Ecological Archives A025-092-A1
Jean Fitts Cochrane, Eric Lonsdorf, Taber D. Allison, and Carol A. Sanders-Reed. 2015. Modeling with uncertain science: estimating mitigation credits from abating lead poisoning in Golden Eagles. Ecological Applications 25:1518–1533. http://dx.doi.org/10.1890/14-0996.1
Appendix A. Golden Eagles and lead poisoning literature summary.
Eagles are opportunistic scavengers, consuming big-game carrion primarily when it is most available and when alternative food sources are less available (Kelly et al. 2011, Bedrosian et al. 2012, Finkelstein et al. 2012, Nadjafzadeh et al. 2013). Golden Eagles (Aquila chrysaetos) scavenge primarily in the late fall and winter when carrion is preserved by colder temperatures, and more rarely in late spring and summer unless the carrion is fresh (Kochert et al. 2002). Eagles are efficient at detecting carcasses and gut piles, which are typically consumed within hours of the game animal’s death (Fisher et al. 2006, Kelly et al. 2011).
Eagles are exposed to lead when scavenging on animal carcasses and gut piles that hunters leave in the field. Lead residue in carcasses and gut piles is largely due to fragmentation of ammunition, which can number in the hundreds of fragments per carcass or gut pile (Hunt et al. 2006, Craighead and Bedrosian 2008, Harmata and Restani 2013). Hunt et al. (2006, 2009) found no lead fragments of any size in only 10% of 20 deer gut piles examined in Wyoming and California; while Warner (2014) reported no lead fragments in 64% of 25 deer gut piles from Illinois, where “many hunters” use lead ammunition and some use non-lead bullets. In addition, Hunt et al. (2006) found that many lead bullet fragments were “minute.” “Ingestion of very small particles of lead would explain the accumulation of sublethal levels in the blood of golden eagles during the hunting season” (Wayland and Bollinger 1999). Eagles typically regurgitate undigested bones and feathers once daily at dawn (Duke et al. 1975), and ingested lead pellets are also typically regurgitated within a week and most often within 2 days – but not before some lead is eroded (Pattee et al. 1981).
Hunt et al. (2006, 2009), Green et al. (2008), and Bedrosian et al. (2012) have documented lead exposure levels in eagles as a predictable function of the number of big game animals shot with lead and hence contaminated carcasses and gut piles available. Seasonal peaks in blood lead levels associated with game hunting seasons and local exposure to shot game animals have been widely and consistently reported for eagles and other avian scavengers (e.g., Pattee et al. 1990, Wayland and Bollinger 1999, Bedrosian and Craighead 2009, Stauber et al. 2010, Fernandez et al. 2011, Kelly et al. 2011, Kelly and Johnson 2011, Bedrosian et al. 2012, Cruz-Martinez et al. 2012, Rideout et al. 2012, Harmata and Restani 2013, Nadjafzadeh et al. 2013).
Blood lead concentrations >100 or >120 ug/dL are generally associated with ‘acute,’ ‘fatal,’ or ‘toxic’ lead poisoning in raptors, based on large numbers of birds treated in rehabilitation centers (e.g., Kramer and Redig 1997, Stauber et al. 2010, Kelly et al. 2011, Bedrosian et al. 2012 citing Redig 1984, Cruz-Martinez et al. 2012). However, blood lead levels for acute mortality in individual birds in natural settings likely vary and we expect peak exposure levels to generally be higher than levels sampled in captive birds. For example, Harmata and Restani (2013) reported two free-flying Golden Eagles captured in Montana during winter with blood lead concentrations >100 ug/dL that “appeared in excellent condition and showed no signs of debilitation or disease.” Similarly, eight of 88 free-flying bald eagles (Haliaeetus leucocephalus) captured in Montana had blood lead concentrations exceeding a ‘toxic’ threshold level (>120 ug/dL; Kramer and Redig 1997), yet appeared “healthy” (Harmata 2011). These apparent cases of higher tolerance to elevated blood lead may be due in part to better pre-existing body condition among some of the randomly caught wild birds than is common for eagles brought in for rehabilitation.
