EcoHealth

, Volume 10, Issue 4, pp 455–464

Lead in Ammunition: A Persistent Threat to Health and Conservation

Authors

    • Wildlife Health Center, School of Veterinary MedicineUniversity of California
  • T. R. Kelly
    • Wildlife Health Center, School of Veterinary MedicineUniversity of California
  • B. A. Rideout
    • Wildlife Disease Laboratories, Institute for Conservation ResearchSan Diego Zoo Global
Review

DOI: 10.1007/s10393-013-0896-5

Cite this article as:
Johnson, C.K., Kelly, T.R. & Rideout, B.A. EcoHealth (2013) 10: 455. doi:10.1007/s10393-013-0896-5

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

leadtoxicosiswildlifescavengercondor

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 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 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 (Milvusmilvus), 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 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 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). 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 <10 μg/dL (Lanphear et al. 2005). Large epidemiological studies, facilitated by access to medical care and diagnostics, were used to identify the wide range of sublethal effects of lead in humans. Comparable investigative efforts would be very difficult to conduct in free-ranging wild animals. However, there is every reason to suspect that similar sublethal effects occur with low level lead exposure in all species (Pokras and Kneeland 2008, Hunt 2012).

The amount of ingested lead necessary for specific clinical or pathological manifestations of intoxication varies by species and individual factors such as nutritional status, genetic predisposition, and co-morbidities influence the development of disease (Pain 1996; Pattee et al. 2006). Effects may be acute if a high level of exposure leads to death in a short period of time, or chronic from repeat low-level exposure over a prolonged period with lead accumulation in tissues. Clinical signs documented in birds include weakness, starvation, debilitation, impaired neurological function, and eventually death in some cases (Hoffmann et al. 1981; Pattee et al. 1981; Reiser and Temple 1981; Sanderson and Bellrose 1986; Redig et al. 1991; Beyer et al. 1998; Carpenter et al. 2003).

Lead Toxicosis in California Condors

Lead exposure from lead-based ammunition is endemic in free-flying California condors (Hall et al. 2007; Parish et al. 2007; Sorenson and Burnett 2007; Finkelstein et al. 2012). The annual prevalence of blood lead levels exceeding 10 μg/dL ranged from 50 to 88% among condors sampled in California between 1997 and 2010 (Finkelstein et al. 2012). Since 2002, annual blood lead screening of condors in Arizona, showed greater than 60% of samples with elevated lead exposure (Parish et al. 2007; Austin et al. 2012). California condors are routinely captured and screened for lead poisoning multiple times each year, and individuals showing signs of illness or injury are also captured and tested for lead exposure. Birds with elevated values are treated by chelation. Over the course of the reintroduction program (1997–2010) approximately 48% of free-flying condors were in need of treatment because of blood lead levels exceeding a threshold of 45 μg/dL (Finkelstein et al. 2012). Despite intensive management efforts, during the first 17 years of the California condor reintroduction program (1992–2009), 23 juvenile or adult birds died from lead poisoning, making it the most significant cause of mortality in these age classes among birds released in California, Arizona, and Baja (35% of the mortalities; Rideout et al. 2012). More importantly, of the 15 adult condors with an established cause of death, 10 died of lead poisoning (67%). From 2010–2012, there were 22 additional adult condor deaths. Of the 18 adult condors with a known cause of death, 15 died of lead poisoning (83%; Rideout, unpublished). Because adult mortalities have the greatest impact on population viability in long-lived, slowly reproducing species, it is apparent that lead poisoning from ingested lead ammunition is by far the most significant mortality factor for the free-ranging California condor population. As the proportion of adult, independently feeding birds in the free-ranging population continues to increase, the threat of lead exposure will require ongoing program investment through intense monitoring and routine screening of the population for lead exposure, with hospitalization and treatment of poisoned individuals. Long-term intensive management, which includes a proffered feeding program, is not compatible with establishment of a self-sufficient free-flying population, and the potential health and behavioral consequences of capture and captive treatment of sick birds must be weighed against the benefit of life-saving treatment of poisoned individuals (Cade 2007; Rideout et al. 2012).

Analyses of sequential feather sample measurements indicate that condors are lead poisoned for an average of 34% of the time of feather growth, or approximately one month after an acute lead exposure event (Finkelstein et al. 2012). Because lead is rapidly eliminated from blood, intermittent sampling for measurement of blood lead levels underestimates the true incidence and peak magnitude of lead exposure. However, a dedicated effort is made to investigate suspected poisoning events in individual condors based on observations of high risk foraging activities and changes in behavior indicative of toxicosis. Furthermore, the majority of individuals in the population are sampled at least once a year for a near perfect recapture rate, which is an exceedingly rare achievement for a free-ranging wild animal population and only achievable for small populations that are intensively managed in a way that insures high recapture rates. Because condors are intensively monitored and they use wide ranging foraging techniques to locate carcasses across the landscape, this species is a particularly excellent sentinel for lead contamination of carcasses throughout their range.

The impact of lead toxicosis on free-ranging wildlife populations is inherently more difficult to document in species that are less well monitored. Studies estimating point prevalence of lead exposure by capturing free-ranging animals and measuring blood lead levels target apparently healthy free-flying animals and assess only very recent exposure to lead, therefore under-estimating the overall burden of lead toxicosis in a population (Kelly and Johnson 2011). Studies that evaluate blood lead exposure in dead and moribund wildlife target the fraction of the population in which clinical lead toxicosis manifests, but these studies typically rely on members of the public to find and submit animals to rehabilitation centers or other facilities, and therefore preferentially select animals with conditions common in the suburban and peri-urban environment, where hunting activities are less common.

