Lead poisoning of raptors: state of the science and cross-discipline mitigation options for a global problem.

Lead poisoning is an important global conservation problem for many species of wildlife, especially raptors. Despite the increasing number of individual studies and regional reviews of lead poisoning of raptors, it has been over a decade since this information has been compiled into a comprehensive global review. Here, we summarize the state of knowledge of lead poisoning of raptors, we review developments in manufacturing of non-lead ammunition, the use of which can reduce the most pervasive source of lead these birds encounter, and we compile data on voluntary and regulatory mitigation options and their associated sociological context. We support our literature review with case studies of mitigation actions, largely provided by the conservation practitioners who study or manage these efforts. Our review illustrates the growing awareness and understanding of lead exposure of raptors, and it shows that the science underpinning this understanding has expanded considerably in recent years. We also show that the political and social appetite for managing lead ammunition appears to vary substantially across administrative regions, countries, and continents. Improved understanding of the drivers of this variation could support more effective mitigation of lead exposure of wildlife. This review also shows that mitigation strategies are likely to be most effective when they are outcome driven, consider behavioural theory, local cultures, and environmental conditions, effectively monitor participation, compliance, and levels of raptor exposure, and support both environmental and human health.

Difference in concentration of lead (Pb) in meat from pheasants killed using lead and iron (Fe) shotgun ammunition.

The use of lead shotgun ammunition for hunting has been banned in a few jurisdictions and habitats, principally to protect wild birds from poisoning by ingestion of spent lead shot. The EU and UK REACH processes have recently considered bans on lead ammunition throughout the European Union and United Kingdom, including assessments of possible health benefits from reduced human dietary exposure to lead from game meat. Comparisons of the mean lead concentrations in meat from gamebirds killed using lead and non­lead shotgun ammunition have not been published. We compared lead concentrations in meat from wild-shot pheasants from which lead shotgun pellets were recovered (n = 27) with those from which iron pellets were recovered (n = 20), having removed all pellets from the meat before analysis. The mean concentration of lead in meat from pheasants killed using lead shot was 2.10 mg/kg w.w., which is >20 times the European Union's maximum permitted level for the lead concentration in meat from domesticated animals. For pheasants killed using iron shot the mean was 0.07 mg/kg w.w., which is below the maximum permitted level.

Lead concentrations in commercial dogfood containing pheasant in the UK.

UK and EU regulators are evaluating the potential health benefits of restricting the use of lead ammunition. Little information is available on exposure of pets to ammunition-derived dietary lead from petfood containing meat from wild-shot game animals. We found dogfood including wild-shot pheasant meat to be widely available in the UK. 77% of samples from three raw pheasant dogfood products exceeded the EU maximum residue level (MRL) for lead in animal feed, with mean concentrations approximately 245, 135 and 49 times above the MRL. Concentrations > MRL were also found in a dried food containing pheasant, but not in a processed food, nor in chicken-based products. Lead concentrations in raw pheasant dogfood considerably exceeded those in pheasant meat sold for human consumption, possibly because the dogfood mincing process further fragmented lead particles from shot. Dogs frequently consuming such high-lead food risk adverse health effects; this should be considered within decision-making processes about regulation.

Lead contamination in Australian game meat.

Lead-based ammunition (gunshot and bullets) frequently leaves small lead fragments embedded in the meat of wild-shot game animals. Australia produces several commercial game meat products from wild animals harvested with lead-based ammunition and has a growing population of recreational hunters. However, no studies have previously investigated the frequency of lead fragments or lead concentrations in Australian game meat. We examined 133 Australian minced game meat items of four types for evidence of lead contamination. Samples were meat from kangaroos (Macropus and Osphranter spp.; n=36) and Bennett's wallabies (Notamacropus rufogriseus; n=28) sold for human consumption, and deer ('venison'; multiple spp.; n=32) and stubble quail (Coturnix pectoralis; n=37) harvested for private consumption by recreational hunters. All packages were studied by digital radiography to detect the presence of radio-dense fragments, assumed to be lead fragments from ammunition. Visible fragments were absent in commercially available kangaroo products, but were present in 4%, 28% and 35% of wallaby, venison and quail, respectively. Mean meat lead concentrations (mg/kg wet weight) were 0.01 ± 0.01 for kangaroo, 0.02 ± 0.01 for wallaby, 0.12 ± 0.07 for venison, and 1.76 ± 3.76 for quail. The Australian food standards threshold for livestock meat (0.1 mg/kg w.w.) was not exceeded by any kangaroo or wallaby products but was exceeded by 53% and 86% of venison and quail, respectively. Radiography only detected 35% of samples that were above the food safety threshold. While average lead concentrations in commercially available macropod (kangaroo and wallaby) meat were low, those in recreationally harvested game meat may pose health risks for hunters and associated consumers.