Instances of elevated blood lead sampled in wild birds may have represented peak concentrations soon after ingesting lead, whereas toxicity thresholds derived from captive eagles do not represent the peak blood lead concentrations experienced by those poisoned birds. The half-life for lead in condor blood was about 13–17 days (Fry and Mauer 2003, public communication: Assessment of lead contamination sources exposing California condors. Final Report. Sacramento, CA: California Department of Fish and Game, Habitat Conservation Planning Branch. http://www.dfg.ca.gov/wildlife/nongame/publications/bm_research/docs/2003_02.pdf accessed 13 May 2014, Green et al. 2008). If it typically takes a week or longer for a wild eagle to exhibit symptoms and be captured, transported, and tested for lead exposure, as our experts suggested, blood lead sampled in captive birds may have declined by one-third from the maximum level.
Direct mortality from lead poisoning has been estimated in several raptor populations. Hunt (2002, public communication: Golden Eagles in a perilous landscape: predicting the effects of mitigation for wind-turbine blade strike mortality. California Energy Commission, Public Interest Energy Research Consultant Report P500-02-043F, July 2002, http://www.energy.ca.gov/reports/2002-11-04_500-02-043F.PDF accessed 13 Mary 2014) could confirm at least three of 100 deaths in radio-tagged golden eagles in California were due to lead poisoning and lead may have caused or contributed to additional mortality. Pattee et al. (1981) reported that 3% of 168 examined dead or dying bald eagles apparently died of lead poisoning in the late 1970s. Between 3-9% of Golden Eagles captured in the wild in Montana and California had ‘clinical’ or ‘acute’ concentrations of lead in their blood (>50–100 ug/dL depending on the study; Pattee et al. 1990, Kelly et al. 2011, Harmata and Restani 2013) indicating elevated risk of imminent mortality. Chronic effects of subclinical lead exposure may predispose eagles to mortality from electrocution, drowning, collision and other threats (Scheuhammer 1987, Kramer and Redig 1997, Wayland and Bollinger 1999, Pain et al. 2009, Lehman et al. 2010, Stauber et al. 2010, Hunt 2012, Katzner et al. 2012).
In its Eagle Conservation Plan Guidance, the USFWS (2013) reviewed available data and determined the best current estimates for Golden Eagle average annual mortality rates in the Western United States are approximately 9% for territorial adult birds (≥5 years old), 21% for both non-breeding adults (“floaters”) and subadults (ages 1–4 years), and 39% for juveniles (post-fledging to 1 year). Assuming a stable population size with stable age structure (roughly 20% juveniles, 40% subadults and non-breeding floaters, 40% breeders; Brian Millsap, personal communication, USFWS, Albuquerque, NM, 2014), the population average annual mortality rate would be approximately 20% across all post-fledging eagles. Scheuhammer and Norris (1996) generalized that lead poisoning from eating prey animals with lead shot embedded in their tissues accounts for an estimated 10–15% of the recorded post-fledging mortality in bald and Golden Eagles in Canada and the United States. Applying that proportion to 20% total mortality, on average 2–3% of Golden Eagles die per year continentally due to scavenging shot animals.
Estimates for the proportion of annual mortality of California Condor (Gymnogyps californianus) definitively attributed to lead exposure range from 7% (Finkelstein et al. 2012) to 35% (Rideout et al. 2012). Green et al. (2008) estimated the average probability of condors dying from lead was 5.1% per year.
Programs to reduce lead exposure due to big game harvest have been attempted in California, Arizona, and Wyoming with measurable results. Voluntary participation with non-lead rifle ammunition and gut-pile removal programs was variable, with 24–83% of hunters reported as participating per year (Seng 2006, public communication: Non-lead ammunition program hunter survey. Final report to the Arizona Game and Fish Department. http://www.azgfd.gov/w_c/documents/AmmoSurveyFINALReport2-23-06_000.pdf accessed 13 May 2014, Sieg et al. 2009, Bedrosian et al 2012). Kelly et al. (2011) found the proportion of non-migrant golden eagles with blood lead exceeding background (defined as >10 mg/dL) dropped from 83% to 0% following a regional lead ammunition ban within California. Bedrosian et al. (2012) documented that the mean seasonal blood lead level of Bald Eagles in northwest Wyoming declined as the number of big game harvested with lead ammunition declined (24–35% of hunters switched to non-toxic ammunition), even though total game harvest increased.
