Exposure, Effects and Absorption of Lead in American Woodcock (Scolopax minor): A Review

  • Amanda D. French
  • Warren C. Conway
  • Jaclyn E. Cañas-Carrell
  • David M. Klein
Focused Review


Due to long term declines of American Woodcock (Scolopax minor) and widespread distribution of environmentally available lead (Pb) throughout their geographic range, it is important to assess if Pb exposure is a potential contributor to these declines. Woodcock are exposed to Pb through various environmental sources and are known to exhibit relatively high bone-Pb concentrations. Absorption of Pb by birds, and woodcock specifically, is not well understood. Some studies show that interactions among calcium, phosphorus, iron, zinc, and vitamin D levels may play an important role in Pb absorption. Therefore, when future Pb studies are performed for woodcock, and other birds, interactions among these elements should be considered. For example, these interactions are relevant in the acquisition and mobilization of calcium in female birds during egg development and shell calcification. These factors should be considered to understand potential mechanisms of Pb exposure, Pb absorption, and subsequent Pb toxicity to birds in general, and woodcock specifically. This review discusses Pb exposure routes, effects of Pb toxicity, and the distribution of Pb in American woodcock and identifies areas for future research in woodcock and other avian species.


American woodcock (Scolopax minorLead (Pb) Calcium (Ca) Phosphorus (P) Zinc (Zn) Iron (Fe) Vitamin D 



We gratefully acknowledge research assistantship funding from the Department of Environmental Toxicology of Texas Tech University.


  1. Abadin H, Ashizawa A, Stevens Y-W (1998) Toxicological profile for lead. US Public Heal Serv Agency. Toxic Subst Dis Regist 582.Google Scholar
  2. Al-saleh IAS (1994) The biochemical and clinical consequences of lead poisoning. Med Res Rev 14:415–486CrossRefGoogle Scholar
  3. Andreotti A, Borghesi F, Aradis A (2016) Lead ammunition residues in the meat of hunted woodcock: a potential health risk to consumers. Ital J Anim Sci 15:22–29CrossRefGoogle Scholar
  4. Ansara-Ross TM, Ross MJ, Wepener V (2013) The use of feathers in monitoring bioaccumulation of metals and metalloids in the South African endangered African grass-owl (Tyto capensis). Ecotoxicology 22:1072–1083CrossRefGoogle Scholar
  5. Bafundo KW, Baker DH, Fitzgerald PR (1984) Lead toxicity in the chick as affected by excess copper and zinc and by Eimeria acervulina infection. Poult Sci 63:1594–1603CrossRefGoogle Scholar
  6. Bar A (2008) Calcium homeostasis and vitamin D metabolism and expression in strongly calcifying laying birds. Comp Biochem Physiol A Mol Integr Physiol 151:477–490CrossRefGoogle Scholar
  7. Basha MR, Wei W, Brydie M, Razmiafshari M, Zawia NH (2003) Lead-induced developmental perturbations in hippocampal Sp1 DNA-binding are prevented by zinc supplementation: In vivo evidence for Pb and Zn competition. Int J Dev Neurosci 21:1–12CrossRefGoogle Scholar
  8. Baski SN, Kenny AD (1979) Vitamin D metabolism in Japanese quail: gonadal hormones and dietary calcium effects. Toxicol Appl Pharmacol 51:489–495CrossRefGoogle Scholar
  9. Beyer WN, Connor EE, Gerould S (1994) Estimates of soil ingestion by wildlife. J Wildl Manage 58:375–382CrossRefGoogle Scholar
  10. Beyer WN, Dalgarn J, Dudding S, French JB, Mateo R, Miesner J, Sileo L, Spann J (2004) Zinc and lead poisoning in wild birds in the Tri-State Mining District (Oklahoma, Kansas, and Missouri). Arch Environ Contam Toxicol 48:108–117CrossRefGoogle Scholar
  11. Beyer WN, Franson JC, French JB, May T, Rattner BA, Shearn-Bochsler VI, Warner SE, Wber J, Mosby D (2013) Toxic exposure of song birds to lead in the Southeast Missouri Lead Mining District. Arch Environ Contam Toxicol 65:598–610CrossRefGoogle Scholar
