EcoHealth 10, 455–464, 2013 DOI: 10.1007/s10393-013-0896-5
Ó 2014 International Association for Ecology and Health
Review
Lead in Ammunition: A Persistent Threat to Health and Conservation C. K. Johnson,1 T. R. Kelly,1 and B. A. Rideout2 1
Wildlife Health Center, School of Veterinary Medicine, University of California, 1089 Veterinary Medicine Drive, Davis, CA 95616 Wildlife Disease Laboratories, Institute for Conservation Research, San Diego Zoo Global, PO Box 120551, San Diego, CA 92112
2
Abstract: 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. Keywords: lead, toxicosis, wildlife, scavenger, condor
As one of the very first species listed under the Endangered Species Protection Act of 1966, the California condor (Gymnogyps californianus) has benefitted from extraordinary recovery efforts involving captive breeding, reintroductions, and intensive management of free-flying populations. This highly collaborative effort highlights the extraordinary potential and the challenges involved in recovery of a critically endangered species. In the late 1980s California condors were extirpated from the wild in order to initiate a captive breeding program. Remarkably, the condor C. K. Johnson and T. R. Kelly contributed equally to this work. Published online: January 14, 2014 Correspondence to: C. K. Johnson, e-mail: [email protected]
population has now grown to over 200 free-flying individuals in the wild, with reintroduced populations free-flying in California, Arizona, Utah, and Baja California. However, condors require continued intensive management after release, and persistent threats in their environment impede the path toward a self-sustaining population (Finkelstein et al. 2012). Threats that contributed to the initial decline of this population are less well documented, but lead poisoning was a major concern and recognized as a cause of death among birds in the remnant wild population in the 1980s (Janssen et al. 1986). As a result of intensive monitoring of reintroduced condors, lead toxicosis is increasingly well documented in condors with extensive data indicating that lead exposure is endemic among re-introduced condor
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populations, lead toxicosis is the leading cause of mortality among adult condors, and intensive daily effort is necessary to manage this threat since reintroductions began in 1992 (Hunt et al. 2009; Walters et al. 2010; Finkelstein et al. 2012; Rideout et al. 2012). As obligate scavengers, condors feed solely on the remains of dead animals, a potentially risky prey base relative to live prey with regard to the prospect of exposure to significant levels of contaminants. Likely it is no coincidence that many vulture populations are experiencing abrupt declines across the globe, and poisoning following ingestion of toxins in contaminated carcasses ranks high among causes for declines (Ogada et al. 2012). Vulnerability of scavenging bird populations to contamination of their carcass prey base was well illustrated by the catastrophic decline of vultures across the Indian subcontinent due to diclofenac toxicosis, a common veterinary pharmaceutical used in livestock (Green et al. 2004; Oaks et al. 2004). Several Gyps species still remain at risk, despite rapid action by India, Pakistan, and Nepal to ban diclofenac manufacture for veterinary use only 2½ years after the cause of the declines was identified (Pain et al. 2008). Lead poisoning in scavenging birds has also been a focus of international attention, mainly because of documented effects on free-flying California condors (Fry and Maurer 2003; Hall et al. 2007; Hunt et al. 2007; Finkelstein et al. 2012). Cade (2007) provided a synthesis of evidence implicating lead from ammunition as a threat to condor recovery, and lead poisoning has been well documented in other obligate and opportunistic scavenging bird species throughout the world (Fisher et al. 2006; Pain et al. 2009). Potential population level effects have been described for species with low recruitment rates or small population sizes, such as bald eagles (Haliaeetus leucophalus), Stellar’s sea eagles (Haliaeetus pelagicus), white-tailed eagles (Haliaeetus albicilla), red kites (Milvus milvus), Spanish imperial eagles (Aquila adalberti), Griffon vultures (Gyps fulvus), and Egyptian vultures (Neophron percnopterus) (Pattee and Hennes 1983; Garcia-Fernandez et al. 2005; Pain et al. 2005; Cade 2007; Gangoso et al. 2009; Krone et al. 2009; Mateo 2009; Saito 2009). Mammalian scavenging species, such as mountain lions and bears, have also been exposed to lead from ammunition (Burco et al. 2012; Rattner et al. 2008). Lead exposure is a risk to all that consume an animal killed by lead-based ammunition, and here we summarize recent evidence for exposure to lead-based ammunition and health implications for many species.
