Management and Conservation Article

Abstract Despite increased knowledge about environmental toxins and changes in lead use (i.e., the mandated use of nonlead paint, gasoline, and shotgun pellets used for hunting waterfowl on federal lands), lead poisoning continues to occur in terrestrial birds. The degree of exposure and its demographic effect, however, continue to be described, emphasizing the growing concern over lead exposure. We examined 302 blood samples from common ravens (Corvus corax) scavenging on hunter-killed large ungulates and their offal piles to determine if lead rifle-bullet residuum was a point source for lead ingestion in ravens. We took blood samples during a 15-month period spanning 2 hunting seasons. Of the ravens tested during the hunting season, 47% exhibited elevated blood lead levels (≥ 10 μg/dL) whereas 2% tested during the nonhunting season exhibited elevated levels. Females had significantly higher blood lead levels than did males. Our results confirm that ravens are ingesting lead during the hunting season and are likely exposed to lead from rifle-shot big-game offal piles.     

Impact of the California lead ammunition ban on reducing lead exposure in golden eagles and turkey vultures

Predatory and scavenging birds may be exposed to high levels of lead when they ingest shot or bullet fragments embedded in the tissues of animals injured or killed with lead ammunition. Lead poisoning was a contributing factor in the decline of the endangered California condor population in the 1980s, and remains one of the primary factors threatening species recovery. In response to this threat, a ban on the use of lead ammunition for most hunting activities in the range of the condor in California was implemented in 2008. Monitoring of lead exposure in predatory and scavenging birds is essential for assessing the effectiveness of the lead ammunition ban in reducing lead exposure in these species. In this study, we assessed the effectiveness of the regulation in decreasing blood lead concentration in two avian sentinels, golden eagles and turkey vultures, within the condor range in California. We compared blood lead concentration in golden eagles and turkey vultures prior to the lead ammunition ban and one year following implementation of the ban. Lead exposure in both golden eagles and turkey vultures declined significantly post-ban. Our findings provide evidence that hunter compliance with lead ammunition regulations was sufficient to reduce lead exposure in predatory and scavenging birds at our study sites.     

Lead in Ammunition: A Persistent Threat to Health and Conservation

Many scavenging bird populations have experienced abrupt declines across the globe, and intensive recovery activities have been necessary to sustain several species, including the critically endangered California condor (Gymnogyps californianus). Exposure to lead from lead-based ammunition is widespread in condors and lead toxicosis presents an immediate threat to condor recovery, accounting for the highest proportion of adult mortality. Lead contamination of carcasses across the landscape remains a serious threat to the health and sustainability of scavenging birds, and here we summarize recent evidence for exposure to lead-based ammunition and health implications across many species. California condors and other scavenging species are sensitive indicators of the occurrence of lead contaminated carcasses in the environment. Transdisciplinary science-based approaches have been critical to managing lead exposure in California condors and paving the way for use of non-lead ammunition in California. Similar transdisciplinary approaches are now needed to translate the science informing on this issue and establish education and outreach efforts that focus on concerns brought forth by key stakeholders.     

Effectiveness of Action to Reduce Exposure of Free-Ranging California Condors in Arizona and Utah to Lead from Spent Ammunition

California condors (Gymnogyps californianus) released into the wild in Arizona ranged widely in Arizona and Utah. Previous studies have shown that the blood lead concentrations of many of the birds rise because of ingestion of spent lead ammunition. Condors were routinely recaptured and treated to reduce their lead levels as necessary but, even so, several died from lead poisoning. We used tracking data from VHF and satellite tags, together with the results of routine testing of blood lead concentrations, to estimate daily changes in blood lead level in relation to the location of each bird. The mean daily increment in blood lead concentration depended upon both the location of the bird and the time of year. Birds that spent time during the deer hunting season in two areas in which deer were shot with lead ammunition (Kaibab Plateau (Arizona) and Zion (Utah)) were especially likely to have high blood lead levels. The influence upon blood lead level of presence in a particular area declined with time elapsed since the bird was last there. We estimated the daily blood lead level for each bird and its influence upon daily mortality rate from lead poisoning. Condors with high blood lead over a protracted period were much more likely to die than birds with low blood lead or short-term elevation. We simulated the effect of ending the existing lead exposure reduction measures at Kaibab Plateau, which encourage the voluntary use of non-lead ammunition and removal of gut piles of deer and elk killed using lead ammunition. The estimated mortality rate due to lead in the absence of this program was sufficiently high that the condor population would be expected to decline rapidly. The extension of the existing lead reduction program to cover Zion (Utah), as well as the Kaibab plateau, would be expected to reduce mortality caused by lead substantially and allow the condor population to increase.     