Bedrosian, B., and D. Craighead. 2009. Blood lead levels of Bald and Golden Eagles sampled during and after hunting seasons in the Greater Yellowstone Ecosystem. Pages 219-220 in Watson, R. T., M. Fuller, M. Pokras, and W.G. Hunt, editors. Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho. DOI 10.4080/ilsa.2009.0209.
Bedrosian, B., D. Craighead, and R. Crandall. 2012. Lead exposure in Bald Eagles from big game hunting, the continental implications and successful mitigation efforts. PLoS ONE 7(12): e51978. doi:10.1371/journal.pone.0051978.
Craighead, D., and B. Bedrosian. 2008. Blood lead levels of common ravens with access to big-game offal. Journal of Wildlife Management 72(1):240–245.
Cruz-Martinez, L, P. T. Redig, and J. Deen. 2012. Lead from spent ammunition: a source of exposure and poisoning in bald eagles. Human-Wildlife Interactions 6:94–104.
Duke, G. E., O. A. Evanson, and A. Jegers. 1975. Meal to pellet intervals in 14 species of captive raptors. Comparative Biochemistry and Physiology 53A:1–6.
Fernandez, J. R.-R., U. Hofle, R. Mateo, O. N. de Francisco, R. Abbott, P. Acevedo, and J. M. Blanco. 2011. Assessment of lead exposure in Spanish imperial eagle (Aquila adalberti) from spent ammunition in central Spain. Ecotoxicology 20:670–681.
Finkelstein, M. E., D. F. Doak, D. George, J. Burnett, J. Brandt, M. Church, J. Grantham, and D. R. Smith. 2012. Lead poisoning and the deceptive recovery of the critically endangered California condor. PNAS 109:11449–11454.
Fisher, I. J., D. J. Pain, and V. G. Thomas. 2006. A review of lead poisoning from ammunition sources in terrestrial birds. Biological Conservation 131:421–432.
Green, R. E., W. G. Hunt, C. N. Parish, and I. Newton. 2008. Effectiveness of action to reduce exposure of free-ranging California Condors in Arizona and Utah to lead from spent ammunition. PLoS One 3(12): e4022. doi:10.1371/journal.pone.0004022.
Harmata, A. R. 2011. Environmental contaminants in tissues of Bald Eagles sampled in southwestern Montana, 2006-2008. Journal of Raptor Research 45:119–135.
Harmata, A. R., and M. Restani. 2013. Lead, mercury, selenium, and other trace elements in tissues of Golden Eagles from southwestern Montana, USA. Journal of Wildlife Diseases 49:114–124.
Hunt, W.G. 2012. Implications of sublethal lead exposure in avian scavengers. Journal of Raptor Research 46: 389–393.
Hunt, W. G., W. Burnham, C. Parish, K. Burnham, B. Mutch, and J. L. Oaks. 2006. Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildlife Society Bulletin 34:167–170.
Hunt, W. G., C. N. Parish, K. Orr, and R. F. Aguilar. 2009. Lead Poisoning and the reintroduction of the California Condor in Northern Arizona. Journal of Avian Medicine and Surgery 23:145–150.
Katzner, T., B. W. Smith, T. A. Miller, D. Brandes, J. Cooper, M. Lanzone, D. Brauning, C. Farmer, S. Harding, D.E. Kramar, C. Koppie, C. Maisonneuve, M. Martell, E. K. Mojica, C. Todd, J. A. Tremblay, M. Wheeler, D. F. Brinker, T. E. Chubbs, R. Gubler, K. O’Malley, S. Mehus, B. Porter, R. P. Brooks, B. D. Watts, and K. L. Bildstein. 2012. Status, biology, and conservation priorities for North America's Eastern Golden Eagle (Aquila chrysaetos) population. The Auk 129:1–9.
