Are there legitimate reasons to retain lead ammunition and fishing gear?

Robert H. PoppengaCalifornia Animal Health and Food Safety Laboratory, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Pat T. RedigVeterinary Clinical Sciences Department, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN 55108.

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James G. SikarskieVeterinary Medical Center, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

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Recently, an adult turkey vulture was submitted to a local wildlife care and rehabilitation center after being found in a yard, unable to fly. A radiograph taken at the center showed a metallic object in the stomach. Despite treatment, the bird died and was submitted to the California Animal Health and Food Safety Laboratory in Davis, California, for necropsy. A metal foreign object that appeared to be a bullet fragment was found in the gizzard on postmortem examination, and heavy metal analysis detected lead (18 μg/g [ppm]) in the liver. Because liver lead concentrations in the range of 2 to 10 μg/g are considered consistent with lead intoxication, depending on the species exposed,1 lead intoxication was concluded to be the cause of death. Unfortunately, such cases are common at veterinary diagnostic laboratories throughout the United States.

Lead has been used for a variety of purposes for thousands of years. It is easy to extract, highly malleable, and inexpensive. Inorganic lead has been used as pigments in paint, dyes, and ceramic glazes, and lead-containing organic compounds were once widely used as a gasoline additive. Lead combined with other metals forms alloys that have been used in batteries, radiation shields, water pipes, ammunition, and fishing tackle.

Although it is a naturally occurring element in the environment, lead has no functional role in biological systems and is toxic at low doses. In fact, no safe level of exposure has been identified for sensitive human populations such as children, and lead remains a serious public health concern despite restrictions on its use in products such as paint and gasoline. There is no threshold of measurable blood lead concentration below which toxic effects have not been identified. In children, even limited exposure to lead can result in damage to the CNS with long-term effects on mental development and psychomotor skills.2 Many other organ systems can also be adversely affected, including the hematopoietic, renal, cardiovascular, immune, and gastrointestinal systems. Before restrictions were placed on lead use in paint and other products, acute and chronic intoxications were common in dogs and cats. Lead intoxication of pets is relatively infrequent now, but cases of acute lead intoxication in ruminants, particularly cattle, still occur. Most commonly these are a result of ingestion of lead fragments from old vehicular battery plates. Currently, most cases of lead intoxication in animals involve a variety of wild bird species, particularly scavengers or fish-eating species.3,4

At toxic blood and tissue concentrations in birds, lead causes lethargy, gastrointestinal stasis, anorexia, vomiting, diarrhea, anemia, disturbances of cellular metabolic functions, and neurologic injury, leading to blindness, seizures, weakness, and death.5–8 At lower concentrations, lead exposure causes a number of sublethal effects, such as neurologic and reproductive impairment and an overall reduction in fitness.9 Postmortem lesions associated with lead intoxication in birds include emaciation, staining of the vent with bright green fecal material, impaction of the esophagus or proventriculus, a prominent and distended gallbladder, dark or bright green staining of the gizzard lining, and the presence of lead bullets, pellets, or fragments in the gastrointestinal tract.

Lead ammunition and fishing tackle constitute forms of concentrated lead that are commonly inadvertently ingested by birds. As has been recognized for > 100 years,10,11 exposure to these sources of lead is hazardous to waterbirds (eg, ducks, swans, and loons). Upland game birds (eg, doves and quail) and scavengers (eg, condors, turkey vultures, and eagles) have also been shown to be exposed to and lethally affected by lead from spent ammunition.12–17 Exposure to lead occurs as a result of ingestion of lead pellets (shotgun) or lead bullets and fragments (shotgun slugs and high-velocity rifle bullets) embedded in the flesh of unrecovered game or other animals (eg, gophers and coyotes) or in offal (gut piles) and other body parts left in the field following dressing of carcasses.18 Hunter harvest data suggest that approximately 186,000 to 200,000 deer are shot and slaughtered annually in Minnesota, so thousands of offal piles potentially containing many lead ammunition fragments are available for scavengers.18