Lead poisoning in captive Andean condors (Vultur gryphus)

Elevated lead in the tissues of raptors, especially those that scavenge, is a common occurrence, and lead poisoning appears to be a significant problem in the ongoing recovery effort for California condors (Gymnogyps californianus). Elevated blood lead levels have been found in released birds, and a number of birds have died of lead poisoning. In earlier work, we dosed turkey vultures (Cathartes aura) with lead shot but found them to be a poor model for lead poisoning. In this study, we dosed four Andean condors (Vultur gryphus) with lead shot and found them to be quite sensitive, as two of the birds died and the other two exhibit signs of lead poisoning within 50 days. All lead-responsive parameters were affected, and regurgitation of dosed shot occurred only once. The response of the Andean condors appeared to mimic California condors, suggesting that once exposed to lead, the possibility of survival is poor. This is consistent with observations in the wild, where otherwise healthy birds exposed to metallic lead quickly succumb. At the very least, the release program has to maintain constant surveillance and an active lead monitoring program.     

High Risk of Lead Contamination for Scavengers in an Area with High Moose Hunting Success

Top predators and scavengers are vulnerable to pollutants, particularly those accumulated along the food chain. Lead accumulation can induce severe disorders and alter survival both in mammals (including humans) and in birds. A potential source of lead poisoning in wild animals, and especially in scavengers, results from the consumption of ammunition residues in the tissues of big game killed by hunters. For two consecutive years we quantified the level lead exposure in individuals of a sentinel scavenger species, the common raven (Corvus corax), captured during the moose (Alces alces) hunting season in eastern Quebec, Canada. The source of the lead contamination was also determined using stable isotope analyses. Finally, we identified the different scavenger species that could potentially be exposed to lead by installing automatic cameras targeting moose gut piles. Blood lead concentration in ravens increased over time, indicating lead accumulation over the moose-hunting season. Using a contamination threshold of 100 µg.L⁻¹, more than 50% of individuals were lead-contaminated during the moose hunting period. Lead concentration was twice as high in one year compared to the other, matching the number of rifle-shot moose in the area. Non-contaminated birds exhibited no ammunition isotope signatures. The isotope signature of the lead detected in contaminated ravens tended towards the signature from lead ammunition. We also found that black bears (Ursus americanus), golden eagles and bald eagles (Aquila chrysaetos and Haliaeetus leucocephalus, two species of conservation concern) scavenged heavily on moose viscera left by hunters. Our unequivocal results agree with other studies and further motivate the use of non-toxic ammunition for big game hunting.     

Lead exposure in free-flying turkey vultures is associated with big game hunting in California

Predatory and scavenging birds are at risk of lead exposure when they feed on animals injured or killed by lead ammunition. While lead ammunition has been banned from waterfowl hunting in North America for almost two decades, lead ammunition is still widely used for hunting big game and small game animals. In this study, we evaluated the association between big game hunting and blood lead concentration in an avian scavenger species that feeds regularly on large mammals in California. We compared blood lead concentration in turkey vultures within and outside of the deer hunting season, and in areas with varying wild pig hunting intensity. Lead exposure in turkey vultures was significantly higher during the deer hunting season compared to the off-season, and blood lead concentration was positively correlated with increasing wild pig hunting intensity. Our results link lead exposure in turkey vultures to deer and wild pig hunting activity at these study sites, and we provide evidence that spent lead ammunition in carrion poses a significant risk of lead exposure to scavengers.     

Winter diet and lead poisoning risk of Greater Spotted Eagles Clanga clanga in southeast Spain

ABSTRACT

Capsule: Diet analysis revealed high lead exposure for Greater Spotted Eagles Clanga clanga wintering in southeast Spain.

Aims: To describe the diet composition of the endangered Greater Spotted Eagle in a wintering area located in southeast Spain, and determine lead ammunition exposure through analysis of regurgitated pellets and prey remains.

