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

Abstract

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.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  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 28:344–363

    CAS  Article  Google 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 42:271–284

    Article  Google 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):91–101

    CAS  Article  Google 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):389–390

    CAS  Google Scholar 

  5. Beyer NW, Spann JW, Sileo L, Franson CJ (1988) Lead poisoning in six captive avian species. Arch Environ Contam Toxicol 17(1):121–130

    CAS  Article  Google 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 450–451:326–333

    Article  Google 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):1–8

    CAS  Article  Google 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):336–343

    CAS  Article  Google Scholar 

  9. Cory-Slechta D, Garman RH, Seidman D (1979) Lead-induced crop dysfunction in the pigeon. Toxicol Appl Pharm 52:462–467

    Article  Google Scholar 

  10. Craig JR, Rimstidt JD, Bonnaffon CA, Collins TK, Scanlon PF (1999) Surface water transport of lead at shooting range. Bull Environ Toxicol 63:312–319

    CAS  Article  Google 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 103:74–81

    CAS  Article  Google Scholar 

  12. Griffin TB, Couiston F, Wills H (1975) Biological and clinical effects of continuous exposure to airborne particulate lead. Arh Hig Toksikol 26:191–208

    Google 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 116:408–428

    Google 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):283–290

    Article  Google 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):2331–2337

    CAS  Article  Google 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):203–213

    Article  Google 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):668–676

    CAS  Article  Google Scholar 

  18. Lee J, Dietert RR (2003) Developmental immunotoxicity of lead: impact on thymic function. Birth Defects Res A Clin Mol Teratol 67(10):861–867

    CAS  Article  Google 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 75:717–724

    Article  Google 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):127–131

    Article  Google 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):1371–1389

    CAS  Article  Google 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, Idaho

  23. Needleman HL (2000) The removal of lead from gasoline: historical and personal reflections. Environ Res A 84:20–35

    CAS  Article  Google 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, Idaho

  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 17:447–450

    CAS  Article  Google Scholar 

  26. Peddicord RK, LaKind JS (2000) Ecological and human health risks at outdoor firing range. Environ Toxicol Chem 19:2602–2613

    CAS  Article  Google Scholar 

  27. Rabinowitz MB, Wetherill GW, Kopple JD (1976) Kinetic analysis of lead metabolism in healthy humans. J Clin Invest 58:260–270

    CAS  Article  Google 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):1–9

    Article  Google 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 111:775–784

    Article  Google 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 205:350–356

    Article  Google 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):1516–1525

    Article  Google 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):3839–3850

    Article  Google 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):12484–12492

    Article  Google Scholar 

  34. Vigeh M, Smith DR, Hsu PC (2011) How does lead induce male infertility? Iran J Reprod Med 9(1):1–8

    Google 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 171:437–444

    CAS  Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Robert M. Gogal Jr..

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Williams, R.J., Tannenbaum, L.V., Williams, S.M. et al. Ingestion of a Single 2.3 mm Lead Pellet by Laying Roller Pigeon Hens Reduces Egg Size and Adversely Affects F1 Generation Hatchlings. Arch Environ Contam Toxicol 73, 513–521 (2017). https://doi.org/10.1007/s00244-017-0406-9

Download citation

Keywords

  • Packed Cell Volume
  • Developmental Toxicity
  • Ebro Delta
  • Trace Metal Grade HNO3
  • Total Blood Cell Count