A recent study19 suggests that more than three-quarters of bald eagles admitted to rehabilitation facilities have detectable blood lead concentrations and 25% have lethal concentrations. Ingestion of spent ammunition and lost fishing tackle by birds is well-documented as triggering a number of negative effects in individual animals and potentially leading to population-level consequences in some species (eg, waterfowl, eagles, condors, mourning doves, and loons).13,20,21 California condors, which have been designated by the federal government as endangered, continue to be at great risk primarily as a result of exposure to lead from spent ammunition found in offal piles and carcasses of shot game and pest species.3,16

Current data for raptors and avian scavengers demonstrate a clear, positive relationship between lead exposure and hunting seasons.19,22–24 The hazard of ingested lead sinkers and fishing tackle is well-documented in swans and loons, and restrictions on the sale or use of lead weights have been instituted in parts of the United Kingdom, Canada, the United States, and other countries to reduce impacts on these and other vulnerable species.25,26 Studies27–30 have demonstrated that the respective 1991 and 1999 US and Canadian bans on the use of lead shot for hunting waterfowl and coots in North America successfully reduced lead exposure in these species and some predatory birds. These results suggest that such legislative actions can reduce the risk of intoxication from spent ammunition. Voluntary reductions in lead use for big game hunting have been demonstrated to reduce the risk of lead exposure to condors in Arizona.23

In 2007, California passed legislation requiring the use of nontoxic ammunition by hunters in a limited area of the California condor range. This legislation's failure to significantly decrease exposure of condors to lead resulted in additional legislation in 2013 that established a 5-year phase-in (2014 to 2019) of a statewide ban on lead ammunition.31 The phase-in is designed to impose the least burden on California's hunters while still adhering to the intent of the law.

Human exposure has been documented to occur following ingestion of lead from spent lead ammunition.32,33 Children, the most sensitive human subpopulation, are at particular risk. Increases in blood lead concentrations have been positively correlated with consumption of game taken with lead ammunition.34,35 The discharge of lead-based ammunition is known to pose risks of lead exposure to gun users.36,37 Lead ammunition fragments on impact, and even if a bullet completely passes through and exits an animal, small amounts of lead are left behind in the tissue. People consuming the meat can, without their knowledge, absorb these fragments and residues.18,32,33,38

Many effective nonlead alternatives to lead-based ammunition and fishing tackle have been developed and are currently available.39 Several companies have developed nonlead ammunition that can be used safely in all varieties of rifles and shotguns for hunting large and small game.40,41 Firearm experts have confirmed that typically only minor adjustments in technique are required for successful use of nonlead hunting ammunition, and the effectiveness of such ammunition has been demonstrated.42 However, the widespread manufacture and use of nontoxic ammunition depends on the development of assured markets supported by education, regulation, and enforcement.41 Legislation is the biggest determinant of assured markets for nontoxic alternatives and compliance with their use. Although there is a slight cost differential between lead-based and nonlead alternatives for fishing tackle and ammunition used for hunting, the increased costs to consumers are negligible, compared with the total investments of participants for their hunting and fishing activities. Required use combined with wider availability would likely result in more competitive pricing of nonlead alternatives. Opponents have suggested that requiring the use of nontoxic alternatives is the first step to a ban on hunting or is an attempt to control gun access. However, there is no factual evidence to support such claims or concerns.

Various professional organizations, including the Association of Avian Veterinarians and the Wildlife Society, have endorsed replacing lead hunting ammunition and fishing tackle with nonlead alternatives.43,44 We encourage the AVMA to work with other organizations and agencies to increase awareness of the dangers lead ammunition and fishing tackle pose to animals. Further, we urge the AVMA to adopt a policy on lead ammunition and fishing tackle, as we believe that doing so could encourage individuals and agencies to formulate solutions to the problems they pose and generate discussions about how society could better protect our environment. Although the AVMA has not adopted a specific policy on lead, it does have a policy on toxicoses, which states, “The AVMA supports education, legislation, regulations, research, and other actions that prevent toxicoses in wildlife, domestic animal, and human populations.” Even though this policy would nominally include lead, perhaps it is time to take a more proactive stance regarding the replacement of lead in ammunition and fishing tackle.