SOURCES AND PATHWAYS OF LEAD EXPOSURE Point source lead exposure occurs when scavenging birds ingest lead pellets or fragments of lead bullets in prey animals or carcasses and discarded viscera from animals shot with lead ammunition (Platt 1976; Janssen et al. 1986; Craig et al. 1990; Gill and Langelier 1994; Kramer and Redig 1997; Locke and Thomas 1996; Pain et al. 2009; Mateo 2009; Saito 2009; Saggese et al. 2009). Lead poisoning associated with ingestion of spent ammunition was first linked to significant die-offs in waterfowl populations in the 1950s (Bellrose 1959; Bates et al. 1968; Irwin and Karstad 1972; Sanderson and Bellrose 1986). In 1976, a phase-in of non-lead (steel) ammunition was initiated for waterfowl hunting in the US, followed by a nationwide ban in 1991 (USFWS 2009). This legislation was enacted to protect waterfowl and endangered bald eagle populations experiencing secondary lead poisoning by feeding on injured and dead waterfowl containing lead ammunition (USFWS 1986; Kendall et al. 1996; Kramer and Redig 1997). Prior to the ban, an estimated 10–15% of documented post-fledging mortality in bald and golden eagles in the United States and Canada was attributed to lead poisoning from ingestion of lead ammunition in prey (Scheuhammer and Norris 1996; Clark and Scheuhammer 2003). While the ban on use of lead shot for hunting waterfowl had a major impact on decreasing waterfowl mortality from secondary lead poisoning (Anderson et al. 2000), the prevalence of lead poisoning in bald eagles did not decrease, indicating that carcasses contaminated with lead from other forms of hunting may be a significant source of lead exposure (Kramer and Redig 1997). Accidental consumption of lead fragments and ensuing intoxication in a scavenger is facilitated by the tendency of a lead bullet to fragment upon impact leaving hundreds of pieces surrounding the wound channel of the animal (Knopper et al. 2006; Hunt et al. 2006). The small irregularly shaped lead fragments are easily absorbed by digestion (Hunt et al. 2006). Depending on the species, lead fragments or pellets may be regurgitated, retained for varying periods of time in the gastrointestinal tract with gradual absorption, or completely dissolved, absorbed, and distributed in tissues (Fisher et al. 2006). Lead absorption depends on transit time through the gastrointestinal tract, the amount of lead ingested, and the surface area of the fragment (Pattee et al. 1981; Carpenter et al. 2003). The approximate half-life of lead following a point source
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exposure is measured in weeks for blood, months for soft tissues, and years for bone (Fry and Maurer 2003; Pain 1996). Directly observing the development of lead toxicosis and death in a free-ranging scavenging bird that has fed upon a carcass contaminated with lead ammunition is logistically impractical, especially given the expected lag time from lead exposure to subsequent debilitation (Pattee et al. 2006). Identification of the source of lead exposure after the development of toxicosis poses additional challenges because lead fragments can be regurgitated, completely absorbed, or be too small to be detected on radiographs. Nonetheless, evidence implicating lead ammunition as the main source of lead poisoning in wild birds is extensive, including (1) physical evidence of lead ammunition inside the gastrointestinal tracts of birds that have died or have been diagnosed with high blood lead levels (Platt 1976; Janssen et al. 1986; Craig et al. 1990; Gill and Langelier 1994; Locke and Thomas 1996; Kramer and Redig 1997; Parish et al. 2007; Pain et al. 2009; Mateo 2009; Saito 2009; Saggese et al. 2009; Rideout et al. 2012); (2) the relationship between foraging preferences for big game and lead-related mortality in an opportunistic scavenger (Nadjafzadeh et al. 2013); (3) correlation of stable lead isotopes between blood/feather and ammunition samples (Lambertucci et al. 2011; Cruz-Martinez et al. 2012; Finkelstein et al. 2012); and (4) spatial and temporal associations between lead exposure in scavenging birds and big game hunting activities. To identify spatial and temporal patterns in lead