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Dietary Exposure to Tebuconazole Affects Testicular and Epididymal Histomorphometry in Frugivorous Bats

Abstract

This study evaluated the effects of a commercially recommended concentration (1 mL/L) of a fungicide tebuconazole (TBZ) on testicular and epididymal histomorphometry of Artibeus lituratus, following 7 and 30-day oral exposure. TBZ30 bats showed a reduction in the percentage of tubules and seminiferous epithelium, as well as a decrease in tubule and epithelium somatic indexes, and tubular diameter. Inversely, these animals showed increased percentage of intertubular compartment, Leydig cells and blood vessels. The volume of Leydig cells and their number per gram of testis also increased in TBZ30 bats. Alterations in epididymal morphometry were observed in all regions of the organ, with increase of ductal diameter in both exposure times. These results indicate that exposure to low concentration of TBZ resulted in testicular and epididymal morphometric changes in fruit bats, mainly at 30-day exposure, suggesting that functional alterations might be occurring in these organs and impacting reproductive capacity.

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References

  1. Amaral TS, Carvalho TF, Silva MC et al (2012) Metabolic and histopathological alterations in the fruit-eating bat Artibeus lituratus induced by the organophosphorous pesticide fenthion. Acta Chiropter 14:225–232

    Article  Google Scholar 

  2. Bartlewicz J, Pozo MI, Honnay O, Lievens B, Jacquemyn H (2016) Effects of agricultural fungicides on microorganisms associated with floral nectar: susceptibility assays and field experiments. Environ Sci Pollut Res 23:19776–19786

    Article  CAS  Google Scholar 

  3. Belleanneé C, Thimon V, Sullivan R (2012) Region-specific gene expression in the epididymis. Cell Tissue Res 349:717–731

    Article  Google Scholar 

  4. Blanco A, Moyano R, Vivo J et al (2007) Quantitative changes in the testicular structure in mice exposed to low doses of cadmium. Environ Toxicol Pharmacol 23:93–101

    Article  CAS  Google Scholar 

  5. Byskov AG, Andersen CY, Nordholm L, Thogersen H, Xia G, Wassmann O (1995) Chemical structure of sterols that activate oocyte meiosis. Nature 374:559–562

    Article  CAS  Google Scholar 

  6. Cao S, Ye L, Wu Y, Mao B, Chen L, Wang X, Huang P, Su Y, Ge RS (2017) The effects of fungicides on human 3β-hydroxysteroid dehydrogenase 1 and aromatase in human placental cell line JEG-3. Pharmacology 100:139–147

    Article  CAS  Google Scholar 

  7. Castro MM, Gonçalves WG, Teixeira SAMV, Fialho MCQ, Santos FC, Oliveira JM, Serrão JE, Machado-Neves M (2017) Ultrastructure and morphometric features of epididymal epithelium in Desmodus rotundus. Micron 102:35–43

    Article  Google Scholar 

  8. Cecconi S, Paro R, Rossi G, Macchiarelli G (2007) The effects of endocrine disruptors dithiocarbamates on the mammalian ovary with particular regard to mancozeb. Curr Pharm Des 13:2989–3004

    Article  CAS  Google Scholar 

  9. Clegg ED, Perreault SD, Klinefelter GR (2001) Assessment of male reproductive toxicity. In: Principles and methods of toxicology, 4th edn. Taylor & Francis, Philadelphia, pp 1263–1300

    Google Scholar 

  10. Cornwall GA (2009) New insights into epididymal biology and function. Hum Reprod Update 15:223–227

    Google Scholar 

  11. Debeljak N, Horvat S, Vouk K, Lee M, Rozman D (2000) Characterization of the mouse lanosterol 14alphademethylase (CYP51), a new member of the evolutionarily most conserved cytochrome P450 family. Arch Biochem Biophys 379:37–45

    Article  CAS  Google Scholar 

  12. Domeniconi RF, Souza ACF, Xu B, Washington AM, Hinton BT (2016) Is the epididymis a series of organs placed side by side? Biol Reprod 95:1–8

    Article  CAS  Google Scholar 

  13. Fernandez CDB, Porto EM, Arena AC, Kempinas WG (2008) Effects of altered epididymal sperm transit time on sperm quality. Int J Androl 31:427–437

    Article  Google Scholar 

  14. França LR, Russell LD (1998) The testis of domestic mammals. In: Martinez-Garcia Regadera J (ed) Male reproduction: a multidisciplinary overview. Churchill Livingstone, Madrid, pp 197–219

    Google Scholar 

  15. Fu Y, Zheng Z, Wei P, Wang M, Zhu G, Liu Y (2016) Distribution of thifluzamide, fenoxanil and tebuconazole in rice paddy and dietary risk assessment. Toxicol Environ Chem 98:118–127

    Article  CAS  Google Scholar 

  16. Gerell R, Lunderg KG (1993) Decline of a bat Pipistrellus pipistrellus population in an industrialized area in south Sweden. Biol Conserv 65:153–157