  12. Beyer WN, Basta NT, Chaney RL, Henry PFP, Mosby DE, Rattner BA, Scheckel KG, Sprague DT, Weber JS (2016) Bioaccessibility tests accurately estimate bioavailability of lead to quail. Environ Toxicol Chem 35:1–9CrossRefGoogle Scholar
  13. Bianchi N, Ancora S, di Fazio N, Leonzio C (2008) Cadmium, lead, and mercury levels in feathers of small passerine birds: noninvasive sampling strategy. Environ Toxicol Chem 27:2064–2070CrossRefGoogle Scholar
  14. Blus LJ, Henny CJ, Hoffman DJ, Grove RA (1995) Accumulation in and effects of lead and cadmium on waterfowl and passerines in northern Idaho. Environ Pollut 89:311–318CrossRefGoogle Scholar
  15. Borghesi F, Migani F, Andreotti A, Baccetti N, Bianchi N, Birke M, Dinelli E (2016) Metals and trace elements in feathers: a geochemical approach to avoid misinterpretation of analytical responses. Sci Total Environ 544:476–494CrossRefGoogle Scholar
  16. Bortolotti GR (2010) Flaws and pitfalls in the chemical analysis of feathers: bad news-good news for avian chemoecology and toxicology. Ecol Appl 20:1766–1774CrossRefGoogle Scholar
  17. Boughattas I, Hattab S, Boussetta H, Sappin-Didier V, Viarengo A, Banni M, Sforzini S (2016) Biomarker responses of Eisenia andrei to a polymetallic gradient near a lead mining site in North Tunisia. Environ Pollut 218:530–541CrossRefGoogle Scholar
  18. Burger J (1993) Metals in avian feathers: bioindicators of environmental pollution. Rev. Environ Toxicol 5:203–311Google Scholar
  19. Carlson BL, Nielsen SW (1985) Influence of dietary calcium on lead poisoning in mallard ducks (Anas platyrynchos). Am J Vet Res 46:276–282Google Scholar
  20. Carvalho PC, Bugoni L, McGill RAR, Bianchini A (2013) Metal and selenium concentrations in blood and feathers of petrels of the genus procellaria. Environ Toxicol Chem 32:1641–1648CrossRefGoogle Scholar
  21. Chrastný V, Komárek M, Hájek T (2010) Lead contamination of an agricultural soil in the vicinity of a shooting range. Environ Monit Assess 162:37–46CrossRefGoogle Scholar
  22. Church ME (2006) Ammunition is the principal source of lead accumulated by California condors re-introduced to the wild. Environ Sci Technol 40:6143–6150CrossRefGoogle Scholar
  23. Custer TW, Franson JC, Pattee OH (1984) Tissue lead distribution and hematologic effects in American kestrels (Falco sparverius L.) fed biologically incorporated lead. J Wildl Dis 20:39–43CrossRefGoogle Scholar
  24. Dacke CG, Arkle S, Cook DJ, Wormstone IM, Jones S, Zaidi M, Bascal ZA (1993) Medullary bone and avian calcium regulation. J Exp Biol 184:63–88Google Scholar
  25. Darling CTR, Thomas VG (2005) Lead bioaccumulation in earthworms, Lumbricus terrestris, from exposure to lead compounds of differing solubility. Sci Total Environ 346:70–80CrossRefGoogle Scholar
  26. Dauwe T, Bervoets L, Blust R, Eens M (2002) Tissue levels of lead in experimentally exposed zebra finches (Taeniopygia guttata) with particular attention on the use of feathers as biomonitors. Arch Environ Contam Toxicol 42:88–92CrossRefGoogle Scholar
  27. Dauwe T, Bervoets L, Pinxten R, Blust R, Eens M (2003) Variation of heavy metals within and among feathers of birds of prey: effects of molt and external contamination. Environ Pollut 124:429–436CrossRefGoogle Scholar
  28. Dauwe T, Snoeijs T, Bervoets L, Blust R, Eens M (2006) Calcium availability influences lead accumulation in a passerine bird. Anim Biol 56:289–298.CrossRefGoogle Scholar
  29. De Francisco N, Troya JDR, Aguera EI (2003) Lead and lead toxicity in domestic and free living birds. Avian Pathol 32:3–13CrossRefGoogle Scholar
  30. Di Giulo RT, Scanlon PF (1984) Effects of cadmium and lead ingestion on tissue concentrations of cadmium, lead, copper and zinc in Mallard ducks. Sci Total Environ 39:103–110CrossRefGoogle Scholar