References

  • 1. US Geological Survey Biological Resources Division. Lead. In: Field manual of wildlife diseases: general field procedures and disease of birds. Washington, DC: US Geological Survey, 1999; 317334.

    • Search Google Scholar
    • Export Citation
  • 2. Sanders T, Liu Y, Buchner, V et al. Neurotoxic effects and biomarkers of lead exposure: a review. Rev Environ Health 2009; 24: 1545.

  • 3. Johnson CK, Kelly TR, Rideout BA. Lead in ammunition: a persistent threat to health and conservation. EcoHealth 2013; 10: 455464.

  • 4. De Francisco N, Ruiz Troya JD, Aguera EI. Lead and lead toxicity in domestic and free living birds. Avian Pathol 2003; 32: 311.

  • 5. Pain DJ, Amiard-Triquett C, Bavoux C, et al. Lead poisoning in wild populations of marsh harrier (Circus aeruginosus) in the Camargue and Charente-Maritime, France. Ibis 1993; 135: 379386.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Custer TW, Franson JC, Pattee OH. Tissue lead distribution and hematologic effects in American kestrels (Falco sparverius) fed biologically incorporated lead. J Wildl Dis 1984; 20: 3943.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Franson JC, Sileo L, Pattee OH, et al. Effects of chronic dietary lead in American kestrels (Falco sparverius). J Wildl Dis 1983; 19: 110113.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Redig PT, Stowe CM, Barnes D, et al. Lead toxicosis in raptors. J Am Vet Med Assoc 1980; 177: 941943.

  • 9. Burger J, Gochfeld M. Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health B Crit Rev 2000; 3: 5978.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Blus LJ, Stroud RK, Reiswig B, et al. Lead poisoning and other mortality factors in trumpeter swans. Environ Toxicol Chem 1989; 8: 263271.

  • 11. Grinnell GB. Lead poisoning. Forest and Stream 1894; 42: 117118.

  • 12. Stauber E, Finch N, Talcott PA, et al. Lead poisoning of bald (Haliaeetus leucocephalus) and golden (Aquila chrysaetos) eagles in the US Inland Pacific Northwest Region—an 18-year retrospective study: 1991–2008. J Avian Med Surg 2010; 24: 279287.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Green RE, Hunt WG, Parish CN, et al. Effectiveness of action to reduce exposure of free-ranging California condors in Arizona and Utah to lead from spent ammunition. PloS ONE [serial online] 2008; 3:e4022. Available at: www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0004022. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 14. Kreager N, Wainman BC, Jayasinghe RK, et al. Lead pellet ingestion and liver-lead concentrations in upland game birds from southern Ontario, Canada. Arch Environ Contam Toxicol 2008; 54: 331336.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Cade TJ. Exposure of California condors to lead from spent ammunition. J Wildl Manage 2007; 71: 21252133.

  • 16. Hunt WG, Burnham W, Parish CN, et al. Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildl Soc Bull 2006; 34: 167170.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Kramer JL, Redig PT. Sixteen years of lead poisoning in eagles, 1980–1995: an epizootiologic view. J Raptor Res 1997; 31: 327332.

    • Search Google Scholar
    • Export Citation
  • 18. Grund MD, Cornicelli L, Carlson LT, et al. Bullet fragmentation and lead deposition in white-tailed deer and domestic sheep. Human Wildl Interact 2010; 4: 4351.

    • Search Google Scholar
    • Export Citation
  • 19. Cruz-Martinez L, Redig PT, Deen J. Lead from spent ammunition: a source of exposure and poisoning in bald eagles. Human Wildl Interact 2012; 6: 94104.

