The impact of lead poisoning from ammunition sources on raptor populations in Europe.

Poisoning caused by ingestion of spent lead (Pb) ammunition in food items is a common cause of death of raptors. However, there has been no previous attempt to assess the impact of lead poisoning on populations of raptors throughout Europe or examine how this relates to the prevalence of hunting. We used measurements of lead concentration in the liver from over 3000 raptors of 22 species found dead or dying in the wild in 13 countries and a lead poisoning threshold of 20 ppm (dry weight) to assess the proportion of these in which lead poisoning caused or contributed to death. The prevalence of lead poisoning as a cause of death of raptors varied substantially among European countries and was positively correlated across countries with the reported number of hunters per unit area. Ten species had a non-zero proportion of individuals with concentrations exceeding the lead poisoning threshold ranging between 0.3% and 16.5%. The estimated annual conditional death rate from lead poisoning for these ten species averaged 0.44% (range 0.06-0.85%). Scavenging species feeding regularly on carcasses of game animals,tended to have a high annual probability of death from lead poisoning. So too did some predators which only sometimes scavenge, but prey on frequently hunted birds, such as gamebirds, waterfowl and pigeons, which may contain ingested or embedded lead shot. Small-bodied predators had a low annual probability of death from lead poisoning. Modelling indicated that European populations of adult raptors of the ten focal species averaged 6.0% smaller (range 0.2-14.4%) than they would be without the effects of lead poisoning. A given rate of lead poisoning mortality resulted in greater expected population reductions for species with high annual survival rate and late age at first breeding.

Widespread exposure to lead affects the body condition of free-living whooper swans Cygnus cygnus wintering in Britain.

Lead poisoning, through the ingestion of spent lead gunshot, is an established cause of morbidity and mortality in waterbirds globally, but the thresholds at which blood levels begin to affect the physiology of birds in the wild are less well known. Here we determine the prevalence of lead exposure in whooper swans and, for the first time, identify the level of blood lead associated with initial reductions in body condition. Blood lead elevated above background levels (i.e. >20 µg dL(-1)) was found in 41.7% (125/300) of swans tested. Blood lead was significantly negatively associated with winter body condition when levels were ≥44 µg dL(-1) (27/260 = 10%). Our findings indicating that sub-lethal impacts of lead on body condition occur at the lower end of previously established clinical thresholds and that a relatively high proportion of individuals in this population may be affected, reaffirm the importance of reducing contamination of the environment with lead shot.

Potential health risks to adults and children in the UK from exposure to dietary lead in gamebirds shot with lead ammunition.

We estimate potential risks to human health in the UK from dietary exposure to lead from wild gamebirds killed by shooting. The main source of exposure to lead in Europe is now dietary. We used data on lead concentrations in UK gamebirds, from which gunshot had been removed following cooking to simulate human exposure to lead. We used UK food consumption and lead concentration data to evaluate the number of gamebird meals consumed weekly that would be expected, based upon published studies, to result in changes, over and above those resulting from exposure to lead in the base diet, in intelligence quotient (IQ), Systolic Blood Pressure and chronic kidney disease (CKD) considered in a recent opinion of the European Food Safety Authority (EFSA) to be significant at a population level and also in SAT test scores and in rates of spontaneous abortion. We found the consumption of <1 meal of game a week may be associated with a one point reduction in IQ in children and 1.2-6.5 gamebird meals per week may be associated with the other effects. These results should help to inform the development of appropriate responses to the risks from ingesting lead from ammunition in game in the UK and European Union (EU).

Diclofenac residues in carcasses of domestic ungulates available to vultures in India.

Gyps vulture populations across the Indian subcontinent are declining rapidly and evidence indicates that veterinary use of the non-steroidal anti-inflammatory drug (NSAID) diclofenac is the major cause. Exposure of vultures to diclofenac is likely to arise from the consumption of livestock carcasses that have been treated shortly before death, however, detailed information regarding the prevalence and residual levels of diclofenac in carcasses available to vultures in India remains unreported. Here, we present data on diclofenac residues in 1848 liver samples taken from carcasses of dead livestock sampled at 67 sites in 12 states within India, between May 2004 and July 2005. Diclofenac residues were detected in carcasses in all states except Orisa, where only one site was sampled. The overall prevalence of detectable diclofenac (>10 microg kg(-1)) across all states was 10.1% and varied significantly among states, with up to 22.3% prevalence determined in Bihar. The geometric mean concentration of diclofenac found in samples in which the drug was detected was 352 microg kg(-1). The prevalence of carcasses containing diclofenac is similar to that previously proposed to be required to have caused the observed Gyps vulture declines in India. On the 11th of May 2006, the Drug Controller General (India) ordered the withdrawal of all licenses granted for the manufacture of diclofenac for veterinary use within India. However, if Gyps vultures are to be protected, potentially substantial existing stocks now need to be quickly and effectively removed from the Indian veterinary market.