How contaminated with ammunition-derived lead is meat from European small game animals? Assessing and reducing risks to human health.

Small game animals are generally hunted with lead gunshot which often fragments causing elevated lead concentrations in meat and presenting health risks to frequent consumers and vulnerable groups. We reviewed three decades of European data on lead concentrations in the meat of gamebirds, rabbits and hares across countries with various restrictions on lead gunshot use. Mean meat lead concentrations decreased to a low level in Denmark, the only country in the study with a total ban on lead gunshot use. In contrast, elsewhere in Europe meat lead concentrations increased over time, an unexplained and previously undescribed finding. The only regulatory restriction associated with a decrease in meat lead concentrations was the Danish total ban on lead gunshot use. We calculated an arithmetic mean lead concentration in small game meat of 5.205 ppm w.w. (2011-2021) from across Europe. EU and UK regulators are considering banning lead ammunition for all hunting to protect human and wildlife health. The mean value we found for small game meat (2011-2021) was fourteen times higher than that used in a recent EU-wide risk assessment.

Lead ammunition residues in a hunted Australian grassland bird, the stubble quail (Coturnix pectoralis): Implications for human and wildlife health.

Scavenging and predatory wildlife can ingest lead (Pb) from lead-based ammunition and become poisoned when feeding on shot game animals. Humans can similarly be exposed to ammunition-derived lead when consuming wild-shot game animals. Studies have assessed the degree of lead contamination in the carcasses of game animals but this scrutiny has not so far extended to Australia. Stubble quail (Coturnix pectoralis) are one of the only native non-waterfowl bird species that can be legally hunted in Australia, where it is commonly hunted with lead shot. The aim of this study was to characterize lead contamination in quail harvested with lead-based ammunition. The frequency, dimensions, and number of lead fragments embedded in carcasses were assessed through use of radiography (X-ray). From these data, the average quantity of lead available to scavenging wildlife was estimated along with potential risks to human consumers. We radiographed 37 stubble quail harvested by hunters using 12-gauge (2.75") shotguns to fire shells containing 28 g (1 oz) of #9 (2 mm or 0.08" diameter) lead shot in western Victoria, Australia, in Autumn 2021. Radiographs revealed that 81% of carcasses contained embedded pellets and/or fragments with an average of 1.62 embedded pellets detected per bird. By excising and weighing a sample of 30 shotgun pellets (all had a mass of 0.75 grain or 48.6 mg), we calculated an average lead load of 78 mg/100 g of body mass. This was a conservative estimate, because fragments were not considered. This level of lead contamination was comparable to hunted bird species examined using similar methods in Europe. The quantity and characteristics of lead ammunition residues found suggest that predatory and scavenging wildlife and some groups of human consumers will be at risk of negative health impacts.

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

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.

Setting maximum levels for lead in game meat in EC regulations: An adjunct to replacement of lead ammunition.