Methods: Between 2008 and 2018, a total of 26 pellets, 29 prey remains and 10 direct predation observations were collected in El Hondo Natural Park, Spain. All the pellets and 10 prey remains were analysed with X-ray in order to detect metal from ammunition.

Results: Greater Spotted Eagles fed mainly on birds, with 18 different species accounting for 73.1% of prey items and 66.1% of biomass consumed. The most frequent species identified were Common Moorhen Gallinula chloropus (23.1%), rats Rattus spp. (15.4%) and Common Teal Anas crecca (8.9%). Ammunition was detected in 42.3% of regurgitated pellets and in 40.0% of prey remains analysed. Of those containing ammunition, lead shot was found in 63.9% of pellets and 25.0% of prey remains.

Conclusion: High lead shot presence in pellets and prey remains of wintering Greater Spotted Eagles in southeast Spain warns of a high risk of lead poisoning. Factors such as feeding behaviour, the large space–time overlap between the raptor presence and the waterbird hunting season and non-compliance with the ban on the use of lead ammunition are likely contributing to high lead exposure.     

Embedded lead shot in European starlings Sturnus vulgaris: an underestimated hazard for humans and birds of prey

The poisoning of wild animals by lead (Pb) ammunition fired by hunters has been known for many decades, especially in the case of waterbirds. More recently, it has been demonstrated that raptors are also exposed to the risk of plumbism when feeding on unretrieved quarry that was wounded or killed by hunters. Further studies reveal that even humans can be subject to a significant Pb dose while consuming game animals killed by traditional ammunition. Given the relevance of this issue, several pieces of research have been carried out to assess frequency, dimension, and the number of Pb fragments embedded in the carcasses of ungulates, partridges, ducks, and other birds to evaluate the risk related to the consumption of game meat. In spite of their great importance as quarry species across southern Europe, until now, no data have been available on small passerines. To assess the quantity and type of Pb embedded in songbirds, we x-rayed 196 starlings shot in Italy and found Pb pellets and/or visible fragments in 118 carcasses (60.2 %). We counted 128 shotgun pellets in 85 carcasses. In 28 birds, we detected both whole pellets and lead fragments; in 33, we found only small fragments. By excising and weighing a sample of 20 shotgun pellets (diameter 1.35–1.99 mm), we calculated a Pb load of 3.75 g in the whole sample of 196 starlings, corresponding to an average of 27.32 mg/100 g of body weight. This is a conservative estimation, because fragments were not considered. Compared to game birds of a larger size, the starlings in our study had a lower amount of embedded Pb, but the shot pellets and fragments embedded in their tissues were abundant and tiny. Given the results of previous studies, the quantity and level of fragmentation suggest that the risk of Pb poisoning cannot be ruled out for humans and birds of prey consuming the meat from songbirds killed with traditional ammunition.     

Lead Exposure in Bald Eagles from Big Game Hunting,the Continental Implications and Successful Mitigation Efforts

Studies suggest hunter discarded viscera of big game animals (i.e., offal) is a source of lead available to scavengers. We investigated the incidence of lead exposure in bald eagles in Wyoming during the big game hunting season, the influx of eagles into our study area during the hunt, the geographic origins of eagles exposed to lead, and the efficacy of using non-lead rifle ammunition to reduce lead in eagles. We tested 81 blood samples from bald eagles before, during and after the big game hunting seasons in 2005–2010, excluding 2008, and found eagles had significantly higher lead levels during the hunt. We found 24% of eagles tested had levels indicating at least clinical exposure (>60 ug/dL) during the hunt while no birds did during the non-hunting seasons. We performed driving surveys from 2009–2010 to measure eagle abundance and found evidence to suggest that eagles are attracted to the study area during the hunt. We fitted 10 eagles with satellite transmitters captured during the hunt and all migrated south after the cessation of the hunt. One returned to our study area while the remaining nine traveled north to summer/breed in Canada. The following fall, 80% returned to our study area for the hunting season, indicating that offal provides a seasonal attractant for eagles. We fitted three local breeding eagles with satellite transmitters and none left their breeding territories to feed on offal during the hunt, indicating that lead ingestion may be affecting migrants to a greater degree. During the 2009 and 2010 hunting seasons we provided non-lead rifle ammunition to local hunters and recorded that 24% and 31% of successful hunters used non-lead ammunition, respectively. We found the use of non-lead ammunition significantly reduced lead exposure in eagles, suggesting this is a viable solution to reduce lead exposure in eagles.     

