Ingestion of a Single 2.3 mm Lead Pellet by Laying Roller Pigeon Hens Reduces Egg Size and Adversely Affects F1 Generation Hatchlings

  • Robert J. Williams
  • Lawrence V. Tannenbaum
  • Susan M. Williams
  • Steven D. Holladay
  • Richard C. Tuckfield
  • Ajay Sharma
  • Danny Joe Humphrey
  • Robert M. GogalJr.Email author


Many aquatic and terrestrial avian species inadvertently ingest lead (Pb) in the form of spent or fragmented ammunition, mistaking it for food or grit. Previous studies in our laboratory have shown that ingestion of even a single 45-mg pellet can significantly increase blood-Pb levels and significantly inhibit the enzyme delta aminolevulinic-acid dehydratase (δ-ALAD) for a period of greater than 4 weeks. In the current study, proven breeder pairs of domestic Roller pigeons were housed in individual cages. The hens were orally gavaged with dH2O vehicle, a single #9 Pb pellet (2.0 mm/45 mg) or a single #7.5 Pb pellet (2.3 mm/95 mg), placed back with the cock bird and allowed to mate for two consecutive clutches. The eggs were monitored for fertilization, shell damage, egg weight, and length during the 16- to 18-day incubation period. Hatchlings remained with the hen and cock through the weaning period (28–35 days post hatch) and were monitored for weight, development, and mortality. Weanling blood was collected for blood-Pb levels, δ-ALAD activity, red blood cell counts, total protein, and packed cell volume. Following euthanasia, weanling liver, spleen, kidney, sciatic nerve, thymus, and brain were collected for histopathology. Egg weight and length were significantly decreased in the #7.5 Pb pellet treatment group for the first clutch, and hatchling weight 7 days post hatch also was significantly less in the #7.5 Pb pellet treatment group during the first clutch. Histopathologic analysis showed increased lesions in liver, kidney, spleen, and thymus of the Pb-treated weanlings, during both the first and second clutch compared with the non-Pb-treated weanlings. These data suggest that maternal consumption of a single 95-mg Pb pellet can adversely impact egg size and hatchling organ development.


Packed Cell Volume Developmental Toxicity Ebro Delta Trace Metal Grade HNO3 Total Blood Cell Count 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors thank Danny Joe Humphrey for selecting and supplying the mating pairs of birds for this study. They also thank Brent Lovern, Rose Hill, and all of the animal care workers at the University of Georgia Poultry Diagnostic and Research Center for the care of the birds. This study was funded by a Grant provided by the Department of Defense, U.S. Army Institute for Public Health.


