Effects of Experimental Lead Exposure on Testis of the Chestnut Capped Blackbird Chrysomus ruficapillus

  • Danusa Leidens
  • Adalto Bianchini
  • Antonio Sergio Varela Junior
  • Indianara Fernanda Barcarolli
  • Carlos Eduardo Rosa
  • Josiane Bonnel
  • Cecilia Perez Calabuig
  • Carine Dahl CorciniEmail author


Lead (Pb) effects on testis histology, as well as sperm quality and oxidative status were evaluated in male Chestnut Capped Blackbird (Chrysomus ruficapillus). Wild blackbirds were captured, immediately sampled (field group) or kept in captivity and treated with a single intraperitoneal injection of saline solution (control) or saline solution with Pb acetate (50 or 100 mg/kg Pb). Seven days after injection, whole blood, ductus deferens and testis samples were collected. Increased Pb concentrations were observed in whole blood and testis of Pb-exposed blackbirds with respect to those from field and control blackbirds. Sperm cells of Pb-exposed blackbirds showed loss of membrane integrity, mitochondrial functionality, and DNA integrity. Also, oxidative damage was observed in testis of blackbirds injected with 100 mg/kg Pb. These findings indicate that Pb is accumulated in testis of C. ruficapillus, inducing severe morphological and biochemical injury that can compromise the reproductive performance of male blackbirds. Although the exposure scenario (Pb acetate, high dosage and intraperitoneal injection) tested in the present study would likely not occur in the wild, it was adequate to show potential and relevant toxic effects of Pb in wild birds.


Blackbird Histopathology Lead toxicity Reproduction Sperm 



The present study was financially supported by the Brazilian Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). A. Bianchini and C.D. Corcini are research fellows from the Brazilian CNPq. Authors are grateful to “Granjas Quatro Irmãos” for field assistance.