Nonetheless, lead poisoning has been identified as a widespread cause of death among many other species of scavenging birds around the world. Among 600 dead bald eagles in the Midwestern United States that were submitted for post-mortem examination, at least 16% were documented with lead toxicosis as a cause of death (Strom et al. 2009). A study assessing lead poisoning in bald and golden eagles admitted to a raptor rehabilitation clinic in Minnesota over a 16 year period showed that 21% (138/654) of eagles had evidence of lead poisoning (Kramer and Redig 1997). Wayland (1999) documented lethal lead poisoning in 12% of 127 dead or moribund bald and golden eagles (Aquila chrysateos) in the Canadian Prairie Provinces. In a more recent study by Wayland et al. (2003), including 372 bald and golden eagles from western Canada, 10% were diagnosed as lead poisoned. Similar results were documented in bald eagles originating from British Columbia where 37% of 65 exhibited significant lead exposure and 14% were classified as lead poisoned (Miller et al. 2001). Live caught bald and golden eagles in Wyoming had elevated blood lead concentrations consistent with clinical poisoning (>100 μg/dL) in 14% of individuals (Bedrosian and Craighead 2009, Bedrosian et al. 2012). In Japan, significant mortality of white-tailed eagles and Stellar’s sea-eagles wintering on the island of Hokkaido has been attributed to lead poisoning from feeding on hunter killed Sika deer (Cervus Nippon; Saito 2009).

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 μg/dL have adverse effects on intellectual and socio-behavioral development in humans (Needleman et al. 1990; Nevin 2000; Needleman et al. 2002; Canfield et al. 2003; Needleman 2004; Ris et al. 2004; Braun et al. 2006). From a public health perspective, lead exposure in pregnant women and children is of particular concern because of serious central nervous system disorders that may occur during development of the fetus and young child (Sowers et al. 2002). Regulations exist for lead used in industrial activities, manufacture of consumer products, and more recently lead used at indoor and outdoor shooting ranges (US EPA 2001; NIOSH 2010), however, there have been no major public health interventions to address risks associated with consumption of lead-based ammunition in game meat in the US. Some subsistence hunting communities have been shown to have increased prevalence of elevated blood lead concentrations and retained lead pellets in their digestive tracts (Tsuji and Nieboer 1997; Levesque 2003; Bjerregaard et al. 2004; Walker et al. 2006; Tsuji et al. 2008). Case reports have also documented marked lead exposure associated with lead pellet retention in the gastrointestinal tract of occasional consumers of hunter-harvested meat (Hillman 1967; Durlach et al. 1986; Gustavsson and Gerhardsson 2005). The North Dakota Department of Health (NDDH) and the CDC conducted a study evaluating blood lead concentrations in individuals from a convenience sample of the US population, 81% of which reported a history of consuming wild game (Iqbal 2008). A small increase in blood lead concentration was associated with wild game consumption in this study. Studies have documented that deer and elk harvested by licensed hunters with lead projectiles contain lead fragments along the bullet channel wound and surrounding tissues (Hunt et al. 2006; Hunt et al. 2009), and a study found that 56% (53/95) of ground venison donated to food pantries contained lead fragments (NDDH 2008). Furthermore, lead concentrations in the meat of waterfowl and upland game harvested with lead shot have been documented to be significantly elevated, even after lead pellets were removed (Johansen 2004; Mateo et al. 2007; Pain et al. 2010).

Lead Ammunition Reduction Efforts to Benefit Wildlife

Eliminating the hazards of lead exposure for scavenging wildlife requires a complete transition to non-lead ammunition for shooting animals that may serve as food sources for scavengers. Lead ammunition reduction programs include both regulatory and voluntary measures (Avery and Watson 2009; Ross-Winslow and Teel 2011). While lead-based shot has been banned for waterfowl hunting in several countries around the world, regulation of lead ammunition for other types of hunting activities is more limited in scope, with the exception of Sweden and Denmark, where restrictions exist for all hunting activities (Avery and Watson 2009). In North America, with the exception of hunting on federal lands, hunting regulations fall under state and provincial jurisdiction, leading to significant variation in ammunition restrictions across the continent (Rattner et al. 2008). Possibly, the most noteworthy regulation of lead ammunition for hunting outside of the federal ban of lead shot for waterfowl hunting has occurred recently in California. Lead ammunition was banned for big game and non-game hunting activities in the state’s range of the California condor in July, 2008 (CDFW 2008, Ridley-Tree Condor Preservation Act 2008). Most recently, a bill was passed that will prohibit the use of lead ammunition for take of wildlife statewide in California (State Assembly Bill 711, October 2013). As early as 2004, surveys and focus group meetings were conducted by federal agencies to gather baseline information about hunter and private landowner knowledge of and attitudes toward the issue of lead poisoning in the California condor in order to develop an effective communications plan for key audiences (Sieg et al. 2009). Various localized hunter outreach efforts emerged within the condor range in California to provide hunters and landowners with information about lead poisoning in scavenging birds and to promote the use of non-lead ammunition. These outreach efforts included shooting clinics to familiarize hunters and landowners with the types of non-lead ammunition available to them and a non-lead ammunition giveaway program for hunters in central California (Institute for Wildlife Studies 2009; Ventana Wildlife Society 2012). So far, these efforts have been localized, and there have not yet been any broad scale efforts in California to widely disseminate free non-lead ammunition or engage shooters outside of the hunting community through outreach and education programs.

Blood lead concentrations significantly declined in both eagles and vultures in the year immediately following implementation of lead ammunition regulations in California with a 100% reduction in the prevalence of elevated lead exposure (>10 μg/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 minimize use of lead-based ammunition in California must address a wide variety of shooting activities, including year-round hunting and shooting of nuisance wildlife for depredation on private lands.

Future Approaches

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 lead-based 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.

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 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.

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© International Association for Ecology and Health 2014