  1. Anders E, Dietz DD, Bagnell CR, Gaynor J, Krigman MR, Ross DW, Leander JD, Mushak P (1982) Morphological, pharmacokinetic, and hematological studies of lead-exposed pigeons. Environ Res 28:344–363CrossRefGoogle Scholar
  2. Barthalamus GT, Leander JD, McMillan DE, Mushak P, Krigman MR (1977) Chronic effects of lead on schedule-controlled pigeon behavior. Toxicol Appl Pharmacol 42:271–284CrossRefGoogle Scholar
  3. Bennett JR, Kaufman CA, Koch I, Sova J, Reimer KJ (2007) Ecological risk assessment of lead contamination at rifle and pistol ranges using techniques to account for site characteristics. Sci Total Environ 374(1):91–101CrossRefGoogle Scholar
  4. Berlin A, Schaller KH (1974) European standardized method for the determination of delta-aminolevulinic acid dehydratase activity in blood. Z Klin Chem Klin Biochem 12(8):389–390Google Scholar
  5. Beyer NW, Spann JW, Sileo L, Franson CJ (1988) Lead poisoning in six captive avian species. Arch Environ Contam Toxicol 17(1):121–130CrossRefGoogle Scholar
  6. Binkowski LJ, Sawicka-Kapusta S, Szarek J, Strzyzweska E, Felsman M (2013) Histopathology of liver and kidneys of wild living Mallards Ans platyrhynchos and Coots Fulica atra with considerable concentrations of lead and cadmium. Sci Total Environ 450–451:326–333CrossRefGoogle Scholar
  7. Buerger TJ, Mirarchi RE, Lisano ME (1986) Effects of lead shot ingestion on captive mourning dove survivability and reproduction. J Wildlife Manage 50(1):1–8CrossRefGoogle Scholar
  8. Burger J, Gochfeld M (2004) Metal levels in eggs of common terns (Sterna hirundo) in New Jersey: temporal trends from 1971 to 2002. Environ Res 94(3):336–343CrossRefGoogle Scholar
  9. Cory-Slechta D, Garman RH, Seidman D (1979) Lead-induced crop dysfunction in the pigeon. Toxicol Appl Pharm 52:462–467CrossRefGoogle Scholar
  10. Craig JR, Rimstidt JD, Bonnaffon CA, Collins TK, Scanlon PF (1999) Surface water transport of lead at shooting range. Bull Environ Toxicol 63:312–319CrossRefGoogle Scholar
  11. Ferreyra H, Romano M, Beldomenico P, Caselli A, Correa A, Uhart M (2014) Lead gunshot pellet ingestion and tissue lead levels in wild ducks from Argentine hunting hotspots. Ecotox Environ Saf 103:74–81CrossRefGoogle Scholar
  12. Griffin TB, Couiston F, Wills H (1975) Biological and clinical effects of continuous exposure to airborne particulate lead. Arh Hig Toksikol 26:191–208Google Scholar
  13. Haig SM, D’Elia J, Eagles-Smith C, Fair JM, Gervais J, Herring G, River JW, Schulz JH (2014) The persistent problem of lead poisoning in birds form ammunition and fishing tackle. Condor Ornithol Appl 116:408–428Google Scholar
  14. Hanna-Attisha M, LaChance J, Sadler RC, Champney Schnepp A (2016) Elevated blood lead levels in children associated with the Flint drinking water crisis: a spatial analysis of risk and public health response. Am J Public Health 106(2):283–290CrossRefGoogle Scholar
  15. Holladay JP, Nisanian M, Williams S, Tuckfield RC, Kerr R, Jarret T, Tannenbaum L, Holladay SD, Sharma A, Gogal RM Jr (2012) Dosing of adult pigeons with as little as one #9 lead pellet caused severe δ-ALAD depression, suggesting potential adverse effects in wild populations. Ecotoxicology 21(8):2331–2337CrossRefGoogle Scholar
  16. Kendall RJ, Scanlon PF (1981) Effects of chronic lead ingestion on reproductive characteristics of ringed turtle doves Streptopelia risoria and on tissue lead concentrations of adults and their progeny. Environ Pollut A Ecol Biol 23(3):203–213CrossRefGoogle Scholar
  17. Kerr R, Holladay J, Holladay S, Tannenbaum L, Selcer B, Meldrum B et al (2011) Oral lead bullet fragment exposure in northern bobwhite (Colinus virgianus). Arch Environ Contam Toxicol 61(4):668–676CrossRefGoogle Scholar
  18. Lee J, Dietert RR (2003) Developmental immunotoxicity of lead: impact on thymic function. Birth Defects Res A Clin Mol Teratol 67(10):861–867CrossRefGoogle Scholar
  19. Lee J, Naqi SA, Kao E, Dietert RR (2001) Embryonic exposure to lead: comparison of immune and cellular responses in unchallenged and virally stressed chickens. Arch Toxicol 75:717–724CrossRefGoogle Scholar