Lead contamination and associated disease in captive and reintroduced red kites Milvus milvus in England.

Since 1989, a red kite Milvus milvus reintroduction programme has been underway in the United Kingdom, with 4-6 week old nestlings brought into captivity and held for 6-8 weeks before reintroduction. As scavengers, red kites may consume unretrieved game, and ingest shot or lead (Pb) fragments in their prey's flesh. We evaluated exposure to Pb in captive and wild red kites by taking blood samples from 125 captive young red kites prior to release, through analysing 264 pellets (regurgitated by wild birds) collected from under a roost site, and analysing Pb concentrations in livers and/or bones of 87 red kites found dead between 1995 and 2003. Lead isotope analyses of livers were also conducted in an effort to identify Pb exposure routes. Forty-six (36.8%) kites sampled prior to release had elevated blood Pb concentrations (201-3340 microg l(-1)). The source of this Pb was probably small fragments of lead ammunition in the carcasses of birds or mammals either fed to the nestlings by their parents or, more likely, subsequently whilst in captivity. Once released, kites were also exposed to lead shot in their food, and a minimum of 1.5-2.3% of regurgitated pellets contained Pb gunshot. Seven of 44 red kites found dead or that were captured sick and died within a few days had elevated (>6 mg kg(-1) dry weight [d.w.]) liver Pb concentrations, and six of these (14%) had concentrations of >15 mg kg(-1) d.w., compatible with fatal Pb poisoning. Post-mortem analyses indicated that two of these birds had died of other causes (poisoning by rodenticide and a banned agricultural pesticide); the remaining four (9%) probably died of Pb poisoning. Bone samples from 86 red kites showed a skewed distribution of Pb concentration, and 18 samples (21%) had Pb concentrations >20 mg kg(-1) d.w., indicating elevated exposure to Pb at some stage in the birds' life. Lead isotopic signatures (Pb (208/206); Pb (206/207)) in liver samples of the majority of kites were compatible with those found in lead shot extracted from regurgitated pellets. Lead isotope ratios found in the livers of kites with very low Pb concentrations were distinct from UK petrol Pb isotopic signatures, indicating that birds were exposed to little residual petrol Pb. We conclude that the primary source of Pb to which red kites are exposed is lead ammunition (shotgun pellets or rifle bullets), or fragments thereof, in their food sources; in some cases exposure appears sufficient to be fatal. We make recommendations to reduce Pb poisoning in both captive and wild red kites and other scavenging species.

Diclofenac disposition in Indian cow and goat with reference to Gyps vulture population declines.

Gyps vultures across India are declining rapidly and the NSAID diclofenac has been shown to be the major cause. Vultures scavenge livestock carcasses that have been treated with diclofenac within the days preceding death. We present data on diclofenac disposition in Indian cow and goat, and field data on the prevalence of diclofenac in carcases in the environment. In the disposition experiment, animals were treated with a single intramuscular injection of diclofenac at 1000 microg kg-1 bw. In cow, diclofenac was detectable in liver, kidney and intestine up to 71 h post-treatment; in plasma, half-life was 12.2 h. In goat, tissue residues were undetectable after 26 h. Prevalence of diclofenac in liver from 36 dead livestock collected in the field was 13.9%. Data suggest that diclofenac residues in Indian cow and goat are short-lived, but diclofenac prevalence in carcasses available to vultures may still be very high.

Arsenic levels in the soils and macrophytes of the 'Entremuros' after the Aznalcóllar mine spill.

In April 1998, a holding lagoon containing pyrite ore processing waste rich in arsenic, failed and released 5-6 million m(3) of highly polluting sludge and acidic water. Over 2700 ha of the internationally important Doñana National and Natural Parks were contaminated. The area of Natural Park to sustain the greatest impact was known as the Entremuros. This paper presents 0-5 cm soil monitoring data from the Entremuros, from sampling campaigns 6 and 18 months after the disaster; as well as macrophyte root, rhizome and stem data from samples taken 18 months after the spill. Results show a clear, decreasing, north-south arsenic soil pollution trend, both 6 and 18 months after the spill, and suggest a small reduction in total soil arsenic levels occurred over time; although a significant increase in extractable arsenic is also noted. The two macrophytes (Typha dominguensis and Scirpus maritimus) studied herein are not accumulating arsenic in stem parts, however, accumulation of arsenic on iron plaque on the roots of these plants may be occurring. Further work is recommended in order to determine the ecotoxicological significance of this process in relation to the avian food-chains of Doñana, and elsewhere.