    • Search Google Scholar
    • Export Citation
  • 20. Rideout BA, Stalis I, Papendick R, et al. Patterns of mortality in free-ranging California condors (Gymnogyps californianus). J Wildl Dis 2012; 48: 95112.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Sidor IF, Pokras MA, Major AR, et al. Mortality of common loons in New England, 1987 to 2000. J Wildl Dis 2003; 39: 306315.

  • 22. Neumann K. Bald eagle lead poisoning in winter. In: Watson RT, Fuller M, Pokras M, et al, eds. Ingestion of lead from spent ammunition: implications for wildlife and humans. Boise, Idaho: The Peregrine Fund, 2009; 210218.

    • Search Google Scholar
    • Export Citation
  • 23. Sieg R, Sullivan KA, Parrish CN. Voluntary lead reduction efforts within the northern Arizona range of the California condor. In: Watson RT, Fuller M, Pokras M, et al, eds. Ingestion of lead from spent ammunition: implications for wildlife and humans. Boise, Idaho: The Peregrine Fund, 2009; 341349.

    • Search Google Scholar
    • Export Citation
  • 24. Craighead D, Bedrosian B. Blood lead levels of common ravens with access to big-game offal. J Wildl Manage 2008; 72: 240245.

  • 25. Wilson LK, Grigg G, Forsyth R, et al. Lead poisoning in trumpeter swans in the Pacific Northwest: can recovered shot pellets help to elucidate the source? In: Watson RT, Fuller M, Pokras M, et al, eds. Ingestion of lead from spent ammunition: implications for wildlife and humans. Boise, Idaho: The Peregrine Fund, 2009; 278282.

    • Search Google Scholar
    • Export Citation
  • 26. Pokras MA, Kneeland MR, Major A. Lead objects ingested by common loons in New England. In: Watson RT, Fuller M, Pokras M, et al, eds. Ingestion of lead from spent ammunition: implications for wildlife and humans. Boise, Idaho: The Peregrine Fund, 2009; 283286.

    • Search Google Scholar
    • Export Citation
  • 27. Kelly TR, Bloom PH, Torres SG, et al. Impact of the California lead ammunition ban on reducing lead exposure in golden eagles and turkey vultures. PloS ONE [serial online]. 2011; 6:e17656. Available at: www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0017656. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 28. Stevenson AL, Scheuhammer AM, Chan HM. Effects of non-toxic shot regulations on lead accumulation in ducks and American woodcock in Canada. Arch Environ Contam Toxicol 2005; 48: 405413.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Anderson WL, Havera SP, Zercher BW. Ingestion of lead and nontoxic shotgun pellets by ducks in the Mississippi flyway. J Wildl Manage 2000; 64: 848857.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Samuel MD, Bowers EF. Lead exposure in American black ducks after implementation of non-toxic shot. J Wildl Manage 2000; 64: 947953.

  • 31. California Department of Fish and Wildlife. Lead free ammunition. Available at: www.dfg.ca.gov/wildlife/hunting/lead-free/Accessed Jul 17, 2014.

    • Search Google Scholar
    • Export Citation
  • 32. Mateo R, Vallverdú-Coll N, López-Antia A, et al. Reducing Pb poisoning in birds and Pb exposure in game meat consumers: a duel benefit of effective Pb shot regulation. Environ Int 2014; 63: 163168.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Green RE, Pain DJ. Potential health risks to adults and children in the UK from exposure to dietary lead in gamebirds shot with lead ammunition. Food Chem Toxicol 2012; 50: 41804190.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Tsuji L, Wainman B, Jayasinghe R, et al. Determining tissue-lead levels in large game mammals harvested with lead bullets: human health concerns. Bull Environ Contam Toxicol 2009; 82: 435439.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Levesque B, Duschesne JF, Gariepy C, et al. Monitoring of umbilical cord blood lead levels and sources assessment among the Inuit. Occup Environ Med 2003; 60: 693695.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Bellinger DC, Bradman A, Burger J, et al. Health risks from lead-based ammunition in the environment—a consensus statement of scientists (2013). UC Santa Cruz: Microbiology and Environmental Toxicology. Available at escholarship.org/uc/item/6dq3h64x. Accessed Jul 2, 2014.