Experimental lead poisoning in turkey vultures (Cathartes aura)

Lead-induced mortality appears to have been a major factor in the decline of the California condor (Gymnogyps californianus). We orally dosed turkey vultures (Cathartes aura) with BB-sized lead shot from January 1988 through July 1988 to determine physiologic response (delta-aminolevulinic acid dehydratase inhibition, erythrocyte protoporphyrin levels, anemia), diagnostic tissue lead concentrations (blood, liver, and kidney), and comparative sensitivity of this species. Two turkey vultures died and two became so intoxicated they were euthanized. Overall, responses of measured parameters were comparable to other species exposed to lead although there was considerable individual variation. Survival time (143-211 days), even with the large numbers of shot and constant redosing, was much longer than reported for other species of birds, suggesting considerable tolerance by turkey vultures to the deleterious effects of lead ingestion. Based on these observations, turkey vultures appear to be poor models for assessing the risk of lead poisoning to California condors or predicting their physiologic response.     

Widespread Lead Exposure in Golden Eagles Captured in Montana

Lead poisoning threatens many species of raptors, including golden eagles (Aquila chrysaetos). Much of this lead likely comes from bullet fragments that remain in the carcasses of animals killed by hunters. The likelihood of lead exposure may peak during fall hunting seasons and early winter until carcasses from hunting become scarce. From 2011 to 2018 in western Montana, USA, we captured 91 golden eagles in winter, tested their blood lead levels (BLL), and outfitted a subset of birds (n = 29) with global positioning system [GPS] transmitters. Nearly all golden eagles (94.5%) had elevated BLL (≥10 μg/dL), and 8 of them had BLL above clinical exposure (>60 μg/dL), where they may lose coordination and experience a host of other neurological and physiological disorders. Golden eagles caught late in winter tended to have lower BLL than those caught earlier. At least 69% of the golden eagles equipped with GPS transmitters migrated northward, spending the summer throughout Alaska, USA, and northwestern Canada. Blood lead levels did not differ between migratory and nonmigratory golden eagles. Overall, elevated BLL are widespread among golden eagles throughout winter in western Montana. Promoting nonlead hunting ammunition in areas with high densities of golden eagles will reduce the birds' lead exposure. © 2020 The Wildlife Society.     

Prevalence of embedded shotgun pellets in protected and in legally hunted medium-sized carnivores in Denmark

Illegal killings of protected species may significantly affect their population status or lower recovery rates after protection. Poaching is difficult to monitor directly, hence indirect methods are required to document poaching incidences and levels. The use of shotguns inevitably results in wounding some animals that are not killed. Inefficient hunting methods may result in high annual infliction rates in game species. To reduce wounding of game species, an action plan was implemented in Denmark. Using X-ray analysis, we monitor trends in prevalence of embedded shotgun pellets in the legally hunted red fox (Vulpes vulpes) after the implementation of the action plan, and assess poaching levels of two protected species, the otter (Lutra lutra) and the badger (Meles meles) in Denmark. Overall, 13.8% of the red foxes and 6.9% of the otters carried embedded shotgun pellets, while none were recorded in badgers. The prevalence of embedded shotgun pellets in red foxes declined from 24.9% to 8.5% from the late 1990s to the late 2000s, while no change was recorded in otters. Prevalence of embedded shotgun pellets was similar in otters and red foxes collected in the late 2000s. The decline in wounded red foxes suggests that the hunting methods have changed after the action plan was implemented in Denmark. The high proportion of otters carrying embedded shotgun pellets shows that there is a significant poaching of this protected species in Denmark, possibly by hunters and fish farmers that cannot distinguish between otter and non-native American mink (Neovison vison).     