Kelly, T. R., P. H. Bloom, S. G. Torres, Y. Z. Hernandez, R. H. Poppenga, W. M. Boyce, and C. K. Johnson. 2011. Impact of the California lead ammunition ban on reducing lead exposure in Golden Eagles and Turkey Vultures. PLoS ONE 6(4): e17656. doi:10.1371/journal.pone.0017656.
Kelly, T. R., and C. K. Johnson. 2011. Lead exposure in free-flying Turkey Vultures is associated with big game hunting in California. PLoS ONE 6(4): e15350. doi:10.1371/journal.pone.0015350.
Kochert, M. N., K. Steenhof, C. L. Mcintyre, and E. H. Craig. 2002. Golden Eagle (Aquila chrysaetos). In Poole, E., editor, The Birds of North America Online. Cornell Lab of Ornithology, Ithaca, New York. The Birds of North America Online: http://bna.birds.cornell.edu/bna/species/684
Kramer, J. L., and P. T. Redig. 1997. Sixteen years of lead poisoning in eagles, 1980–95: an epizootiologic view. Journal of Raptor Research 31:327–332.
Lehman, R. N., J. A. Savidge, P. L. Kennedy, and R. E. Harness. 2010. Raptor electrocution rates for a utility in the Intermountain Western United States. Journal of Wildlife Management 74(3):459–470.
Nadjafzadeh, M., H. Hofer, and O. Krone. 2013. The link between feeding ecology and lead poisoning in White-tailed Eagles. Journal of Wildlife Management 77:48–57.
Pain, D. J., I. J. Fisher, and V. G. Thomas. 2009. A global update of lead poisoning in terrestrial birds from ammunition sources. Pages 99-118 in Watson, R. T., M. Fuller, M. Pokras, and W. G. Hunt, editors. Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho. DOI 10.4080/ilsa.2009.0108.
Pattee, O. H., S. N. Wiemeyer, B. M. Mulhern, L. Sileo, and J. W. Carpenter. 1981. Experimental lead-shot poisoning in Bald Eagles. Journal of Wildlife Management 45(3):806–810.
Pattee, O. H., P. H. Bloom, J. M. Scott, and M. R. Smith. 1990. Lead hazards within the range of the California Condor. Condor 92:931–937.
Rideout, B. A., I. Stalis, R. Papendick, A. Pessier, B. Puschner, M. E. Finkelstein, D. R. Smith, M. Johnson, M. Mace, R. Stroud, J. Brandt, J. Burnett, C. Parish, J. Petterson, C. Witte, C. Stringfield, K. Orr, J. Zuba, M. Wallace, and J. Granham. 2012. Patterns of mortality in free-ranging California Condors (Gymnogyps californianus). Journal of Wildlife Diseases 48:95–112.
Scheuhammer, A. M. 1987. The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environmental Pollution 46(4):263–295.
Scheuhammer, A. M., and S. L. Norris. 1996. The ecotoxicology of lead shot and lead fishing weights. Ecotoxicology 5:279–295.
Sieg, R., K. A. Sullivan, and C. N. Parish. 2009. Voluntary lead reduction efforts within the northern Arizona range of the California Condor. Pages 341–349 in Watson, R. T., M. Fuller, M. Pokras, and W. G. Hunt, editors. Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho. DOI 10.4080/ilsa.2009.0309.
Stauber, E., N. Finch, P. A. Talcott, and J. M. Gay. 2010. 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. Journal of Avian Medicine and Surgery 24:279–287.
U.S. Fish and Wildlife Service (USFWS). 2013. Eagle Conservation Plan Guidance. Module 1 – Land-based Wind Energy Version 2. U.S. Fish and Wildlife Service, Division of Migratory Bird Management, Branch of Policy, Permits and Regulations, Arlington, Virginia. April 2013.
Warner, S., E. Britton, D. Becker, and M. Coffey. 2014. Bald eagle lead exposure in the Upper Midwest. Journal of Fish and Wildlife Management 5(2):208–216; e1944-687X. doi: 10.3996/032013-JFWM-029.
Wayland, M., and T. Bollinger. 1999. Lead exposure and poisoning in Bald Eagles and Golden Eagles in the Canadian prairie provinces. Environmental Pollution 104(3):341–350.
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