  31. Edelstein S, Fullmer CS, Wasserman RH (1984) Gastrointestinal absorption of lead in chicks: Involvement of the cholecalciferol endocrine system. J Nutr 114:692–700Google Scholar
  32. Edwards HM Jr (2000) Nutrition and skeletal problems in poultry. Poult Sci 79:1018–1023CrossRefGoogle Scholar
  33. Eeva T, Lehikoinen E (2004) Rich calcium availability diminishes heavy metal toxicity. Funct Ecol 18:548–553CrossRefGoogle Scholar
  34. Ek KH, Morrison GM, Lindberg P, Rauch S (2004) Comparative tissue distribution of metals in birds in Sweden using ICP-MS and laser ablation ICP-MS. Arch Environ Contam Toxicol 47:259–269CrossRefGoogle Scholar
  35. Ethier ALM, Braune BM, Scheuhammer AM, Bond DE (2007) Comparison of lead residues among avian bones. Environ Pollut 145:915–919CrossRefGoogle Scholar
  36. Finkelstein ME, George D, Scherbinski S, Gwiazda R, Johnson M, Burnett J, Brandt J, Lawrey S, Pessier AP, Clark M, Wynne J, Grantham J, Smith DR (2010) Feather lead concentrations and 207Pb/206Pb ratios reveal lead exposure history of California condors (Gymnogyps californianus). Environ Sci Technol 44:2639–2647CrossRefGoogle Scholar
  37. Finkelstein ME, Doak DF, George D, Burnett J, Brandt J, Church M, Grantham J, Smith DR (2012) Lead poisoning and the deceptive recovery of the critically endangered California condor. Proc Natl Acad Sci USA 109:11449–11454CrossRefGoogle Scholar
  38. Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131:421–432CrossRefGoogle Scholar
  39. Flora SJS, Tandon SK (1990) Beneficial effects of zinc supplementation during chelation treatment of lead intoxication in rats. Toxicology 64:129–139CrossRefGoogle Scholar
  40. Fullmer CS (1992) Intestinal interactions of lead and calcium. Neurotoxicology 13:799–808Google Scholar
  41. Fullmer CS (1997) Lead-calcium interactions: involvment of 1,25-dihydroxyvitamin D. Environ Res 72:45–55CrossRefGoogle Scholar
  42. Fullmer CS, Edelstein S, Wasserman RH (1985) Lead-binding properties of intestinal calcium-binding proteins. J Biol Chem 260:6816–6819Google Scholar
  43. Gochfeld JBM (2000) Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health Part B 3:59–78CrossRefGoogle Scholar
  44. Goede AA, de Bruin M (1984) The use of bird feather parts as a monitor for metal pollution. Environ Pollut Ser B 8:281–298CrossRefGoogle Scholar
  45. Goede AA, De Bruin M (1986) The use of bird feathers for indicating heavy metal pollution. Environ Monit Assess 7:249–256CrossRefGoogle Scholar
  46. Haig SM, D’Elia J, Eagles-Smith C, Fair JM, Gervais J, Herring G, Rivers JW, Schulz JH (2014) The persistent problem of lead poisoning in birds from ammunition and fishing tackle. Condor 116:408–428CrossRefGoogle Scholar
  47. Hargreaves AL, Whiteside DP, Gilchrist G (2010) Concentrations of 17 elements, including mercury, and their relationship to fitness measures in arctic shorebirds and their eggs. Sci Total Environ 408:3153–3161CrossRefGoogle Scholar
  48. Härtel H (1990) Evaluation of the dietary interaction of calcium and phosphorus in the high producing laying hen. Br Poult Sci 31:473–494CrossRefGoogle Scholar
  49. Hiller BJ, Barclay JS (2011) Concentrations of heavy metals in American woodcock harvested in Connecticut. Arch Environ Contam Toxicol 60:156–164CrossRefGoogle Scholar
  50. Hosseini Alhashemi AS, Karbassi AR, Hassanzadeh Kiabi B, Monavari SM, Nabavi SMB, Sekhavatjou MS (2011) Bioaccumulation of trace elements in trophic levels of wetland plants and waterfowl birds. Biol Trace Elem Res 142:500–516CrossRefGoogle Scholar
  51. Hsu PC, Guo YL (2002) Antioxidant nutrients and lead toxicity. Toxicology 180:33–44CrossRefGoogle Scholar