Acute toxicity of lead, steel, and an iron-tungsten-nickel shot to mallard ducks (Anas platyrhynchos)

Twenty mallards (Anas platyrhynchos) of both sexes were dosed by oral gavage with Heavi-Shot (H-S; Environ-Metal, Inc., Sweet Home, Oregon, USA) pellets, 20 with steel shot, and 10 with lead (Pb) pellets, all of equal size. All pellets were fired from a shotgun into an absorbent material, retrieved, and weighed prior to introduction into the ducks. Birds were fed whole kernel corn and grit and observed for signs of toxicity for 30 days following dosing. Hevi-Shot pellets lost an average of 6.2% of their mass and steel shot pellets lost 57% of their mass in the birds' gizzards. Almost all (90%) of the Pb shot dosed birds died before the end of the study, while no mortality was observed in the steel or H-S dosed groups. Even though total food consumption differed between the H-S and steel shot groups, mean bird weight change was not different. There were no significant morphologic or histopathologic abnormalities of the liver and kidney in the H-S and steel shot groups. Results indicated that mallards dosed orally with eight No. 4 H-S pellets were not adversely affected over a 30-day period, and that H-S provides another environmentally safe nontoxic shot for use in waterfowl hunting.     

Effects of a Danish action plan on reducing shotgun wounding of Common Eider Somateria mollissima

Capsule The incidence of embedded shotgun pellets in Common Eider females declined from 34.1% to 5.5% from 1997 to 2009–2011 after the implementation of an action plan to reduce wounding. Males, which were exposed to hunting outwith the area of the action plan, showed a lower rate of decline.     

Effects of Lead Exposure,Flock Behavior,and Management Actions on the Survival of California Condors (Gymnogyps californianus)

Translocation is an increasingly important tool for managing endangered species, but factors influencing the survival of translocated individuals are not well understood. Here we examine intrinsic and extrinsic drivers of survival for critically endangered California condors (Gymnogyps californianus) whose wild population recovery is reliant upon releases of captively bred stock. We used known fate models and information-theoretic methods to compare the ability of hypothesized covariates, most of which serve as proxies for lead exposure risk, to predict survival rates of condors in California. Our best supported model included the following predictors of survival: age of the recovery program, precipitation, proportion of days observed feeding on proffered carcasses, maximum blood lead concentration over the preceding 18 months, and time since release. We found that as flocks have increased in size and age, condors are increasingly likely to range more widely and less likely to be observed feeding on proffered food, and these “wilder” behaviors were associated with lower survival. After accounting for these behaviors, we found a positive survival trend, which we attribute to ongoing improvements in management. Our findings illustrate that the survival of translocated animals, such as highly social California condors, is influenced by behaviors that change through time.

     

Lead exposure in large carnivores in the greater Yellowstone ecosystem

Ingestion of lead rifle bullet fragments found in discarded hunter-harvested ungulate gut piles negatively affects avian wildlife. Some large carnivores, such as grizzly bears, are also known to target these gut piles as a food source and are therefore potentially at risk of lead exposure. We investigated whether large carnivores in the greater Yellowstone ecosystem were exposed to lead, and if so, if ammunition ingested from gut piles was an apparent source of exposure. Grizzly bears (Ursus arctos, n = 82) exhibited higher blood lead levels (median = 4.4 µg/dL, range 1.1–18.6 µg/dL) than black bears (Ursus americanus, n = 35, median = 1.6, range 0.5–6.9 µg/dL), but blood lead levels did not increase during the autumn hunting season when potentially lead-tainted gut piles are available. Wolves (Canis lupus, n = 21) and cougars (Puma concolor, n = 8) showed lead concentrations near or below the minimum level of detection in both blood and tissue samples. Unlike findings in previous studies on avian scavengers, we did not find lead ammunition fragments to be a widespread source of lead exposure in large carnivores. Grizzly bears do, however, exhibit blood lead levels that are higher than what is considered safe in humans, but the source of this exposure remains unknown. © 2011 The Wildlife Society.     