    • Search Google Scholar
    • Export Citation
  • 37. NRC. Potential health risks to DOD firing-range personnel from recurrent lead exposure. Washington, DC: National Academies Press, 2012.

    • Search Google Scholar
    • Export Citation
  • 38. Hunt WG, Watson RT, Oaks JL, et al. Lead bullet fragments in venison from rifle-killed deer: potential for human dietary exposure. PloS ONE [serial online]. 2009; 4:e5330. Available at: www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0005330. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 39. New York State Department of Environmental Conservation. Alternative ammo. Good for hunting; great for conservation. Available at: www.dec.ny.gov/pubs/85022.html. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 40. SOAR: Saving Our Avian Resources. How good are copper bullets, really??? Available at: huntingwithnonlead.org/PDFs_Main/WI%20DNR%20Copper%20Bullet%20Study.pdf. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 41. Thomas VG. Lead-free hunting rifle ammunition: product availability, price, effectiveness, and role in global wildlife conservation. Ambio 2013; 6: 737745.

    • Search Google Scholar
    • Export Citation
  • 42. Knott J, Gilbert J, Green RE, et al. Comparison of the lethality of lead and copper bullets in deer control operations to reduce incidental lead poisoning; field trials in England and Scotland. Conserv Evid 2009; 6: 7178.

    • Search Google Scholar
    • Export Citation
  • 43. AVMA. Protecting wild birds from lead poisoning. Available at: https://www.avma.org/News/JAVMANews/Pages/121215e.aspx. Accessed Jul 17, 2014.

    • Search Google Scholar
    • Export Citation
  • 44. The Wildlife Society. Final position statement: lead in ammunition and fishing tackle. Available at: joomla.wildlife.org/documents/positionstatements/Lead_final_2009.pdf. Accessed Jul 18, 2014.

    • Search Google Scholar
    • Export Citation

Contributor Notes

The authors have no sources of funding, financial conflicts of interest, or disclaimers to declare.

Address correspondence to Dr. Poppenga (rhpoppenga@ucdavis.edu).
  • 1. US Geological Survey Biological Resources Division. Lead. In: Field manual of wildlife diseases: general field procedures and disease of birds. Washington, DC: US Geological Survey, 1999; 317334.

    • Search Google Scholar
    • Export Citation
  • 2. Sanders T, Liu Y, Buchner, V et al. Neurotoxic effects and biomarkers of lead exposure: a review. Rev Environ Health 2009; 24: 1545.

  • 3. Johnson CK, Kelly TR, Rideout BA. Lead in ammunition: a persistent threat to health and conservation. EcoHealth 2013; 10: 455464.

  • 4. De Francisco N, Ruiz Troya JD, Aguera EI. Lead and lead toxicity in domestic and free living birds. Avian Pathol 2003; 32: 311.

  • 5. Pain DJ, Amiard-Triquett C, Bavoux C, et al. Lead poisoning in wild populations of marsh harrier (Circus aeruginosus) in the Camargue and Charente-Maritime, France. Ibis 1993; 135: 379386.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Custer TW, Franson JC, Pattee OH. Tissue lead distribution and hematologic effects in American kestrels (Falco sparverius) fed biologically incorporated lead. J Wildl Dis 1984; 20: 3943.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Franson JC, Sileo L, Pattee OH, et al. Effects of chronic dietary lead in American kestrels (Falco sparverius). J Wildl Dis 1983; 19: 110113.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Redig PT, Stowe CM, Barnes D, et al. Lead toxicosis in raptors. J Am Vet Med Assoc 1980; 177: 941943.

  • 9. Burger J, Gochfeld M. Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health B Crit Rev 2000; 3: 5978.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Blus LJ, Stroud RK, Reiswig B, et al. Lead poisoning and other mortality factors in trumpeter swans. Environ Toxicol Chem 1989; 8: 263271.