Each year, hunters from 12 of the 27 European Union (EU) countries and the UK shoot over 6 million large game mammals, 12 million rabbits and hares and over 80 million birds. They support an international game meat market worth over 1.1 thousand million Euros. Animals shot with lead ammunition frequently contain lead fragments in the carcass which contaminate meals made from game meat with concentrations of lead substantially above the maximum allowable level (ML) set by European Commission Regulation EC1881/2006 for meat from domesticated animals. This poses a health risk to frequent consumers of wild-shot game meat, with children and pregnant women being particularly vulnerable. Total replacement of lead rifle and shotgun ammunition with available non-toxic alternatives is needed for all hunting in EU nations to prevent exposure of humans and wildlife to ammunition-derived lead and to allow the depletion of the long-term environmental legacy of lead from spent ammunition. We propose that EC1881/2006 is amended to incorporate an ML for game meats as a supplementary measure to the replacement of lead ammunition. This would harmonise food safety standards for lead in meats traded across and imported into the EU.

Risks to human health from ammunition-derived lead in Europe.

It has been known for centuries that lead is toxic to humans. Chronic exposure to lead, even at low levels, is associated with an elevated risk of cardiovascular and chronic kidney disease in adults and of impaired neurodevelopment and subsequent cognitive and behavioural development in the foetus and young children. Health agencies throughout the world have moved from assuming that there are tolerable levels of exposure to lead to a recognition that valid 'no-effect' thresholds cannot currently be defined. Formerly, the most important exposure pathways were occupational exposure, water from lead plumbing, paints, petrol additives and foods. Regulation of products and improved health and safety procedures at work have left dietary lead as the main remaining pathway of exposure in European countries. Ammunition-derived lead is now a significant cause of dietary lead exposure in groups of people who eat wild game meat frequently. These are mostly hunters, shoot employees and their families, but also some people who choose to eat game for ethical, health or other reasons, and their children. Extrapolation from surveys conducted in the UK and a review of studies of game consumption in other countries suggest that approximately 5 million people in the EU may be high-level consumers of lead-shot game meat and that tens of thousands of children in the EU may be consuming game contaminated with ammunition-derived lead frequently enough to cause significant effects on their cognitive development.

Effects of lead from ammunition on birds and other wildlife: A review and update.

Poisoning of wild birds following ingestion of lead from ammunition has long been recognised and considerable recent research has focused on terrestrial birds, including raptors and scavengers. This paper builds upon previous reviews and finds that both the number of taxa affected and geographical spread of cases has increased. Some lead may also be absorbed from embedded ammunition fragments in injured birds which risk sub-lethal and welfare effects. Some papers suggest inter-specific differences in sensitivity to lead, although it is difficult to disentangle these from other factors that influence effect severity. Sub-lethal effects have been found at lower blood lead concentrations than previously reported, suggesting that previous effect-level 'thresholds' should be abandoned or revised. Lead poisoning is estimated to kill a million wildfowl a year in Europe and cause sub-lethal poisoning in another ≥ 3 million. Modelling and correlative studies have supported the potential for population-level effects of lead poisoning in wildfowl, terrestrial birds, raptors and scavengers.

Wildlife, human and environmental costs of using lead ammunition: An economic review and analysis.

A proposed European Union (EU)-wide restriction on the use of lead gunshot for shooting in and over wetlands estimated that the societal benefits of a restriction outweighed costs, despite few identified benefits being quantified economically. A subsequent Annex XV Investigation Report on the evidence of impacts of lead ammunition in terrestrial environments concluded that additional measures to control its use are warranted, although to date this has not been further evaluated. To help inform this process, we review the literature and undertake new analyses to estimate the costs of continued use of lead ammunition associated with impacts on wildlife, people and the environment. We estimate minimum annual direct costs across the EU and Europe of c. €383 million-€960 million and €444 million-€1.3 thousand million respectively. The value that society places on being able to avoid these losses, estimated using a 'willingness to pay' approach, was c. €2.2 thousand million for wildfowl alone. Our estimated costs of the continued use of lead ammunition across the EU appear to be considerably greater than the likely costs of switching to non-toxic alternative ammunition types, although these have not been formally estimated in full.

Toward a management framework for networks of protected areas in the face of climate change.