Lead Bullet Fragments in Venison from Rifle-Killed Deer: Potential for Human Dietary Exposure

Human consumers of wildlife killed with lead ammunition may be exposed to health risks associated with lead ingestion. This hypothesis is based on published studies showing elevated blood lead concentrations in subsistence hunter populations, retention of ammunition residues in the tissues of hunter-killed animals, and systemic, cognitive, and behavioral disorders associated with human lead body burdens once considered safe. Our objective was to determine the incidence and bioavailability of lead bullet fragments in hunter-killed venison, a widely-eaten food among hunters and their families. We radiographed 30 eviscerated carcasses of White-tailed Deer (Odocoileus virginianus) shot by hunters with standard lead-core, copper-jacketed bullets under normal hunting conditions. All carcasses showed metal fragments (geometric mean = 136 fragments, range = 15–409) and widespread fragment dispersion. We took each carcass to a separate meat processor and fluoroscopically scanned the resulting meat packages; fluoroscopy revealed metal fragments in the ground meat packages of 24 (80%) of the 30 deer; 32% of 234 ground meat packages contained at least one fragment. Fragments were identified as lead by ICP in 93% of 27 samples. Isotope ratios of lead in meat matched the ratios of bullets, and differed from background lead in bone. We fed fragment-containing venison to four pigs to test bioavailability; four controls received venison without fragments from the same deer. Mean blood lead concentrations in pigs peaked at 2.29 µg/dL (maximum 3.8 µg/dL) 2 days following ingestion of fragment-containing venison, significantly higher than the 0.63 µg/dL averaged by controls. We conclude that people risk exposure to bioavailable lead from bullet fragments when they eat venison from deer killed with standard lead-based rifle bullets and processed under normal procedures. At risk in the U.S. are some ten million hunters, their families, and low-income beneficiaries of venison donations.     

Effects of Lead Exposure,Flock Behavior,and Management Actions on the Survival of California Condors (<Emphasis Type="Italic">Gymnogyps californianus</Emphasis>)

Translocation is an increasingly important tool for managing endangered species, but factors influencing the survival of translocated individuals are not well understood. Here we examine intrinsic and extrinsic drivers of survival for critically endangered California condors (Gymnogyps californianus) whose wild population recovery is reliant upon releases of captively bred stock. We used known fate models and information-theoretic methods to compare the ability of hypothesized covariates, most of which serve as proxies for lead exposure risk, to predict survival rates of condors in California. Our best supported model included the following predictors of survival: age of the recovery program, precipitation, proportion of days observed feeding on proffered carcasses, maximum blood lead concentration over the preceding 18 months, and time since release. We found that as flocks have increased in size and age, condors are increasingly likely to range more widely and less likely to be observed feeding on proffered food, and these “wilder” behaviors were associated with lower survival. After accounting for these behaviors, we found a positive survival trend, which we attribute to ongoing improvements in management. Our findings illustrate that the survival of translocated animals, such as highly social California condors, is influenced by behaviors that change through time.     

Lead poisoning in wild populations of Marsh Harriers Circus aeruginosus in the Camargue and Charente-Maritime, France

Lead poisoning of waterfowl, through the ingestion of spent gunshot, has been recognized as a mortality factor for over a century. However, in Europe relatively little attention has been paid to raptors that may ingest shot embedded in the flesh of prey. The present study examines the incidence of lead poisoning in wild Marsh Harriers Circus aeruginosus trapped at two sites in France, the Camargue and Charente-Maritime.
Eight captive Marsh Harriers (controls) had blood lead (PbB) concentrations of 5.3–10.8 μg per dl. Of 94 wild birds trapped during the winters of 1990/1991 and 1991/1992 either in baited clap traps or in mist nets at night roosts, 29 (31%) had elevated (>30 μg/dl) PbB concentrations and 13 (14%) had concentrations indicative of clinical poisoning (> 60 μg/dl). Similar percentages of birds caught using the two trapping methods had elevated (>30 μg/dl) PbB concentrations. However, clap netting appeared to select for more heavily contaminated birds and for juvenile birds, although the two are not necessarily correlated. In the Camargue, significantly more females than males trapped in clap nets had elevated PbB concentrations.
The incidence of shot in regurgitated Marsh Harrier pellets increased significantly between October and December, indicating increased exposure to lead as the hunting season progressed. There appeared to be a parallel increase in PbB concentrations throughout the hunting season, although this could not be clearly demonstrated as sex ratios were different during different sampling periods.
Elevated PbB concentrations of harriers in the Camargue are likely to result primarily from the ingestion of shot in the flesh of crippled or unretrieved waterfowl and in Charente-Maritime, from eating crippled or dead mammals.
Other raptors at risk from lead poisoning and solutions to this problem are discussed.