  52. Johnson GD, Audet DJ, Kern JW, LeCaptain LJ, Strickland MD, Hoffman DJ, McDonald LL (1999) Lead exposure in passerines inhabiting lead-contaminated floodplains in the Coeur D’Alene River Basin, Idaho, USA. Environ Toxicol Chem 18:1190–1194Google Scholar
  53. Kaufman CA, Bennett JR, Koch I, Reimer KJ (2007) Lead bioaccessibility in food web intermediates and the influence on ecological risk characterization. Environ Sci Technol 41:5902–5907CrossRefGoogle Scholar
  54. Kendall RJ, Lacher TE Jr, Bunck C, Daniel B, Driver C, Grue CE, Leighton F, Stansley W, Watanabe PG, Whitworth M (1996) An ecological risk assessment of lead shot exposure in non-waterfowl avian species: upland game birds and raptors. Environ Toxicol Chem 15:4–20CrossRefGoogle Scholar
  55. Kendall RJ, Scanlon PF, Di Giulio RT (1982) Toxicology of ingested lead shot in ringed turtle doves. Arch Environ Contam Toxicol 11:259–263CrossRefGoogle Scholar
  56. Keppie DM, Whiting RM Jr (1994) American woodcock (Scolopax minor). In: Poole A, Gill F (eds) The birds of North America, no 100. The Academy of Natural Sciences, Philadelphia; The American Ornithologists’ Union, Washington D.C.Google Scholar
  57. Kerr R, Holladay J, Holladay S, Tannenbaum L, Selcer B, Meldrum B, Williams S, Jarrett T, Gogal R (2011) Oral lead bullet fragment exposure in Northern bobwhite (Colinus virginianus). Arch Environ Contam Toxicol 61:668–676CrossRefGoogle Scholar
  58. Kim J, Oh J-M (2014) Lead and cadmium contaminations in feathers of heron and egret chicks. Environ Monit Assess 186:2321–2327CrossRefGoogle Scholar
  59. Kitowski I, Sujak A, Wiącek D, Komosa A (2017) Ecological factors helping to avoid the toxic element accumulation in livers of the lesser spotted eagle (Clanga pomarina Brehm) from Eastern Poland. J Elementol 22:305–314Google Scholar
  60. Koivula MJ, Eeva T (2010) Metal-related oxidative stress in birds. Environ Pollut 158:2359–2370CrossRefGoogle Scholar
  61. Komárek M, Ettler V, Chrastný V, Mihaljevic M (2008) Lead isotopes in environmental sciences: a review. Environ Int 34:562–577CrossRefGoogle Scholar
  62. Krohn WB (1977) Band-recovery distribution of eastern Maine woodcock. Wildl Soc Bull 5:118–122Google Scholar
  63. Kwong WT, Friello P, Semba RD (2004) Interactions between iron deficiency and lead poisoning: epidemiology and pathogenesis. Sci Total Environ 330:21–37CrossRefGoogle Scholar
  64. Legagneux P, Suffice P, Messier J-S, Lelievre F, Tremblay JA, Maisonneuve C, Saint-Louis R, Bety J (2014) High risk of lead contamination for scavengers in an area with high moose hunting success. PLoS ONE 9:1–7CrossRefGoogle Scholar
  65. Lester MB, Van Riper C (2014) The distribution and extent of heavy metal accumulation in song sparrows along Arizona’s upper Santa Cruz River. Environ Monit Assess 186:4779–4791CrossRefGoogle Scholar
  66. Lounsbury-Billie MJ, Rand GM, Cai Y, Bass OL (2008) Metal concentrations in osprey (Pandion haliaetus) populations in the Florida Bay estuary. Ecotoxicology 17:616–622CrossRefGoogle Scholar
  67. Lumeij JT (1985) Clinicopathologic aspects of lead poisoning in birds: a review. Vet Q 7:133–138CrossRefGoogle Scholar
  68. Marguí E, Iglesias M, Queralt I, Hidalgo M (2006) Lead isotope ratio measurements by ICP-QMS to identify metal accumulation in vegetation specimens growing in mining environments. Sci Total Environ 367:988–98CrossRefGoogle Scholar
  69. Martinez-Haro M, Taggart MA, Green AJ, Mateo R (2009) Avian digestive tract simulation to study the effect of grit geochemistry and food on Pb shot Bioaccessibility. Environ Sci Technol 43:9480–9486CrossRefGoogle Scholar
  70. Mateo R, Hoffman DJ (2001) Differences in oxidative stress between young Canada geese and mallards exposed to lead-contaminated sediment. J Toxicol Environ Health A 64:531–545CrossRefGoogle Scholar
