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.

Experimental safety testing confirms that the NSAID nimesulide is toxic to Gyps vultures in India.

Population declines of Gyps vultures throughout South Asia were caused by unintentional poisoning by the NSAID diclofenac, which was subsequently banned. However, other vulture-toxic NSAIDs are available, including nimesulide, which, in experiments carried out in South Africa, was shown to be toxic to Gyps vultures. We report on safety-testing of nimesulide carried out on Himalayan Griffons G. himalayensis. We gave two vultures a dose of nimesulide by oral gavage at the maximum level of exposure, with two controls dosed with benzyl alcohol. In the two tested birds, plasma nimesulide concentrations peaked after six hours, while serum uric acid concentrations increased steadily up until 24 h post-treatment, after which both birds died, displaying severe visceral gout. The control birds showed no adverse clinical or biochemical signs. We confirm that nimesulide is toxic to Gyps vultures. Veterinary use of nimesulide should be banned in all Gyps vulture range countries in the region.

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.

Metabolism of aceclofenac to diclofenac in the domestic water buffalo Bubalus bubalis confirms it as a threat to Critically Endangered Gyps vultures in South Asia.

Vulture declines in South Asia were caused by accidental poisoning by the veterinary non-steroidal anti-inflammatory drug (NSAID) diclofenac. Although veterinary use of diclofenac has been banned, other vulture-toxic NSAIDs are legally available, including aceclofenac, which has been shown to metabolise into diclofenac in domestic cattle. We gave nine domestic water buffalo the recommended dose of aceclofenac (2 mg kg-1 body weight), collected blood at intervals up to 48 h, and carried out a pharmacokinetic analysis of aceclofenac and its metabolite diclofenac in plasma. Aceclofenac was rapidly converted to diclofenac, and was barely detectable in plasma at any sampling time. Diclofenac was present within 20 min, and peaked 4-8 h after dosing. Aceclofenac is a prodrug of diclofenac, and behaves similarly in domestic water buffalo as it did in domestic cattle, posing the same risk to vultures. We recommend an immediate ban on the veterinary use of aceclofenac across vulture-range countries.

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.

The non-steroidal anti-inflammatory drug nimesulide kills Gyps vultures at concentrations found in the muscle of treated cattle.

Throughout South Asia, cattle are regularly treated with non-steroidal anti-inflammatory drugs (NSAIDs) and their carcasses are left for scavengers to consume. Residues of the NSAID diclofenac in cattle carcasses caused widespread mortality and catastrophic population declines in three species of Gyps vulture during the 1990s and 2000s. Diclofenac is now banned, but other NSAIDs are used in its place. Different lines of evidence, including safety testing in Gyps vultures, have shown that some of these other NSAIDs are toxic, or probably toxic, to vultures. The NSAID nimesulide is widely available and commonly used, and has been found in dead vultures with signs of renal failure (i.e. visceral gout) and without the presence of diclofenac and/or other vulture-toxic NSAIDs. Nimesulide is therefore probably toxic to vultures. Here, we report safety testing of nimesulide in Gyps vultures. In a controlled toxicity experiment, we gave two vultures the maximum likely exposure (MLE) of nimesulide calculated from initial pharmacokinetic and residue experiments in cattle. Two other control birds were given an oral dose of water. Both vultures dosed with nimesulide died within 30 h, after showing outward signs of toxicity and increases in biochemical indicators of renal failure. Post-mortem examinations found extensive visceral gout in both vultures. Both control vultures survived without biochemical indicators of renal failure. With this evidence, we call for an immediate and comprehensive ban of nimesulide throughout South Asia to ensure the survival of the region's Critically Endangered vultures. More generally, testing the impacts of drugs on non-target species should be the responsibility of the pharmaceutical industry, before their veterinary use is licensed.

Experimental safety testing shows that the NSAID tolfenamic acid is not toxic to Gyps vultures in India at concentrations likely to be encountered in cattle carcasses.