  • 11. Grinnell GB. Lead poisoning. Forest and Stream 1894; 42: 117118.

  • 12. Stauber E, Finch N, Talcott PA, et al. Lead poisoning of bald (Haliaeetus leucocephalus) and golden (Aquila chrysaetos) eagles in the US Inland Pacific Northwest Region—an 18-year retrospective study: 1991–2008. J Avian Med Surg 2010; 24: 279287.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Green RE, Hunt WG, Parish CN, et al. Effectiveness of action to reduce exposure of free-ranging California condors in Arizona and Utah to lead from spent ammunition. PloS ONE [serial online] 2008; 3:e4022. Available at: www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0004022. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 14. Kreager N, Wainman BC, Jayasinghe RK, et al. Lead pellet ingestion and liver-lead concentrations in upland game birds from southern Ontario, Canada. Arch Environ Contam Toxicol 2008; 54: 331336.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Cade TJ. Exposure of California condors to lead from spent ammunition. J Wildl Manage 2007; 71: 21252133.

  • 16. Hunt WG, Burnham W, Parish CN, et al. Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildl Soc Bull 2006; 34: 167170.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Kramer JL, Redig PT. Sixteen years of lead poisoning in eagles, 1980–1995: an epizootiologic view. J Raptor Res 1997; 31: 327332.

    • Search Google Scholar
    • Export Citation
  • 18. Grund MD, Cornicelli L, Carlson LT, et al. Bullet fragmentation and lead deposition in white-tailed deer and domestic sheep. Human Wildl Interact 2010; 4: 4351.

    • Search Google Scholar
    • Export Citation
  • 19. Cruz-Martinez L, Redig PT, Deen J. Lead from spent ammunition: a source of exposure and poisoning in bald eagles. Human Wildl Interact 2012; 6: 94104.

    • Search Google Scholar
    • Export Citation
  • 20. Rideout BA, Stalis I, Papendick R, et al. Patterns of mortality in free-ranging California condors (Gymnogyps californianus). J Wildl Dis 2012; 48: 95112.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Sidor IF, Pokras MA, Major AR, et al. Mortality of common loons in New England, 1987 to 2000. J Wildl Dis 2003; 39: 306315.

  • 22. Neumann K. Bald eagle lead poisoning in winter. In: Watson RT, Fuller M, Pokras M, et al, eds. Ingestion of lead from spent ammunition: implications for wildlife and humans. Boise, Idaho: The Peregrine Fund, 2009; 210218.

    • Search Google Scholar
    • Export Citation
  • 23. Sieg R, Sullivan KA, Parrish CN. Voluntary lead reduction efforts within the northern Arizona range of the California condor. In: Watson RT, Fuller M, Pokras M, et al, eds. Ingestion of lead from spent ammunition: implications for wildlife and humans. Boise, Idaho: The Peregrine Fund, 2009; 341349.

    • Search Google Scholar
    • Export Citation
  • 24. Craighead D, Bedrosian B. Blood lead levels of common ravens with access to big-game offal. J Wildl Manage 2008; 72: 240245.

  • 25. Wilson LK, Grigg G, Forsyth R, et al. Lead poisoning in trumpeter swans in the Pacific Northwest: can recovered shot pellets help to elucidate the source? In: Watson RT, Fuller M, Pokras M, et al, eds. Ingestion of lead from spent ammunition: implications for wildlife and humans. Boise, Idaho: The Peregrine Fund, 2009; 278282.

    • Search Google Scholar
    • Export Citation
  • 26. Pokras MA, Kneeland MR, Major A. Lead objects ingested by common loons in New England. In: Watson RT, Fuller M, Pokras M, et al, eds. Ingestion of lead from spent ammunition: implications for wildlife and humans. Boise, Idaho: The Peregrine Fund, 2009; 283286.