  71. Morgan JE, Morgan AJ (1998) The distribution and intracellular compartmentation of metals in the endogeic earthworm Aporrectodea caliginosa sampled from an unpolluted and a metal-contaminated site. Environ Pollut 99:167–175CrossRefGoogle Scholar
  72. Mykkanen HM, Wasserman RH, Fullmer S (1984) Effect of phosphate on the intestinal absorption lead (203Pb) in chicks. J Nutr 114:68–75Google Scholar
  73. Niethammer KR, Atkinson RD, Baskett TS, Samson FB (1985) Metals in riparian wildlife of the lead mining district of Southeastern Missouri. Arch Environ Cont Toxicol 14:213–223CrossRefGoogle Scholar
  74. Nordberg GF, Fowler BA, Nordberg M, Friberg LT (eds) (2007) Handbook on the toxicology of metals, 3rd edn. Alternative Press, San DiegoGoogle Scholar
  75. Norman AW, Hurwitz S (1993) The role of the vitamin D endocrine system in avian bone biology. J Nutr 25:310–316Google Scholar
  76. Owen RBJ, Krohn WB (1973) Molt patterns and weight changes of the American woodcock. Wilson Bull 85:31–41Google Scholar
  77. Pain DJ (1992) Lead poisoning of waterfowl: a review. Proc IWRB Work IWRB Spec Publ 7–13Google Scholar
  78. Pain DJ, Meharg AA, Ferrer M, Taggart M, Penteriani V (2005) Lead concentrations in bones and feathers of the globally threatened Spanish imperial eagle. Biol Conserv 121:603–610CrossRefGoogle Scholar
  79. Pain DJ, Carter I, Sainsbury AW, Shore RF, Eden P, Taggart MA, Konstantinos S, Walker LA, Meharg AA, Raab A (2007) Lead contamination and associated disease in captive and reintroduced red kites (Milvus milvus) in England. Sci Total Environ 376:116–127CrossRefGoogle Scholar
  80. Pain DJ, Fisher IJ, Thomas VG (2009) A global update of lead poisoning in terrestrial birds from ammunition sources. In: Watson RT, Fuller M, Pokras M, Hunt WG (Eds.) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, p 99–118Google Scholar
  81. Pattee OH, Pain DJ (2002) Chapter 15: Lead in the environment. In: Hoffman DJ, Rattner BA, Burton GA Jr, Cairns J Jr (eds) Handbook of ecotoxicology, 2nd edn. CRC Press, p 373Google Scholar
  82. Pelicia K, Garcia E, Faitarone A, Silva AP, Berto DA, Molino AB, Vercese F (2009) Calcium and available phosphorus levels for laying hens in second production cycle. Braz J Poult Sci 11:39–49Google Scholar
  83. Peraza MA, Ayala-Fierro F, Barber DS, Casarez E, Rael LT (1998) Effects of micronutrients on metal toxicity. Environ Health Perspect 106:203–216Google Scholar
  84. Pikula J, Hajkova P, Bandouchova H, Bednarova I, Adam V, Beklova M, Kral J, Ondracek K, Osickova J, Pohanka M, Sedlackova J, Skchova H, Sobotka J, Treml F, Kizek R (2013) Lead toxicosis of captive vultures: case description and responses to chelation therapy. BMC Vet Res 9:11CrossRefGoogle Scholar
  85. Pokras MA, Kneeland MR (2009) Understanding lead uptake and effects across species lines: a conservation medicine based approach. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, p 7–22Google Scholar
  86. Poppenga RH, Tawde S (2012) Veterinary toxicology. Academic Press, Elsevier, San DiegoGoogle Scholar
  87. Rattner BA, Ackerson BK (2008) Potential environmental contaminant risks to avian species at important bird areas in the Northeastern United States. Integr Environ Assess Manag 4:344–357CrossRefGoogle Scholar
  88. Rattner BA, Franson JC, Sheffield SR, Goddard CI, Leonard NJ, Stang D, Wingate PJ (2008) Sources and implications of lead ammunition and fishing tackle on natural resources. The Wildlife Society and American Fisheries Society Technical Review Committee on Lead in the EnvironmentGoogle Scholar
  89. Rosado JL, Lo P, Kordas K, Garcia-Vargas G, Ronquillo D, Alatorre J, Stoltzfus RJ (2006) Iron and/or zinc supplementation did not reduce blood lead concentrations in children in a randomized, placebo-controlled trial. J Nutr 136:2378–2383Google Scholar