exposure, large scale investigative efforts involving capture of free-flying birds or sampling of birds admitted to rehabilitation centers are often necessary. Nonetheless, a link between lead exposure and big game hunting has been described in many species. For example, blood lead concentrations in California condors have been documented to be highest during the deer hunting season (Hall et al. 2007; Parish et al. 2007; Sorenson and Burnett 2007), and in Arizona and Utah, peak blood lead levels are associated with specific movements of the population to an area with high deer hunting pressure (Hunt et al. 2007). Correlations between lead exposure and big game hunting activities have been described for turkey vultures and golden eagles and turkey vulture blood lead concentrations were positively correlated with a gradient of increasing wild pig hunting intensity in California (Kelly and Johnson 2011; Kelly et al. 2011). Among turkey vultures captured at a single site with
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high intensity deer hunting, blood lead concentrations were 3 fold higher among vultures captured during the deer hunting season compared to outside of the deer hunting season (Kelly and Johnson 2011). Bald and golden eagles admitted to a raptor rehabilitation center in the Pacific Northwest had elevated blood lead concentrations coincident with the end of deer and elk hunting season and high coyote hunting intensity (Stauber et al. 2010). Similar temporal and spatial correlations with big game hunting activities have also been documented in bald and golden eagles in the Midwestern United States (Kramer and Redig 1997; Strom et al. 2009; Neumann 2009; Cruz-Martinez et al. 2012) and common ravens and bald eagles in the Greater Yellowstone area (Craighead and Bedrosian 2009). Gangoso et al. (2009) compared blood lead concentrations in free-ranging Egyptian vulture populations with differing exposures to hunter-killed carrion and found that lead concentrations were significantly higher in resident vultures in the population with greater access to lead ammunition fragments in hunter-killed carrion, with peak exposures during winter hunting activities (Gangoso et al. 2009). Hunted big game carcasses are not the only plausible source of lead ammunition available to scavenging birds and other, potentially year-round sources of lead ammunition include non-game animal hunting, depredation or encounter shooting of wildlife on private land, euthanization of farm animals by gunshot, and shooting at outdoor shooting ranges (Kelly and Johnson 2011). Ammunition casings have been identified in condor chicks with impacted stomachs (Mee et al. 2007) suggesting that lead ammunition deposited on the landscape can find its way into scavenging birds that pick up and ingest trash. A detailed examination of the evidence implicating spent lead ammunition as a source of lead exposure in condors was summarized by Cade (2007), and this review, along with independent investigations in a range of wild bird species, indicate that lead-based ammunition is a pervasive source of high levels of lead exposure beyond the level of exposure that could come from environmental background sources.
Health Effects of Lead Exposure Lead can cause a myriad of harmful health effects in animals and people through interference of normal enzymatic reactions (Pearson and Schonfeld 2003; Kosnett 2006).
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Lead has documented toxic effects on multiple organ systems in people, including the cardiovascular, reproductive, hematopoietic, renal, and neurological systems (ATSDR 2007). Effects on the nervous system can be particularly serious, resulting in impaired motor function. A range of sublethal symptoms have also been described in humans at relatively low levels of exposure, including cognitive impairment at blood lead concentrations 100 lg/dL) in 14% of individuals (Bedrosian and Craighead 2009, Bedrosian et al. 2012). In Japan, significant mortality of white-tailed eagles and Stellar’s seaeagles wintering on the island of Hokkaido has been attributed to lead poisoning from feeding on hunter killed Sika deer (Cervus Nippon; Saito 2009).