Networks of sites of high importance for conservation of biological diversity are a cornerstone of current conservation strategies but are fixed in space and time. As climate change progresses, substantial shifts in species' ranges may transform the ecological community that can be supported at a given site. Thus, some species in an existing network may not be protected in the future or may be protected only if they can move to sites that in future provide suitable conditions. We developed an approach to determine appropriate climate-change adaptation strategies for individual sites within a network that was based on projections of future changes in the relative proportions of emigrants (species for which a site becomes climatically unsuitable), colonists (species for which a site becomes climatically suitable), and persistent species (species able to remain within a site despite the climatic change). Our approach also identifies key regions where additions to a network could enhance its future effectiveness. Using the sub-Saharan African Important Bird Area (IBA) network as a case study, we found that appropriate conservation strategies for individual sites varied widely across sub-Saharan Africa, and key regions where new sites could help increase network robustness varied in space and time. Although these results highlight the potential difficulties within any planning framework that seeks to address climate-change adaptation needs, they demonstrate that such planning frameworks are necessary, if current conservation strategies are to be adapted effectively, and feasible, if applied judiciously.

Potential hazard to human health from exposure to fragments of lead bullets and shot in the tissues of game animals.

BACKGROUND: Lead is highly toxic to animals. Humans eating game killed using lead ammunition generally avoid swallowing shot or bullets and dietary lead exposure from this source has been considered low. Recent evidence illustrates that lead bullets fragment on impact, leaving small lead particles widely distributed in game tissues. Our paper asks whether lead gunshot pellets also fragment upon impact, and whether lead derived from spent gunshot and bullets in the tissues of game animals could pose a threat to human health. METHODOLOGY/PRINCIPAL FINDINGS: Wild-shot gamebirds (6 species) obtained in the UK were X-rayed to determine the number of shot and shot fragments present, and cooked using typical methods. Shot were then removed to simulate realistic practice before consumption, and lead concentrations determined. Data from the Veterinary Medicines Directorate Statutory Surveillance Programme documenting lead levels in raw tissues of wild gamebirds and deer, without shot being removed, are also presented. Gamebirds containing > or =5 shot had high tissue lead concentrations, but some with fewer or no shot also had high lead concentrations, confirming X-ray results indicating that small lead fragments remain in the flesh of birds even when the shot exits the body. A high proportion of samples from both surveys had lead concentrations exceeding the European Union Maximum Level of 100 ppb w.w. (0.1 mg kg(-1) w.w.) for meat from bovine animals, sheep, pigs and poultry (no level is set for game meat), some by several orders of magnitude. High, but feasible, levels of consumption of some species could result in the current FAO/WHO Provisional Weekly Tolerable Intake of lead being exceeded. CONCLUSIONS/SIGNIFICANCE: The potential health hazard from lead ingested in the meat of game animals may be larger than previous risk assessments indicated, especially for vulnerable groups, such as children, and those consuming large amounts of game.

Analysis of nine NSAIDs in ungulate tissues available to critically endangered vultures in India.

In 2006, India, Pakistan, and Nepal banned the manufacture of veterinary formulations of the nonsteroidal anti-inflammatory drug (NSAID) diclofenac. This action was taken to halt the unprecedented decline of three Gyps vulture species that were being poisoned by diclofenac residues commonly present in carcasses of domestic livestock upon which they scavenged. To assess the affect of this ban and evaluate residue prevelances of other NSAIDs, we present a method to detect diclofenac and eight more NSAIDs by liquid chromatography-mass spectrometry and apply this to 1488 liver samples from carcasses of livestock taken across seven Indian states. Diclofenac was present in 11.1% of samples taken between April and December 2006, and meloxicam (4%), ibuprofen (0.6%), and ketoprofen (0.5%) were also detected. Although meloxicam is safe for a range of avian scavengers, including Gypsvultures, data regarding the safety of other NSAIDs is currently limited. If wild Gyps on the Indian subcontinent are to survive, diclofenac bans must be completely effective, and NSAIDs that replace it within the veterinary drug market must be of low toxicity toward Gyps and other scavenging birds.

Projected impacts of climate change on a continent-wide protected area network.