Population declines of Gyps vultures across the Indian subcontinent were caused by unintentional poisoning by the non-steroidal anti-inflammatory drug (NSAID) diclofenac. Subsequently, a number of other NSAIDs have been identified as toxic to vultures, while one, meloxicam, is safe at concentrations likely to be encountered by vultures in the wild. Other vulture-safe drugs need to be identified to reduce the use of those toxic to vultures. We report on safety-testing experiments on the NSAID tolfenamic acid on captive vultures of three Gyps species, all of which are susceptible to diclofenac poisoning. Firstly, we estimated the maximum level of exposure (MLE) of wild vultures and gave this dose to 40 Near Threatened Himalayan Griffons G. himalayensis by oral gavage, with 15 control birds dosed with benzyl alcohol (the carrier solution for tolfenamic acid). Two birds given tolfenamic acid died with elevated uric acid levels and severe visceral gout, while the remainder showed no adverse clinical or biochemical signs. Secondly, four G. himalayensis were fed tissues from water buffaloes which had been treated with double the recommended veterinary dose of tolfenamic acid prior to death and compared to two birds fed uncontaminated tissue; none suffered any clinical effects. Finally, two captive Critically Endangered vultures, one G. bengalensis and one G. indicus, were given the MLE dose by gavage and compared to two control birds; again, none suffered any clinical effects. The death of two G. himalayensis may have been an anomaly due to i) the high dose level used and ii) the high ambient temperatures at the time of the experiment. Tolfenamic acid is likely to be safe to Gyps vultures at concentrations encountered by wild birds and could therefore be promoted as a safe alternative to toxic NSAIDs. It is manufactured in the region, and is increasingly being used to treat livestock.

Bayesian Skyline Plots disagree with range size changes based on Species Distribution Models for Holarctic birds.

During the Quaternary, large climate oscillations impacted the distribution and demography of species globally. Two approaches have played a major role in reconstructing changes through time: Bayesian Skyline Plots (BSPs), which reconstruct population fluctuations based on genetic data, and Species Distribution Models (SDMs), which allow us to back-cast the range occupied by a species based on its climatic preferences. In this paper, we contrast these two approaches by applying them to a large data set of 102 Holarctic bird species, for which both mitochondrial DNA sequences and distribution maps are available, to reconstruct their dynamics since the Last Glacial Maximum (LGM). Most species experienced an increase in effective population size (Ne , as estimated by BSPs) as well as an increase in geographical range (as reconstructed by SDMs) since the LGM; however, we found no correlation between the magnitude of changes in Ne and range size. The only clear signal we could detect was a later and greater increase in Ne for wetland birds compared to species that live in other habitats, a probable consequence of a delayed and more extensive increase in the extent of this habitat type after the LGM. The lack of correlation between SDM and BSP reconstructions could not be reconciled even when range shifts were considered. We suggest that this pattern might be linked to changes in population densities, which can be independent of range changes, and caution that interpreting either SDMs or BSPs independently is problematic and potentially misleading.

Climatic change and extinction risk of two globally threatened Ethiopian endemic bird species.

Climate change is having profound effects on the distributions of species globally. Trait-based assessments predict that specialist and range-restricted species are among those most likely to be at risk of extinction from such changes. Understanding individual species' responses to climate change is therefore critical for informing conservation planning. We use an established Species Distribution Modelling (SDM) protocol to describe the curious range-restriction of the globally threatened White-tailed Swallow (Hirundo megaensis) to a small area in southern Ethiopia. We find that, across a range of modelling approaches, the distribution of this species is well described by two climatic variables, maximum temperature and dry season precipitation. These same two variables have been previously found to limit the distribution of the unrelated but closely sympatric Ethiopian Bush-crow (Zavattariornis stresemanni). We project the future climatic suitability for both species under a range of climate scenarios and modelling approaches. Both species are at severe risk of extinction within the next half century, as the climate in 68-84% (for the swallow) and 90-100% (for the bush-crow) of their current ranges is predicted to become unsuitable. Intensive conservation measures, such as assisted migration and captive-breeding, may be the only options available to safeguard these two species. Their projected disappearance in the wild offers an opportunity to test the reliability of SDMs for predicting the fate of wild species. Monitoring future changes in the distribution and abundance of the bush-crow is particularly tractable because its nests are conspicuous and visible over large distances.

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.

Implications of the prevalence and magnitude of sustained declines for determining a minimum threshold for favourable population size.