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Lead Ammunition and Public Health Significance In 2010, the Centers for Disease Control (CDC) established a working group to re-evaluate the threshold lead concentration for interventions and concluded that there is no safe level of lead exposure (Canfield et al. 2003; CDC 2005; Lanphear et al. 2005; Carlisle et al. 2009) based on research suggesting that concentrations 10 lg/dL) in non-migrant golden eagles and up to 83% in turkey vultures sampled, suggesting that lead ammunition regulations may be effective for reducing lead exposure in scavenging birds within some areas of the condor range in California (Kelly et al. 2011). However, lead exposure remains a serious threat to the condor population following implementation of regulations in California. Eliminating the threat of lead poisoning in condors may be especially challenging, because this species is spectacularly wide ranging in its foraging ecology and, as individuals become increasingly independent, the population will be less aided by proffered feeding programs in California. Voluntary lead reduction programs have also been implemented to reduce lead exposure in condors in Arizona and Utah. The Arizona Game and Fish Department initiated a public education campaign in 2003 promoting the voluntary use of non-lead ammunition for hunting within the condor range in Arizona (Sieg et al. 2009). Hunter education and outreach programs in Arizona have had 80–90% participation by deer hunters since 2007, however, participation has only been 5% in Utah where outreach efforts are still in their infancy (Sieg et al. 2009; Austin et al. 2012). Although voluntary lead reduction efforts have significantly reduced the amount of lead available to condors in Arizona (Green et al. 2009; Sieg et al. 2009), these programs have not yet led to significant reductions in lead exposure in this population (Green et al. 2009; Austin et al. 2012). Since 2005, condors have increased their foraging in southern Utah, which may explain why lead exposure has not yet declined (Austin et al. 2012). In contrast, hunter outreach including non-lead ammunition provisioning programs succeeded in significantly reducing lead exposure in bald eagles feeding on hunter-killed big game in Jackson Hole Valley (Bedrosian et al. 2012). Unlike the condor range in California, where there are a variety of shooting activities including year-round hunting and shooting of wildlife for depredation on private lands, seasonal big game hunting is the principal source of lead to scavenging birds and there is no non-game animal or predator shooting in this area in Wyoming (Bedrosian et al. 2012). Outreach initiatives to
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minimize use of lead-based ammunition in California must address a wide variety of shooting activities, including yearround hunting and shooting of nuisance wildlife for depredation on private lands.
to this work. Views presented by the coauthors do not necessarily represent the views of the Condor Recovery Program or US Fish and Wildlife Service.
Future Approaches
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The challenges facing obligate scavenger populations that are declining across the globe require a transdisciplinary approach to investigating threats in their environment. Lead poisoning from lead-based ammunition remains a serious impediment to condor recovery and the persistent threat of lead exposure to scavenging wildlife, along with the risk posed to public health, highlight the need for education and outreach, regardless of local restrictions on the use of leadbased ammunition. In California and elsewhere, there is the need to engage a diverse group of stakeholders including hunters, landowners, and livestock ranchers. Lead-free ammunition is increasingly available for a wide range of bullet and slug calibers that meet accuracy and safety standards (Thomas 2013). Education efforts are best done collaboratively with key stakeholders to address concerns, disbeliefs, and key issues brought forth by participants, whose attitudes are likely to evolve over time (Ross-Winslow and Teel 2011). To maximize the impacts of outreach efforts, information is needed on stakeholders’ knowledge of and attitudes toward the adverse effects of lead on health and options for lead reduction in the environment. An assessment of existing outreach efforts is also critical to inform on future programs. Solutions to this problem will require highly effective communication and translation of science across the many disciplines informing on this issue. One Health approaches are classically applied to infectious disease problems, but toxins also affect many species and can impact ecosystem health. Lead-based ammunition is a problem best solved by involving key stakeholders in One Health solutions that consider the risks of lead to wildlife, human, and environmental health.