  20. Locke LN, Bagley GE, Irby HD (1966) Acid-fast intranuclear inclusion bodies in the kidneys of mallards fed lead shot. Bull Wildlife Dis Assoc 2(4):127–131CrossRefGoogle Scholar
  21. Mateo R, Beyer WN, Spann J, Hoffman D, Ramis A (2003) Relationship between oxidative stress, pathology, and behavioral signs of lead poisoning in Mallards. J Toxicol Environ Health A 66(17):1371–1389CrossRefGoogle Scholar
  22. Matero R (2009) Lead poisoning in wild birds in Europe and the regulations adopted by different countries. Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, IdahoGoogle Scholar
  23. Needleman HL (2000) The removal of lead from gasoline: historical and personal reflections. Environ Res A 84:20–35CrossRefGoogle Scholar
  24. Pain DJ, Fisher IJ, Thomas VG (2009) A global update of lead poisoning in terrestrial birds from ammunition sources. Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, IdahoGoogle Scholar
  25. Pant N, Upadhyay G, Pandey S, Mathur N, Saxena DK, Srivastava SP (2003) Lead and cadmium concentration in the seminal plasma of men in the general population: correlation with sperm quality. Reprod Toxicol 17:447–450CrossRefGoogle Scholar
  26. Peddicord RK, LaKind JS (2000) Ecological and human health risks at outdoor firing range. Environ Toxicol Chem 19:2602–2613CrossRefGoogle Scholar
  27. Rabinowitz MB, Wetherill GW, Kopple JD (1976) Kinetic analysis of lead metabolism in healthy humans. J Clin Invest 58:260–270CrossRefGoogle Scholar
  28. Taggart MA, Green AJ, Mateo R, Meharg AA (2008) Metal levels in the bones and livers of globally threatened marbled teal and white-headed duck from El Hondo, Spain. Ecotox Environ Saf 72(1):1–9CrossRefGoogle Scholar
  29. Tsipora N, Burger J, Newhouse M, Christian J, Gochfeld M, Mizrahi D (2011) Lead, mercury, cadmium, chromium, and arsenic levels in eggs, feathers, and tissues of Canada geese of the New Jersey Meadowlands. Environ Res 111:775–784CrossRefGoogle Scholar
  30. Vallverdú-Coll N, Lopez-Antia A, Martinez-Haro M, Ortiz-Santaliestra ME, Mateo R (2015a) Altered immune response in mallard ducklings exposed to lead through maternal transfer in the wild. Environ Pollut 205:350–356CrossRefGoogle Scholar
  31. Vallverdú-Coll N, Mougeot F, Ortiz-Santaliestra ME, Rodriguez-Estival J, López-Antia A, Mateo R (2015b) Lead exposure reduces carotenoid-based coloration and constitutive immunity in wild mallards. Environ Toxicol Chem 35(6):1516–1525CrossRefGoogle Scholar
  32. Vallverdú-Coll N, Ortiz-Santaliestra ME, Mougeot F, Vidal D, Mateo R (2015c) Sublethal Pb exposure produces season-dependent effects on immune response, oxidative balance and investment in carotenoid-based coloration in red-legged partridges. Environ Sci Technol 49(6):3839–3850CrossRefGoogle Scholar
  33. Vallverdú-Coll N, Mougeot F, Ortiz-Santaliestra ME, Castano C, Santiago-Moreno J, Mateo R (2016) Effects if lead exposure on sperm quality and reproductive success in an avian model. Environ Sci Technol 50(22):12484–12492CrossRefGoogle Scholar
  34. Vigeh M, Smith DR, Hsu PC (2011) How does lead induce male infertility? Iran J Reprod Med 9(1):1–8Google Scholar
  35. Wang H, Li S, Teng X (2016) The antagonistic effect of selenium on lead-induced inflammatory factors and heat shock proteins mRNA expression in chicken livers. Biol Trace Elem Res 171:437–444CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Robert J. Williams
    • 1
  • Lawrence V. Tannenbaum
    • 2
  • Susan M. Williams
    • 3
  • Steven D. Holladay
    • 1
  • Richard C. Tuckfield
    • 4
  • Ajay Sharma
    • 1
  • Danny Joe Humphrey
    • 5
  • Robert M. GogalJr.
    • 1
    Email author
  1. 1.Department of Veterinary Biosciences and Diagnostic Imagining, College of Veterinary MedicineUniversity of GeorgiaAthensUSA
  2. 2.U.S. Army Institute of Public HealthAberdeenUSA
  3. 3.Poultry Diagnostic and Research Center, College of Veterinary MedicineUniversity of GeorgiaAthensUSA
  4. 4.Savannah River Ecology LaboratoryUniversity of GeorgiaAikenUSA
  5. 5.Color PigeonsKinstonUSA

Personalised recommendations