  1. Acharya UR, Rathore RM, Mishra M (2003) Role of vitamin C on lead acetate induced spermatogenesis in Swiss mice. Environ Toxicol Pharmacol 13:9–14. CrossRefGoogle Scholar
  2. Almansour MI (2009) Histological alterations induced by lead in the testes of the quail Coturnix coturnix. Res J Environ Toxicol 3:24–30. CrossRefGoogle Scholar
  3. Amado LL, Garcia ML, Ramos PB, Freitas RF, Zafalon B, Ferreira JL, Yunes JS, Monserrat JM (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci Total Environ 407:2115–2123. CrossRefGoogle Scholar
  4. ATSDR (2017) ATSDR’s substance priority list. Agency for toxicy substances and disease registry. Accessed 27 Nov 2017
  5. Beyer WN, Franson JC, French JB, May T, Rattner BA, Shearn-Bochsler VI, Warner SE, Weber J, Mosby D (2013) Toxic exposure of songbirds to lead in the Southeast Missouri Lead Mining District. Arch Environ Contam Toxicol 65:598–610. CrossRefGoogle Scholar
  6. Buekers J, Redeker ES, Smolders E (2009) Lead toxicity to wildlife: derivation of a critical blood concentration for wildlife monitoring based on literature data. Sci Total Environ 407:3431–3438. CrossRefGoogle Scholar
  7. Burger J, Gochfeld M (2004) Effects of lead and exercise on endurance and learning in young herring gulls. Ecotoxicol Environ Saf 57:136–144. CrossRefGoogle Scholar
  8. Burger J, Gochfeld M (2005) Effects of lead on learning in herring gulls: an avian wildlife model for neurobehavioral deficits. Neurotoxicology 26:615–624. CrossRefGoogle Scholar
  9. Carson FL, Hladik C (2009) Histotechnology: a self-instructional text. American Society for Clinical Pathology Press, ChicagoGoogle Scholar
  10. 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 32:1641–1648. CrossRefGoogle Scholar
  11. Cerolini S, Zaniboni L, Maldjian A, Gliozzi T (2006) Effect of docosahexaenoic acid and atocopherol enrichment in chicken sperm on semen quality, sperm lipid composition and susceptibility to peroxidation. Theriogenology 66:877–886. CrossRefGoogle Scholar
  12. Chapa-Vargas L, Mejia-Saavedra JJ, Monzalvo-Santos K, Puebla-Olivares F (2010) Blood lead concentrations in wild birds from a polluted mining region at Villa de La Paz, San Luis Potosi, Mexico. J Environ Sci Health Part A 45:90–98. CrossRefGoogle Scholar
  13. Cirne MP, López-Iborra GM (2005) Breeding biology of Chestnut-capped Blackbirds in rice paddies in southern Brazil. J Field Ornithol 76:411–416. CrossRefGoogle Scholar
  14. Coeurdassier M, Fritsch C, Faivre B, Crini N, Scheifler R (2012) Partitioning of Cd and Pb in the blood of European blackbirds (Turdus merula) from a smelter contaminated site and use for biomonitoring. Chemosphere 87:1368–1373. CrossRefGoogle Scholar
  15. Dauwe T, Janssens E, Kempenaers B, Eens M (2004) The effect of heavy metal exposure on egg size, eggshell thickness and the number of spermatozoa in blue tit Parus caeruleus eggs. Environ Pollut 129:125–129. CrossRefGoogle Scholar
  16. Doumouchtsis KK, Doumouchtsis SK, Doumouchtsis EK, Perrea DN (2009) The effect of lead intoxication on endocrine functions. J Endocrinol Invest 2:175–183. CrossRefGoogle Scholar
  17. Fahim MA, Tariq S, Adeghate E (2013) Vitamin E modifies the ultrastructure of testis and epididymis in mice exposed to lead intoxication. Ann Anat 195:272–277. CrossRefGoogle Scholar
  18. Franson JC, Pain DJ (2011) Lead in birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations, 2nd edn. CRC Press, Boca Raton, pp 563–593CrossRefGoogle Scholar
  19. Furness RW, Greenwood JJD (1993) Birds as monitors of environmental change. Chapman and Hall, LondonCrossRefGoogle Scholar
  20. Garu U, Sharma R, Barber I (2011). Effect of lead toxicity on developing testis of mice. Int J Pharm Sci Res 2:2403–2407. Google Scholar
  21. Harrison RAP, Vickers SE (1990) Use of fluorescent probes to assess membrane integrity in mammalian spermatozoa. J Reprod Fertil 88:343–352. CrossRefGoogle Scholar
  22. Hermes-Lima M, Willmore G, Storey KB (1995) Quantification of lipid peroxidation in tissue extracts based on Fe(III) xylenol orange complex formation. Free Radical Biol Med 19:271–280. CrossRefGoogle Scholar
  23. Hernandez-Ochoa I, Sanchez-Gutierrez M, Solis-Heredia MJ, Quintanilla-Veja B (2006) Spermatozoa nucleus takes up lead during the epididymal maturation altering chromatin condensation. Reprod Toxicol 21:171–178. CrossRefGoogle Scholar
  24. Hong SH, Shim WJ, Han GM, Ha SY, Jang M, Rani M, Hong S, Yeo GY (2014) Levels and profiles of persistent organic pollutants in resident and migratory birds from an urbanized coastal region of South Korea. Sci Total Environ 470–471:1463–1470. CrossRefGoogle Scholar
  25. McDowell SK, Conway WC, Haukos DA, Moon JA, Comer CE, Hung I-K (2015) Blood lead exposure concentrations in mottled ducks (Anas fulvigula) on the upper Texas coast. JSAFWA 2:221–228Google Scholar
  26. McLean DJ, Korn N, Perez BS, Thurston RJ (1993) Isolation and characterization of mitochondria from turkey spermatozoa. J Androl 14:433–438. Google Scholar
  27. Mishra M, Acharya UR (2004) Protective action of vitamins on the spermatogenesis in lead treated Swiss mice. J Trace Elem Med Biol 18:173–178. CrossRefGoogle Scholar
  28. Myhre O, Fonnum F (2001) The effect of aliphatic, naphtenic and aromatic hydrocarbons on production of reactive oxygen species and reactive nitrogen species in rat brain synaptosome fraction: the involvement of calcium, nitric oxide synthase, mitochondria and phospholipase A. Biochem Pharmacol 62:119–128. CrossRefGoogle Scholar
  29. Pain DJ (1996) Lead in waterfowl. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife: interpreting tissue concentrations. CRC Press, Boca Raton, pp 251–264Google Scholar
  30. Riecke TV, Conway WC, Haukos DA, Moon JA, Comer CE (2015) Baseline blood Pb concentrations in black-necked stilts on the upper Texas coast. Bull Environ Contam Toxicol 95:465–469. CrossRefGoogle Scholar
  31. Scheifler R, Cœurdassier M, Morilhat C, Bernard N, Faivre B, Flicoteaux P, Giraudoux P, Noël 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 371:197–205. CrossRefGoogle Scholar
  32. Tsipoura N, Burger J, Feltes R, Yacabucci J, Mizrahi D, Jeitner C, Gochfeld M (2008) Metal concentrations in three species of passerine birds breeding in the Hackensack Meadowlands of New Jersey. Environ Res 107:218–228. CrossRefGoogle Scholar
  33. Włostowski T, Dmowski K, Bonda-Ostaszewska E (2010) Cadmium accumulation, metallothionein and glutathione levels, and histopathological changes in the kidneys and liver of magpie (Pica pica) from a zinc smelter area. Ecotoxicology 19:1066–1073. CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Danusa Leidens
    • 1
  • Adalto Bianchini
    • 2
  • Antonio Sergio Varela Junior
    • 2
  • Indianara Fernanda Barcarolli
    • 2
  • Carlos Eduardo Rosa
    • 2
  • Josiane Bonnel
    • 4
  • Cecilia Perez Calabuig
    • 3
  • Carine Dahl Corcini
    • 1
    • 4
    Email author
  1. 1.Programa de Pós-Graduação em Ciências Fisiológicas - Instituto de Ciências BiológicasUniversidade Federal do Rio Grande - FURGRio GrandeBrazil
  2. 2.Instituto de Ciências BiológicasUniversidade Federal do Rio Grande - FURGRio GrandeBrazil
  3. 3.Departamento de Ciências AnimaisUniversidade Federal Rural do SemiáridoMossoróBrazil
  4. 4.Departamento de Patologia, Faculdade de VeterináriaUniversidade Federal de Pelotas - UFPELPelotasBrazil

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