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Ó 2014 International Association for Ecology and Health
Review
Lead in Ammunition: A Persistent Threat to Health and Conservation C. K. Johnson,1 T. R. Kelly,1 and B. A. Rideout2 1
Wildlife Health Center, School of Veterinary Medicine, University of California, 1089 Veterinary Medicine Drive, Davis, CA 95616 Wildlife Disease Laboratories, Institute for Conservation Research, San Diego Zoo Global, PO Box 120551, San Diego, CA 92112
2
Abstract: 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. Keywords: lead, toxicosis, wildlife, scavenger, condor
As one of the very first species listed under the Endangered Species Protection Act of 1966, the California condor (Gymnogyps californianus) has benefitted from extraordinary recovery efforts involving captive breeding, reintroductions, and intensive management of free-flying populations. This highly collaborative effort highlights the extraordinary potential and the challenges involved in recovery of a critically endangered species. In the late 1980s California condors were extirpated from the wild in order to initiate a captive breeding program. Remarkably, the condor C. K. Johnson and T. R. Kelly contributed equally to this work. Published online: January 14, 2014 Correspondence to: C. K. Johnson, e-mail: [email protected]
population has now grown to over 200 free-flying individuals in the wild, with reintroduced populations free-flying in California, Arizona, Utah, and Baja California. However, condors require continued intensive management after release, and persistent threats in their environment impede the path toward a self-sustaining population (Finkelstein et al. 2012). Threats that contributed to the initial decline of this population are less well documented, but lead poisoning was a major concern and recognized as a cause of death among birds in the remnant wild population in the 1980s (Janssen et al. 1986). As a result of intensive monitoring of reintroduced condors, lead toxicosis is increasingly well documented in condors with extensive data indicating that lead exposure is endemic among re-introduced condor
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populations, lead toxicosis is the leading cause of mortality among adult condors, and intensive daily effort is necessary to manage this threat since reintroductions began in 1992 (Hunt et al. 2009; Walters et al. 2010; Finkelstein et al. 2012; Rideout et al. 2012). As obligate scavengers, condors feed solely on the remains of dead animals, a potentially risky prey base relative to live prey with regard to the prospect of exposure to significant levels of contaminants. Likely it is no coincidence that many vulture populations are experiencing abrupt declines across the globe, and poisoning following ingestion of toxins in contaminated carcasses ranks high among causes for declines (Ogada et al. 2012). Vulnerability of scavenging bird populations to contamination of their carcass prey base was well illustrated by the catastrophic decline of vultures across the Indian subcontinent due to diclofenac toxicosis, a common veterinary pharmaceutical used in livestock (Green et al. 2004; Oaks et al. 2004). Several Gyps species still remain at risk, despite rapid action by India, Pakistan, and Nepal to ban diclofenac manufacture for veterinary use only 2½ years after the cause of the declines was identified (Pain et al. 2008). Lead poisoning in scavenging birds has also been a focus of international attention, mainly because of documented effects on free-flying California condors (Fry and Maurer 2003; Hall et al. 2007; Hunt et al. 2007; Finkelstein et al. 2012). Cade (2007) provided a synthesis of evidence implicating lead from ammunition as a threat to condor recovery, and lead poisoning has been well documented in other obligate and opportunistic scavenging bird species throughout the world (Fisher et al. 2006; Pain et al. 2009). Potential population level effects have been described for species with low recruitment rates or small population sizes, such as bald eagles (Haliaeetus leucophalus), Stellar’s sea eagles (Haliaeetus pelagicus), white-tailed eagles (Haliaeetus albicilla), red kites (Milvus milvus), Spanish imperial eagles (Aquila adalberti), Griffon vultures (Gyps fulvus), and Egyptian vultures (Neophron percnopterus) (Pattee and Hennes 1983; Garcia-Fernandez et al. 2005; Pain et al. 2005; Cade 2007; Gangoso et al. 2009; Krone et al. 2009; Mateo 2009; Saito 2009). Mammalian scavenging species, such as mountain lions and bears, have also been exposed to lead from ammunition (Burco et al. 2012; Rattner et al. 2008). Lead exposure is a risk to all that consume an animal killed by lead-based ammunition, and here we summarize recent evidence for exposure to lead-based ammunition and health implications for many species.