We propose a new approach to quantifying a minimum threshold value for the size of an animal population, below which that population might be categorised as having unfavourable status. Under European Union law, the concept of Favourable Conservation Status requires assessment of populations as having favourable or unfavourable status, but quantitative methods for such assessments have not yet been developed. One population threshold that is well established in conservation biology is the minimum viable population (MVP) defined as the size of a small but stable population with an acceptably low risk of extinction within a specified period. Our approach combines this small-population paradigm MVP concept with a multiplier, which is a factor by which the MVP is multiplied to allow for the risk of a sustained future decline. We demonstrate this approach using data on UK breeding bird population sizes. We used 43-year time-series data for 189 species and a qualitative assessment of population trends over almost 200 years for 229 species to examine the prevalence, duration and magnitude of sustained population declines. Our study addressed the problem of underestimation of the duration and magnitude of declines caused by short runs of monitoring data by allowing for the truncation of time series. The multiplier was derived from probability distributions of decline magnitudes within a given period, adjusted for truncation. Over a surveillance period of 100 years, we estimated that there was a 10% risk across species that a sustained population decline of at least sixteen-fold would begin. We therefore suggest that, in this case, a factor of 16 could be used as the multiplier of small-population MVPs to obtain minimum threshold population sizes for favourable status. We propose this 'MVP Multiplier' method as a new and robust approach to obtaining minimum threshold population sizes which integrates the concepts of small-population and declining-population paradigms. The minimum threshold value we propose is intended for use alongside a range of other measures to enable overall assessments of favourable conservation status.

Land sparing to make space for species dependent on natural habitats and high nature value farmland.

Empirical evidence from four continents indicates that human food demand may be best reconciled with biodiversity conservation through sparing natural habitats by boosting agricultural yields. This runs counter to the conservation paradigm of wildlife-friendly farming, which is influential in Europe, where many species are dependent on low-yielding high nature value farmland threatened by both intensification and abandonment. In the first multi-taxon population-level test of land-sparing theory in Europe, we quantified how population densities of 175 bird and sedge species varied with farm yield across 26 squares (each with an area of 1 km2) in eastern Poland. We discovered that, as in previous studies elsewhere, simple land sparing, with only natural habitats on spared land, markedly out-performed land sharing in its effect on region-wide projected population sizes. However, a novel 'three-compartment' land-sparing approach, in which about one-third of spared land is assigned to very low-yield agriculture and the remainder to natural habitats, resulted in least-reduced projected future populations for more species. Implementing the three-compartment model would require significant reorganization of current subsidy regimes, but would mean high-yield farming could release sufficient land for species dependent on both natural and high nature value farmland to persist.

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.

Bird conservation and the land sharing-sparing continuum in farmland-dominated landscapes of lowland England.

Empirical evidence from many regions suggests that most species would be least negatively affected if human food demand were met through high-yield agricultural production and conservation of nonfarm ecosystems (land sparing), rather than through wildlife-friendly farming over a larger area (land sharing). However, repeated glaciation and a long history of agriculture may lead to different results in regions such as western Europe. We compared the consequences of land sparing and land sharing on breeding bird species in 2 lowland regions of England, The Fens, with 101 species, and Salisbury Plain, with 83. We derived density-yield responses for each species and then estimated regional population size under regional food production strategies, including land sharing and land sparing, a range of intermediate strategies, and a novel mixed strategy. In both regions, more species achieved maximum regional population size under land sparing than land sharing. In The Fens, the majority of birds were loser species (estimated to have smaller populations under all food production strategies than in the preagricultural baseline scenario), whereas in Salisbury Plain the majority were winners (smaller populations in the preagricultural baseline scenario). Loser species overwhelmingly achieved maximum regional population size under land sparing, whereas winner species achieved maximum regional population size under either land sharing or an intermediate strategy, highlighting the importance of defining which groups of species are the target of conservation. A novel 3-compartment strategy (combining high-yield farming, natural habitat, and low-yield farming) often performed better than either land sharing or land sparing. Our results support intermediate or 3-compartment land-sparing strategies to maximize bird populations across lowland agricultural landscapes. To deliver conservation outcomes, any shift toward land sparing must, however, ensure yield increases are sustainable in the long term, do not entail increased negative effects on surrounding areas, and are linked to allocation of land for nature.