Mortality of globally threatened Sarus cranes Grus antigon from monocrotophos poisoning in India.

Globally threatened Sarus cranes Grus antigon are resident at Keoladeo National Park World Heritage site and the surrounding area near Bharatpur, Western Rajasthan, India. In winter, they are joined by c. 200 wintering common cranes Grus grus. On 23 November 2000, 15 Sarus cranes and three common cranes were found dead in a field adjacent to the park, where wheat seed had been sown the previous day. Chemical analyses of seed samples from the field and the cranes' alimentary tract contents identified residues of the organophosphate insecticide monocrotophos. Monocrotophos concentrations of 0.8 and 1.8 ppm were found in wheat samples, and 0.2-0.74 ppm (x=0.33) in the alimentary tract contents of five of the seven cranes examined. No other organophosphate or organochlorine pesticides were detected. We conclude that the cranes died from monocrotophos poisoning after eating treated seed. We discuss similar incidents of avian mortality, and recommend that measures be taken to reduce these.

The distribution of arsenic in soils affected by the Aznalcóllar mine spill, SW Spain.

In April 1998, a holding lagoon containing pyrite ore processing waste, failed and released an estimated 5-6 million m(3) of metal rich sludge and acidic waters into the Rio Guadiamar, SW Spain. Over 2700 ha of the internationally important Doñana National and Natural Parks were contaminated. The sludge component of the waste contained up to 0.6% arsenic. This paper presents an extensive set of 0-5 cm soil analyses results from samples taken 6-8 months after the spill. Data are presented on pseudo-total arsenic levels in these samples, and on arsenic removed by both single batch and sequential extraction techniques. Pseudo-total levels of arsenic in the sludge ranged from 1521 to 3510 mg kg(-1), and a mean 4.4% of this was found to be extractable using 2.5% acetic acid. Soils in the Guadiamar Valley and Entremuros areas (those worst affected by the spill) were found to contain 85.4-782 mg kg(-1) and 7.1-196 mg kg(-1) pseudo-total arsenic, respectively. The mean acetic acid extractable component in these areas was 2.5% and 4.9%, respectively. Background pseudo-total arsenic levels in the soils of the area have been found to be 4.2-13.6 mg kg(-1). Rapid input of acidic waters, and the acidic nature of the sludge itself, may have caused depletion of Mg, Na and K, and to a lesser extent Mn, Ca and PO(4) in the upper 5 cm of the worst affected soils. Sequential extraction results suggest clear As-Fe associations, and possible As-Mn associations within the more soluble phases.

The Doñana ecological disaster: contamination of a world heritage estuarine marsh ecosystem with acidified pyrite mine waste.

One of the most important bird breeding and over wintering sites in the west of Europe, the Coto Doñana, was severely impacted by the release of 5 million cubic meters of acid waste from the processing of pyrite ore. The waste entered ecologically sensitive areas of the park (including breeding areas for internationally endangered bird species) causing sustained pH decreases from pH 8.5 to 4.5 and resulting in massive metal contamination of the impacted ecosystem. The contaminating sludge waste contained arsenic at 0.6%, lead at 1.2% and zinc at 0.8% on a dry weight basis. The acid conditions facilitated the solubilization of these metals, leading to water concentrations lethal for aquatic wildlife. The accident caused considerable fish and invertebrate kills and has severe consequences for the protected bird species dependent on the impacted habitats and adjacent areas.

Lead concentrations in birds of prey in Britain.

This paper reports on lead (Pb) concentrations in the livers of 424 individuals of 16 raptor species found dead and sent for analysis to the Institute of Terrestrial Ecology, Monkswood, from the early 1980s to the early 1990s. Elevated Pb concentrations in liver (>20 ppm dry wt), within the range associated with Pb poisoning mortality in raptors, were recorded in one peregrine (4% of species sample) and one buzzard (2% of species sample). These birds are likely to have ingested lead gunshot in the flesh of their prey. Another one each of these species had liver Pb concentrations of 15-20 ppm dry wt, reflecting unusually high absorption of Pb. No individuals of any other species had >15 ppm dry wt liver Pb, although some had 6-15 ppm. The source of Pb in these birds was unknown, but it could have resulted from high Pb concentrations in prey items, including some containing lead shot. Median liver Pb concentrations were generally very low (ranging from <0.07 to 1.61 ppm dry wt for species with sample sizes exceeding 10). In sparrowhawks, for which a large sample was available, liver Pb concentrations in all but one individual were low (<2.6 ppm dry wt). Pb concentrations in juveniles were significantly lower than in adults, and were lowest in recently fledged birds.