SOURCES AND PATHWAYS OF LEAD EXPOSURE Point source lead exposure occurs when scavenging birds ingest lead pellets or fragments of lead bullets in prey animals or carcasses and discarded viscera from animals shot with lead ammunition (Platt 1976; Janssen et al. 1986; Craig et al. 1990; Gill and Langelier 1994; Kramer and Redig 1997; Locke and Thomas 1996; Pain et al. 2009; Mateo 2009; Saito 2009; Saggese et al. 2009). Lead poisoning associated with ingestion of spent ammunition was first linked to significant die-offs in waterfowl populations in the 1950s (Bellrose 1959; Bates et al. 1968; Irwin and Karstad 1972; Sanderson and Bellrose 1986). In 1976, a phase-in of non-lead (steel) ammunition was initiated for waterfowl hunting in the US, followed by a nationwide ban in 1991 (USFWS 2009). This legislation was enacted to protect waterfowl and endangered bald eagle populations experiencing secondary lead poisoning by feeding on injured and dead waterfowl containing lead ammunition (USFWS 1986; Kendall et al. 1996; Kramer and Redig 1997). Prior to the ban, an estimated 10–15% of documented post-fledging mortality in bald and golden eagles in the United States and Canada was attributed to lead poisoning from ingestion of lead ammunition in prey (Scheuhammer and Norris 1996; Clark and Scheuhammer 2003). While the ban on use of lead shot for hunting waterfowl had a major impact on decreasing waterfowl mortality from secondary lead poisoning (Anderson et al. 2000), the prevalence of lead poisoning in bald eagles did not decrease, indicating that carcasses contaminated with lead from other forms of hunting may be a significant source of lead exposure (Kramer and Redig 1997). Accidental consumption of lead fragments and ensuing intoxication in a scavenger is facilitated by the tendency of a lead bullet to fragment upon impact leaving hundreds of pieces surrounding the wound channel of the animal (Knopper et al. 2006; Hunt et al. 2006). The small irregularly shaped lead fragments are easily absorbed by digestion (Hunt et al. 2006). Depending on the species, lead fragments or pellets may be regurgitated, retained for varying periods of time in the gastrointestinal tract with gradual absorption, or completely dissolved, absorbed, and distributed in tissues (Fisher et al. 2006). Lead absorption depends on transit time through the gastrointestinal tract, the amount of lead ingested, and the surface area of the fragment (Pattee et al. 1981; Carpenter et al. 2003). The approximate half-life of lead following a point source
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exposure is measured in weeks for blood, months for soft tissues, and years for bone (Fry and Maurer 2003; Pain 1996). Directly observing the development of lead toxicosis and death in a free-ranging scavenging bird that has fed upon a carcass contaminated with lead ammunition is logistically impractical, especially given the expected lag time from lead exposure to subsequent debilitation (Pattee et al. 2006). Identification of the source of lead exposure after the development of toxicosis poses additional challenges because lead fragments can be regurgitated, completely absorbed, or be too small to be detected on radiographs. Nonetheless, evidence implicating lead ammunition as the main source of lead poisoning in wild birds is extensive, including (1) physical evidence of lead ammunition inside the gastrointestinal tracts of birds that have died or have been diagnosed with high blood lead levels (Platt 1976; Janssen et al. 1986; Craig et al. 1990; Gill and Langelier 1994; Locke and Thomas 1996; Kramer and Redig 1997; Parish et al. 2007; Pain et al. 2009; Mateo 2009; Saito 2009; Saggese et al. 2009; Rideout et al. 2012); (2) the relationship between foraging preferences for big game and lead-related mortality in an opportunistic scavenger (Nadjafzadeh et al. 2013); (3) correlation of stable lead isotopes between blood/feather and ammunition samples (Lambertucci et al. 2011; Cruz-Martinez et al. 2012; Finkelstein et al. 2012); and (4) spatial and temporal associations between lead exposure in scavenging birds and big game hunting activities. To identify spatial and temporal patterns in lead