Conservación de Aves y el Continuo de Suelo Compartido-Reservado en Paisajes Dominados por Tierras de Cultivo en las Tierras Bajas de Inglaterra Resumen La evidencia empírica proveniente de muchas regiones sugiere que la mayoría de las especies se verían menos afectadas negativamente si se cumpliera con la demanda humana de alimentos por medio de una producción agrícola de alto rendimiento y la conservación de ecosistemas no agrícolas (dosificación de suelo) en lugar de hacerlo a través de la agricultura amigable con la fauna en un área mayor (partición de suelo). Sin embargo, la glaciación repetitiva y una larga historia agrícola podrían brindar diferentes resultados en regiones como Europa occidental. Comparamos las consecuencias de la dosificación y la partición de suelo sobre especies de aves en reproducción en dos regiones de tierras bajas en Inglaterra: Los Fens, con 101 especies, y la Planicie Salisbury, con 83 especies. Derivamos las respuestas con densidad de rendimiento para cada especie y después estimamos el tamaño poblacional regional bajo estrategias regionales de producción de alimentos, incluyendo la dosificación y la partición de suelo, una gama de estrategias intermedias y una novedosa estrategia mixta. En ambas regiones, más especies alcanzaron el tamaño poblacional máximo para la región bajo la dosificación del suelo que bajo la partición del suelo. En Los Fens, la mayoría de las aves fueron especies perdedoras (se estimó que tendrían tamaños poblacionales menores bajo todas las estrategias de producción de alimento que en el escenario pre-agrícola de la línea base) mientras que en la Planicie Salisbury, la mayoría de las especies fueron ganadoras (con poblaciones más pequeñas en el escenario pre-agrícola de la línea base). Las especies perdedoras tuvieron abrumadoramente un tamaño poblacional máximo para la región bajo la dosificación de suelo, mientras que las especies ganadoras tuvieron este máximo poblacional bajo la partición de suelo o alguna estrategia intermedia, lo que resalta la importancia de la definición de cuáles grupos de especies son el objetivo de conservación. Una estrategia novedosa de tres compartimentos (combina la agricultura de alto rendimiento, el hábitat natural y la agricultura de bajo rendimiento) muchas veces tuvo un mejor desempeño que la dosificación o la partición del suelo. Nuestros resultados respaldan a las estrategias de dosificación de suelo intermedias o de tres compartimentos para maximizar las poblaciones de aves en todos los paisajes agrícolas de las tierras bajas. Para brindar resultados de conservación, cualquier cambio hacia la dosificación del suelo, sin embargo, debe asegurar que los incrementos en el rendimiento son sustentables a largo plazo, no conllevan un incremento de efectos negativos en las áreas circundantes, y que están vinculados a la asignación de suelo para la naturaleza.

Carbon Storage and Land-Use Strategies in Agricultural Landscapes across Three Continents.

The loss of carbon stocks through agricultural land-use change is a key driver of greenhouse gas emissions [1-4], and the methods used to manage agricultural land will have major impacts on the global climate in the 21st century [4-9]. It remains unresolved whether carbon losses would be minimized by increasing farm yields and limiting the conversion of natural habitats ("land sparing"), or maximizing on-farm carbon stocks, even at the cost of reduced yields and therefore greater habitat clearance ("land sharing"). In this paper, we use field surveys of over 11,000 trees, in-depth interviews with farmers, and existing agricultural data, to evaluate the potential impacts of these contrasting approaches, and plausible intermediate strategies, on above-ground carbon stocks across a diverse range of agricultural and natural systems. Our analyses include agroforestry and oil palm plantations in the humid tropics of Ghana; cattle ranching in dry tropical forest in Mexico; and arable cropping in temperate wetlands and forests in Poland. Strikingly, despite the range of systems investigated, land sparing consistently had a higher potential to sustain regional above-ground carbon stocks than any other strategy. This was the case in all three regions and at all plausible levels of food production, including falls in demand. However, if agricultural production increases to meet likely future demand levels, we project large decreases in above-ground carbon stocks, regardless of land-use strategy. Our results strongly suggest that maintaining above-ground carbon stocks will depend on both limiting future food demand and minimizing agricultural expansion through linking high-yield farming with conserving or restoring natural habitats.