    • Search Google Scholar
    • Export Citation
  • 27. Kelly TR, Bloom PH, Torres SG, et al. Impact of the California lead ammunition ban on reducing lead exposure in golden eagles and turkey vultures. PloS ONE [serial online]. 2011; 6:e17656. Available at: www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0017656. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 28. Stevenson AL, Scheuhammer AM, Chan HM. Effects of non-toxic shot regulations on lead accumulation in ducks and American woodcock in Canada. Arch Environ Contam Toxicol 2005; 48: 405413.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Anderson WL, Havera SP, Zercher BW. Ingestion of lead and nontoxic shotgun pellets by ducks in the Mississippi flyway. J Wildl Manage 2000; 64: 848857.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Samuel MD, Bowers EF. Lead exposure in American black ducks after implementation of non-toxic shot. J Wildl Manage 2000; 64: 947953.

  • 31. California Department of Fish and Wildlife. Lead free ammunition. Available at: www.dfg.ca.gov/wildlife/hunting/lead-free/Accessed Jul 17, 2014.

    • Search Google Scholar
    • Export Citation
  • 32. Mateo R, Vallverdú-Coll N, López-Antia A, et al. Reducing Pb poisoning in birds and Pb exposure in game meat consumers: a duel benefit of effective Pb shot regulation. Environ Int 2014; 63: 163168.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Green RE, Pain DJ. Potential health risks to adults and children in the UK from exposure to dietary lead in gamebirds shot with lead ammunition. Food Chem Toxicol 2012; 50: 41804190.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Tsuji L, Wainman B, Jayasinghe R, et al. Determining tissue-lead levels in large game mammals harvested with lead bullets: human health concerns. Bull Environ Contam Toxicol 2009; 82: 435439.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Levesque B, Duschesne JF, Gariepy C, et al. Monitoring of umbilical cord blood lead levels and sources assessment among the Inuit. Occup Environ Med 2003; 60: 693695.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Bellinger DC, Bradman A, Burger J, et al. Health risks from lead-based ammunition in the environment—a consensus statement of scientists (2013). UC Santa Cruz: Microbiology and Environmental Toxicology. Available at escholarship.org/uc/item/6dq3h64x. Accessed Jul 2, 2014.

    • Search Google Scholar
    • Export Citation
  • 37. NRC. Potential health risks to DOD firing-range personnel from recurrent lead exposure. Washington, DC: National Academies Press, 2012.

    • Search Google Scholar
    • Export Citation
  • 38. Hunt WG, Watson RT, Oaks JL, et al. Lead bullet fragments in venison from rifle-killed deer: potential for human dietary exposure. PloS ONE [serial online]. 2009; 4:e5330. Available at: www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0005330. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 39. New York State Department of Environmental Conservation. Alternative ammo. Good for hunting; great for conservation. Available at: www.dec.ny.gov/pubs/85022.html. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 40. SOAR: Saving Our Avian Resources. How good are copper bullets, really??? Available at: huntingwithnonlead.org/PDFs_Main/WI%20DNR%20Copper%20Bullet%20Study.pdf. Accessed Jul 1, 2014.

    • Search Google Scholar
    • Export Citation
  • 41. Thomas VG. Lead-free hunting rifle ammunition: product availability, price, effectiveness, and role in global wildlife conservation. Ambio 2013; 6: 737745.

    • Search Google Scholar
    • Export Citation
  • 42. Knott J, Gilbert J, Green RE, et al. Comparison of the lethality of lead and copper bullets in deer control operations to reduce incidental lead poisoning; field trials in England and Scotland. Conserv Evid 2009; 6: 7178.

    • Search Google Scholar
    • Export Citation
  • 43. AVMA. Protecting wild birds from lead poisoning. Available at: https://www.avma.org/News/JAVMANews/Pages/121215e.aspx. Accessed Jul 17, 2014.

    • Search Google Scholar
    • Export Citation
  • 44. The Wildlife Society. Final position statement: lead in ammunition and fishing tackle. Available at: joomla.wildlife.org/documents/positionstatements/Lead_final_2009.pdf. Accessed Jul 18, 2014.

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