exposure, large scale investigative efforts involving capture of free-flying birds or sampling of birds admitted to rehabilitation centers are often necessary. Nonetheless, a link between lead exposure and big game hunting has been described in many species. For example, blood lead concentrations in California condors have been documented to be highest during the deer hunting season (Hall et al. 2007; Parish et al. 2007; Sorenson and Burnett 2007), and in Arizona and Utah, peak blood lead levels are associated with specific movements of the population to an area with high deer hunting pressure (Hunt et al. 2007). Correlations between lead exposure and big game hunting activities have been described for turkey vultures and golden eagles and turkey vulture blood lead concentrations were positively correlated with a gradient of increasing wild pig hunting intensity in California (Kelly and Johnson 2011; Kelly et al. 2011). Among turkey vultures captured at a single site with
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high intensity deer hunting, blood lead concentrations were 3 fold higher among vultures captured during the deer hunting season compared to outside of the deer hunting season (Kelly and Johnson 2011). Bald and golden eagles admitted to a raptor rehabilitation center in the Pacific Northwest had elevated blood lead concentrations coincident with the end of deer and elk hunting season and high coyote hunting intensity (Stauber et al. 2010). Similar temporal and spatial correlations with big game hunting activities have also been documented in bald and golden eagles in the Midwestern United States (Kramer and Redig 1997; Strom et al. 2009; Neumann 2009; Cruz-Martinez et al. 2012) and common ravens and bald eagles in the Greater Yellowstone area (Craighead and Bedrosian 2009). Gangoso et al. (2009) compared blood lead concentrations in free-ranging Egyptian vulture populations with differing exposures to hunter-killed carrion and found that lead concentrations were significantly higher in resident vultures in the population with greater access to lead ammunition fragments in hunter-killed carrion, with peak exposures during winter hunting activities (Gangoso et al. 2009). Hunted big game carcasses are not the only plausible source of lead ammunition available to scavenging birds and other, potentially year-round sources of lead ammunition include non-game animal hunting, depredation or encounter shooting of wildlife on private land, euthanization of farm animals by gunshot, and shooting at outdoor shooting ranges (Kelly and Johnson 2011). Ammunition casings have been identified in condor chicks with impacted stomachs (Mee et al. 2007) suggesting that lead ammunition deposited on the landscape can find its way into scavenging birds that pick up and ingest trash. A detailed examination of the evidence implicating spent lead ammunition as a source of lead exposure in condors was summarized by Cade (2007), and this review, along with independent investigations in a range of wild bird species, indicate that lead-based ammunition is a pervasive source of high levels of lead exposure beyond the level of exposure that could come from environmental background sources.
Health Effects of Lead Exposure Lead can cause a myriad of harmful health effects in animals and people through interference of normal enzymatic reactions (Pearson and Schonfeld 2003; Kosnett 2006).
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Lead has documented toxic effects on multiple organ systems in people, including the cardiovascular, reproductive, hematopoietic, renal, and neurological systems (ATSDR 2007). Effects on the nervous system can be particularly serious, resulting in impaired motor function. A range of sublethal symptoms have also been described in humans at relatively low levels of exposure, including cognitive impairment at blood lead concentrations 100 lg/dL) in 14% of individuals (Bedrosian and Craighead 2009, Bedrosian et al. 2012). In Japan, significant mortality of white-tailed eagles and Stellar’s seaeagles wintering on the island of Hokkaido has been attributed to lead poisoning from feeding on hunter killed Sika deer (Cervus Nippon; Saito 2009).