Lead poisoning of raptors in France and elsewhere.

Although lead poisoning, through the ingestion of gunshot embedded in prey, is known to have been a significant mortality factor for several raptor species in the United States (Haliaeetus leucocephalus and Gymnogyps Californianus), very little published information is available concerning raptors in Europe. This paper presents the results of liver lead analysis from 222 raptors collected throughout France and reviews other published and unpublished European information. Of the 11 diurnal and 6 nocturnal raptor species investigated in this study, elevated liver lead concentrations, suggestive of shot ingestion, were found in 3 (Accipiter nisus, A. gentilis, Buteo buteo). The likelihood of a species to ingest shot appears related to feeding habits, with scavengers and predators that take game species the most susceptible. Raptor species at risk from lead poisoning, including some of high conservation value, are described, and future priorities for lead poisoning research and policy are suggested.

Tissue lead concentrations and shot ingestion in nine species of waterbirds from the Camargue (France).

This study investigates the relationship among lead exposure (shot ingestion), current lead impregnation (liver lead values), current and previous lead impregnation (bone lead values), and lead excretion (feather lead) in nine species of waterbird from the Camargue (Rhone river delta), France. Results indicate that for individuals there is no readily predictable relationship between ingested shot and liver or bone lead concentrations. However, at the "population" level, and interspecifically, significant positive relationships exist between the susceptibility to shot ingestion and the degree of lead impregnation. Shoveler (Anas clypeata) proved to be an exception, with a high level of shot ingestion and no elevated tissue lead values. This is probably related to dietary factors. Species with a high degree of current lead contamination tended to be those that had also previously absorbed elevated levels of lead. Feather lead concentrations were not clearly related to the vulnerability of a species to shot ingestion or lead poisoning. There was no significant absorption of arsenic and antimony from gunshot associated with lead absorption.

Lead shot ingestion by waterbirds in the Camargue, france: an investigation of levels and interspecific differences.

Between January 1988 and February 1989, gizzards were collected from 1155 birds from the groups; Anatidae, Charadriidae, Scolopacidae and Rallidae, shot in the Camargue, and examined for the presence of ingested lead shot. Shot was found in nine out of ten Anatidae species, three of 15 Scolopacidae species and all of three Rallidae species. Twenty-seven per cent of Anatidae sampled had ingested shot, 13.8% had one shot present and 6.3% had more than five. Shot ingestion levels ranged from 3-60% of birds examined according to species. The incidence of shot ingestion did not appear to vary seasonally. In Anatidae, a strong interspecific relationship was found between the grit size ingested and susceptibility to ingest shot (r = 0.94). In Scolopacidae, shot ingestion may have been related to grit size ingested, feeding method and bill length. The levels of shot ingestion presented are for most species higher than have been reported elsewhere in the world. This may result from the absence of grit and presence of high shot densities in Camargue marshes.

Haematological parameters as predictors of blood lead and indicators of lead poisoning in the black duck (Anas rubripes).

The validity of various haematological parameters as indicators of blood lead concentration and lead poisoning in the black duck (Anas rubripes) is discussed. Elevated (> 40 microg dl(-1)) blood lead (PbB) levels were recorded in 41% of the 229 wild birds examined. No correlation was found between PbB concentration and haematocrit. Zinc protoporphyrin (ZPP) was positively correlated with PbB. Haemoglobin, delta-aminolevulinic acid dehydratase (ALA-d) activity and non-activated/activated ALA-d ratios were negatively correlated with PbB. The minimum PbB levels at which these parameters were affected varied greatly. ZPP and haemoglobin were relatively insensitive to PbB concentrations; whilst ALA-d activity and ALA-d ratio were influenced by PbB concentrations of < 5 microg dl(-1). Log(10) ALA-d ratio was more strongly correlated with PbB (r = -0.953) than log(10) ALA-d activity (r = -0.914) and the predictive validity (% false -ve and +ve predictions) of the ratio method was higher. The high individual variability in ALA-d activities at low PbB levels was greatly reduced by the use of the ALA-d ratio method. The ALA-d ratio method proved the most efficient for screening black duck for lead poisoning in the field.