Despite widespread concern, the continuing effectiveness of networks of protected areas under projected 21st century climate change is uncertain. Shifts in species' distributions could mean these resources will cease to afford protection to those species for which they were originally established. Using modelled projected shifts in the distributions of sub-Saharan Africa's entire breeding avifauna, we show that species turnover across the continent's Important Bird Area (IBA) network is likely to vary regionally and will be substantial at many sites (> 50% at 42% of IBAs by 2085 for priority species). Persistence of suitable climate space across the network as a whole, however, is notably high, with 88-92% of priority species retaining suitable climate space in >or= 1 IBA(s) in which they are currently found. Only 7-8 priority species lose climatic representation from the network. Hence, despite the likelihood of significant community disruption, we demonstrate that rigorously defined networks of protected areas can play a key role in mitigating the worst impacts of climate change on biodiversity.

Apparent tolerance of turkey vultures (Cathartes aura) to the non-steroidal anti-inflammatory drug diclofenac.

The nonsteroidal anti-inflammatory drug diclofenac is extremely toxic to Old World Gyps vultures (median lethal dose -0.1-0.2 mg/kg), evoking visceral gout, renal necrosis, and mortality within a few days of exposure. Unintentional secondary poisoning of vultures that fed upon carcasses of diclofenac-treated livestock decimated populations in the Indian subcontinent. Because of the widespread use of diclofenac and other cyclooxygenase-2 inhibiting drugs, a toxicological study was undertaken in turkey vultures (Cathartes aura) as an initial step in examining sensitivity of New World scavenging birds. Two trials were conducted entailing oral gavage of diclofenac at doses ranging from 0.08 to 25 mg/kg body weight. Birds were observed for 7 d, blood samples were collected for plasma chemistry (predose and 12, 24, and 48 h and 7 d postdose), and select individuals were necropsied. Diclofenac failed to evoke overt signs of toxicity, visceral gout, renal necrosis, or elevate plasma uric acid at concentrations greater than 100 times the estimated median lethal dose reported for Gyps vultures. For turkey vultures receiving 8 or 25 mg/kg, the plasma half-life of diclofenac was estimated to be 6 h, and it was apparently cleared after several days as no residues were detectable in liver or kidney at necropsy. Differential sensitivity among avian species is a hallmark of cyclooxygenase-2 inhibitors, and despite the tolerance of turkey vultures to diclofenac, additional studies in related scavenging species seem warranted.

Rate of decline of the Oriental white-backed vulture population in India estimated from a survey of diclofenac residues in carcasses of ungulates.

The non-steroidal anti-inflammatory drug diclofenac is a major cause of the rapid declines in the Indian subcontinent of three species of vultures endemic to South Asia. The drug causes kidney failure and death in vultures. Exposure probably arises through vultures feeding on carcasses of domesticated ungulates treated with the drug. However, before the study reported here, it had not been established from field surveys of ungulate carcasses that a sufficient proportion was contaminated to cause the observed declines. We surveyed diclofenac concentrations in samples of liver from carcasses of domesticated ungulates in India in 2004-2005. We estimated the concentration of diclofenac in tissues available to vultures, relative to that in liver, and the proportion of vultures killed after feeding on a carcass with a known level of contamination. We assessed the impact of this mortality on vulture population trend with a population model. We expected levels of diclofenac found in ungulate carcasses in 2004-2005 to cause oriental white-backed vulture population declines of 80-99% per year, depending upon the assumptions used in the model. This compares with an observed rate of decline, from road transect counts, of 48% per year in 2000-2003. The precision of the estimate based upon carcass surveys is low and the two types of estimate were not significantly different. Our analyses indicate that the level of diclofenac contamination found in carcasses of domesticated ungulates in 2004-2005 was sufficient to account for the observed rapid decline of the oriental white-backed vulture in India. The methods we describe could be used again to assess changes in the effect on vulture population trend of diclofenac and similar drugs. In this way, the effectiveness of the recent ban in India on the manufacture and importation of diclofenac for veterinary use could be monitored.