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Lead Ammunition and Public Health Significance In 2010, the Centers for Disease Control (CDC) established a working group to re-evaluate the threshold lead concentration for interventions and concluded that there is no safe level of lead exposure (Canfield et al. 2003; CDC 2005; Lanphear et al. 2005; Carlisle et al. 2009) based on research suggesting that concentrations 10 lg/dL) in non-migrant golden eagles and up to 83% in turkey vultures sampled, suggesting that lead ammunition regulations may be effective for reducing lead exposure in scavenging birds within some areas of the condor range in California (Kelly et al. 2011). However, lead exposure remains a serious threat to the condor population following implementation of regulations in California. Eliminating the threat of lead poisoning in condors may be especially challenging, because this species is spectacularly wide ranging in its foraging ecology and, as individuals become increasingly independent, the population will be less aided by proffered feeding programs in California. Voluntary lead reduction programs have also been implemented to reduce lead exposure in condors in Arizona and Utah. The Arizona Game and Fish Department initiated a public education campaign in 2003 promoting the voluntary use of non-lead ammunition for hunting within the condor range in Arizona (Sieg et al. 2009). Hunter education and outreach programs in Arizona have had 80–90% participation by deer hunters since 2007, however, participation has only been 5% in Utah where outreach efforts are still in their infancy (Sieg et al. 2009; Austin et al. 2012). Although voluntary lead reduction efforts have significantly reduced the amount of lead available to condors in Arizona (Green et al. 2009; Sieg et al. 2009), these programs have not yet led to significant reductions in lead exposure in this population (Green et al. 2009; Austin et al. 2012). Since 2005, condors have increased their foraging in southern Utah, which may explain why lead exposure has not yet declined (Austin et al. 2012). In contrast, hunter outreach including non-lead ammunition provisioning programs succeeded in significantly reducing lead exposure in bald eagles feeding on hunter-killed big game in Jackson Hole Valley (Bedrosian et al. 2012). Unlike the condor range in California, where there are a variety of shooting activities including year-round hunting and shooting of wildlife for depredation on private lands, seasonal big game hunting is the principal source of lead to scavenging birds and there is no non-game animal or predator shooting in this area in Wyoming (Bedrosian et al. 2012). Outreach initiatives to
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minimize use of lead-based ammunition in California must address a wide variety of shooting activities, including yearround hunting and shooting of nuisance wildlife for depredation on private lands.
to this work. Views presented by the coauthors do not necessarily represent the views of the Condor Recovery Program or US Fish and Wildlife Service.
Future Approaches
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The challenges facing obligate scavenger populations that are declining across the globe require a transdisciplinary approach to investigating threats in their environment. Lead poisoning from lead-based ammunition remains a serious impediment to condor recovery and the persistent threat of lead exposure to scavenging wildlife, along with the risk posed to public health, highlight the need for education and outreach, regardless of local restrictions on the use of leadbased ammunition. In California and elsewhere, there is the need to engage a diverse group of stakeholders including hunters, landowners, and livestock ranchers. Lead-free ammunition is increasingly available for a wide range of bullet and slug calibers that meet accuracy and safety standards (Thomas 2013). Education efforts are best done collaboratively with key stakeholders to address concerns, disbeliefs, and key issues brought forth by participants, whose attitudes are likely to evolve over time (Ross-Winslow and Teel 2011). To maximize the impacts of outreach efforts, information is needed on stakeholders’ knowledge of and attitudes toward the adverse effects of lead on health and options for lead reduction in the environment. An assessment of existing outreach efforts is also critical to inform on future programs. Solutions to this problem will require highly effective communication and translation of science across the many disciplines informing on this issue. One Health approaches are classically applied to infectious disease problems, but toxins also affect many species and can impact ecosystem health. Lead-based ammunition is a problem best solved by involving key stakeholders in One Health solutions that consider the risks of lead to wildlife, human, and environmental health.
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ACKNOWLEDGEMENTS We thank the editor for inviting this review. We acknowledge the Condor Recovery Team and the many agencies, organizations, and individuals who have dedicated their time to recovery of this species. We also thank Eric Loft, Steve Torres, Jesse Grantham, Walter Boyce, Robert Poppenga, and Tamara Vodovoz for their contributions
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