  90. Ruiz S, Espín S, Rainio M, Ruuskanen S, Salminen JP, Lilley TM, Eeva T (2016) Effects of dietary lead exposure on vitamin levels in great tit nestlings—an experimental manipulation. Environ Pollut 213:688–697CrossRefGoogle Scholar
  91. Saint-Laurent D, St-Laurent J, Hähni M, Ghaleb B, Chapados C (2010) Using lead concentrations and stable lead isotope ratios to identify contamination events in alluvial soils. Appl Environ Soil Sci 2010:1–12CrossRefGoogle Scholar
  92. Sanderson GC, Bellrose FC (1986) A review of the problem of lead poisoning in waterfowl. Illinois Nat Hist Surv Spec Publ 4:1–34.Google Scholar
  93. Sangster DF, Outridge PM, Davis WJ (2000) Stable lead isotope characteristics of lead ore deposits of environmental significance. Environ Rev 8:115–147CrossRefGoogle Scholar
  94. Scanlon PF, Brien TGO, Schauer NL, Oderwald RG (1979) Lead levels in primary feathers of American woodcocks harvested by hunters throughout the United States range. Bull Envrion Contam Toxicol 21:683–688CrossRefGoogle Scholar
  95. Scheifler R, Cœurdassier M, Morilhat C, Bernard N, Faivre B, Flicoteaux P, Giraudoux P, Noel M, Piotte P, Rieffel D, de Vaufleury A, Badot PM (2006) Lead concentrations in feathers and blood of common blackbirds (Turdus merula) and in earthworms inhabiting unpolluted and moderately polluted urban areas. Sci Total Environ 371:197–205CrossRefGoogle Scholar
  96. Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295CrossRefGoogle Scholar
  97. Scheuhammer AM (1996) Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium, and aluminum in birds. Environ Pollut 94:339–343CrossRefGoogle Scholar
  98. Scheuhammer AM, Templeton DM (1998) Use of stable isotope ratios to distinguish sources of lead exposure in wild birds. Ecotoxicology 7:37–42CrossRefGoogle Scholar
  99. Scheuhammer AM, Rogers CA, Bond D (1999) Elevated lead exposure in American woodcock (Scolopax minor) in eastern Canada. Arch Environ Contam Toxicol 340:334–340CrossRefGoogle Scholar
  100. Scheuhammer AM, Bond DE, Burgess NM, Rodrigue J (2003) Lead and stable lead isotope ratios in soil, earthworms, and bones of American woodcock (Scolopax minor) from eastern Canada. Environ Toxicol Chem 22:2585–2591CrossRefGoogle Scholar
  101. Schulz JH, Millspaugh JJ, Bermudez AJ, Gao X, Bonnot TW, Britt LG, Paine M (2006) Acute lead toxicosis in mourning doves. J Wildl Manage 70:413–421CrossRefGoogle Scholar
  102. Schulz JH, Gao X, Millspaugh JJ, Bermudex AJ (2007) Experimental lead pellet ingestion in mourning doves (Zenaida macroura). Am Midl Nat 158:177–190CrossRefGoogle Scholar
  103. Schulz JH, Feming J, Gao S (2012) 2011 Mourning Dove harest monitoring program annual report. Missouri Department of Conservation, Resource Science Division, Columbia, MO, USAGoogle Scholar
  104. Schwalfenberg GK, Genuis SJ (2015) Vitamin D, essential minerals, and toxic elements: Exploring interactions between nutrients and toxicants in clinical medicine. Sci World J 2015:1–8CrossRefGoogle Scholar
  105. Seamans ME, Rau RD (2016) American woodcock population status, 2016. U.S. Fish Wildlife Service, Laurel, MD, pp 1–17Google Scholar
  106. Smith DR, Niemeyer S, Estes JA, Flegal AR (1990) Stable lead isotopes evidence anthropogenic contamination in Alaskan sea otters. Environ Sci Technol 24:1517–1521CrossRefGoogle Scholar
  107. Sneddon J, Clemente R, Riby P, Lepp NW (2009) Source-pathway-receptor investigation of the fate of trace elements derived from shotgun pellets discharged in terrestrial ecosystems managed for game shooting. Environ Pollut 157:2663–2669CrossRefGoogle Scholar
  108. Snoeijs T, Dauwe T, Pinxten R, Darras VM, Arckens L, Eens M (2005) The combined effect of lead exposure and high or low dietary calcium on health and immunocompetence in the zebra finch (Taeniopygia guttata). Environ Pollut 134:123–132CrossRefGoogle Scholar
