, newsletters and other communications, for bodies of birds of prey found dead. Carcasses were sent to the UK Predatory Bird Monitoring Scheme (PBMS) of the Centre for Ecology and Hydrology and to the Raptor Health Scotland project at the Royal (Dick) School of Veterinary

Means and distributions of concentrations of Pb in the liver and femur

The arithmetic mean concentration of Pb in buzzard livers was 2573 μg kg−1 d.w. (n = 187, standard deviation = 7516 μg kg−1; range- <100–85,400 μg kg−1). The median concentration was 722 μg kg−1 d.w.. The geometric mean concentration was 795 μg kg−1 (95% confidence interval 648–974 μg kg−1). For the femur, the arithmetic mean concentration was 5460 μg kg−1 d.w. (n = 125, standard deviation = 10,669 μg kg−1; range- 146 to 110,000 μg kg−1). The median concentration was 3240 μg kg−1 and the

Discussion

The concentrations of Pb we found in livers of 187 Eurasian buzzards collected between 2007 and 2018 were broadly similar to those determined for a smaller sample (n = 56) of buzzards found dead in the UK in 1981–1992 (Pain et al., 1995). The proportions of birds with levels of Pb indicating elevated or acute exposure were broadly similar and not significantly different between the earlier study and ours. In 1981–1992, liver concentration exceeded 6000 μg kg−1 d.w. for 5.3% of birds (cf. 8.0%

Conclusions

Concentrations of Pb consistent with acute exposure were found in the livers of 2.7% of Eurasian buzzards and Pb concentrations in the femur consistent with exposure to lethal levels were found in 4.0% of birds. Pb concentration in the femur did not vary consistently among or within years, but the concentration in old buzzards was about twice that for young birds. For Pb concentration in the liver, there was no effect of the birds’ age, but marked variation among years and a consistent tendency

CRediT author statement

Mark A. Taggart, Richard F. Shore: Conceptualisation, Methodology, Data curation, Chemical analysis, Writing – review. Deborah J. Pain: Conceptualisation, Methodology, Writing – review. Mónica Martinez-Haro, Rafael Mateo: Methodology, Data curation, Chemical analysis, Writing – review. Gabriela Peniche, Jemima Parry-Jones: Resources, Writing – review. Alan J. Lawlor, Elaine D. Potter, Lee A. Walker, David W. Braidwood, Andrew S. French: Methodology, Data curation, Chemical analysis. Julia

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This paper is dedicated to the memory of our co-author and friend Professor Richard Shore (Centre for Ecology and Hydrology). Richard was central to the completion of this study, and as always, worked collaboratively and supportively towards its realisation. Those fortunate enough to have worked alongside Richard will miss him and his contributions to our field. We are honoured to have worked with him.

We thank the many members of the public and wildlife managers who contributed buzzard

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    This paper is dedicated to the memory of Richard F. Shore.

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    Deceased.

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