  109. Stevenson AL, Scheuhammer AM, Chan HM (2005) Effects of nontoxic shot regulations on lead accumulation in ducks and American woodcock in Canada. Arch Environ Contam Toxicol 48:405–413CrossRefGoogle Scholar
  110. Strom SM, Patnode KA, Langenberg JA, Bodenstein BL, Scheuhammer AM (2005) Lead contamination in American woodcock (Scolopax minor) from Wisconsin. Arch Environ Contam Toxicol 49:396–402CrossRefGoogle Scholar
  111. Strom S, Langenberg JA, Businga NK, Batten JK (2009) Lead exposure in Wisconsin birds. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion lead from spent ammunition: impliccations for wildlife and humans. The Peregine Fund, Biose, p 194–201Google Scholar
  112. Suthar S, Singh S, Dhawan S (2008) Earthworms as bioindicator of metals (Zn, Fe, Mn, Cu, Pb and Cd) in soils: is metal bioaccumulation affected by their ecological category? Ecol Eng 32:99–107CrossRefGoogle Scholar
  113. Sutherland RA, Day JP, Bussen JO (2003) Lead concentrations, isotope ratios, and source apportionment in road deposited sediments, Honolulu, Oahu, Hawaii. Water Air Soil Pollut 142:165–186CrossRefGoogle Scholar
  114. Svanberg F, Mateo R, Hillström L, Green AJ, Taggart MA, Raab A, Meharg AA (2006) Lead isotopes and lead shot ingestion in the globally threatened marbled teal (Marmaronetta angustirostris) and white-headed duck (Oxyura leucocephala). Sci Total Environ 370:416–424CrossRefGoogle Scholar
  115. Thomas VG, Scheuhammer AM, Bond DE (2009) Bone lead levels and lead isotope ratios in red grouse from Scottish and Yorkshire moors. Sci Total Environ 407:3494–3502CrossRefGoogle Scholar
  116. Tranel M, Kimmel RO (2009) Impacts of lead ammunition on wildlife, the environment, and human health—a literature review and implications for Minnesota. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, p 318–337Google Scholar
  117. Tsuji LJS, Wainman BC, Martin ID, Sutherland C, Weber JP, Dumas P, Nieboer E (2008) The identification of lead ammunition as a source of lead exposure in first nations: the use of lead isotope ratios. Sci Total Environ 393:291–298CrossRefGoogle Scholar
  118. U.S. EPA (1993) Wildlife exposure factors handbook, vol I of II. United States Environmental Protection Agency, Washington D.C.Google Scholar
  119. Vermillion B, Brugam R, Retzlaff W, Bala I (2005) The sedimentary record of environmental lead contamination at St. Louis, Missouri (USA) area smelters. J Paleolimnol 33:189–203CrossRefGoogle Scholar
  120. Vyas NB, Spann JW, Heinz GH (2001) Lead shot toxicity to passerines. Environ Pollut 111:135–138CrossRefGoogle Scholar
  121. Wasserman RH, Taylor AN (1963) Vitamin D3 inhibition of radiocalcium binding by chick intestinal homogenates. Nature 198:30–32CrossRefGoogle Scholar
  122. Wasserman RH, Taylor AN (1966) Vitamin D3-induced calcium-binding protein in chick intestinal mucosa. Science 152:791–793CrossRefGoogle Scholar
  123. Whittow GC (ed) (2000) Sturkies avian physiology, 5th edn. Academic Press, San DiegoGoogle Scholar
  124. Wong CSC, Duzgoren-Aydin NS, Aydin A, Wong MH (2007) Evidence of excessive releases of metals from primitive e-waste processing in Guiyu, China. Environ Pollut 148:62–72CrossRefGoogle Scholar
  125. Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Intern Schol Resear. Network 2011:1–20Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Amanda D. French
    • 1
  • Warren C. Conway
    • 2
  • Jaclyn E. Cañas-Carrell
    • 1
  • David M. Klein
    • 1
  1. 1.Department of Environmental Toxicology, The Institute of Environmental and Human HealthTexas Tech UniversityLubbockUSA
  2. 2.Department of Natural Resources ManagementTexas Tech UniversityLubbockUSA

Personalised recommendations