    Article  Google Scholar 

  17. Goetz AK, Rockett JC, Ren H, Thillainadarajah I, Dix DJ (2009) Inhibition of rat and human steroidogenesis by triazole antifungals. Syst Biol Reprod Med 55:214–226

    Article  CAS  Google Scholar 

  18. Gorchov DL, Cornejo F, Ascorra C, Jaramillo M (1993) The role of seed dispersal in the natural regeneration of rain forest after stripcutting in the Peruvian Amazon. In: Fleming TH, Estrada A (eds) Frugivory and seed dispersal: ecological and evolutionary aspects. W. Kluwer Academic Publishers, Dordrecht, pp 339–349

    Chapter  Google Scholar 

  19. Gray LE, Wilson VS, Stoker T, Lambright C, Furr J, Noriega N, Howdeshell K, Ankley GT, Guillette L (2006) Adverse effects of environmental antiandrogens and androgens on reproductive development in mammals. Int J Androl 29:96–104

    Article  CAS  Google Scholar 

  20. Hass U, Boberg J, Christiansen S, Jacobsen PR, Vinggaard AM, Taxvig C, Poulsen ME, Herrmann SS, Jensen BH, Petersen A, Clemmensen LH, Axelstad M (2012) Adverse effects on sexual development in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reprod Toxicol 34:261–274

    Article  CAS  Google Scholar 

  21. Joshi SC, Gulati N (2005) Effects of tebuconazole on reproductive function of male rat. J Cell Tissue Res 5:457–460

    CAS  Google Scholar 

  22. Joshi SC, Nandan G, Bhawana S, Priyanka S (2016) Effects of tebuconazole (a fungicide) on reproduction of male rat. Int J Pharma Res Health Sci 4:1489–1494

    CAS  Article  Google Scholar 

  23. Kwok IM-Y, Loeffler RT (1993) The biochemical mode of action of some newer azole fungicides. Pestic Sci 39:1–11

    Article  CAS  Google Scholar 

  24. Melo BES, Barros MS, Carvalho TF, Amaral TS, Freitas MB (2012) Energy reserves of Artibeus lituratus (Chiroptera: Phyllostomidae) in two areas with different degrees of conservation in Minas Gerais, Brazil. Braz J Biol 72:181–187

    Article  CAS  Google Scholar 

  25. Mispagel C, Allinson M, Allinson G, Iseki N, Grant C, Morita M (2004) DDT and metabolites residues in the southern bent-wing bat (Miniopterus schreibersii bassanii) of south-eastern Australia. Chemosphere 55:997–1003

    Article  CAS  Google Scholar 

  26. Morais ACT, Balarini MK, Lopes EO, Menezes TP, Quintela FM, Morais DB, Gomes Mde L, Matta SL (2014) The tubular compartment and the spermatogenic dynamics of the wild rodent Oxymycterus nasutus (Rodentia: Cricetidae). Anim Reprod Sci 149:249–258

    Article  Google Scholar 

  27. Mori H, Christensen K (1980) Morphometric analysis of Leydig cells in the normal rat testis. J Cell Biol 84:340–354

    Article  CAS  Google Scholar 

  28. Moser VC, Barone S Jr, Smialowicz RJ, Harris MW, Davis BJ, Overstreet D, Mauney M, Chapin RE (2001) The effects of perinatal tebuconazole exposure on adult neurological, immunological, and reproductive function in rats. Toxicol Sci 62:339–352

    Article  CAS  Google Scholar 

  29. Qi S. Liu X, Zhu L, Chen X, Wang C (2018) Racemic, R-, and S-tebuconazole altered chitinase and chitobiase activity of Daphnia magna. J Environ Sci Health B 53:171–175

    Article  CAS  Google Scholar 

  30. Robertson KM, O’Donnell L, Jones ME, Meachem SJ, Boon WC, Fisher CR, Graves KH, McLachlan RI, Simpson ER (1999) Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc Natl Acad Sci USA 96:7986–7991

    Article  CAS  Google Scholar 

  31. Russell LD, Ettlin RA, Sinha-Hikim AP, Clegg ED (1990) Histological and histopathological evaluation of the testis. Cache River Press, Clearwater, Florida

    Google Scholar 

  32. Sancho E, Fernández-Vega C, Villarroel MA, Andreu-Moliner E, Ferrando MA (2009) Physiological effects of tricyclazole on zebrafish (Danio rerio) and post-exposure recovery. Comp Biochem Physiol C Toxicol Pharmacol 150:25–32

    Article  CAS  Google Scholar 

  33. Shen Z, Zhu W, Liu D, Xu X, Zhang P, Zhou Z (2012) Stereoselective degradation of tebuconazole in rat liver microsomes. Chirality 24:67–71

    Article  CAS  Google Scholar 

  34. Siu ER, Mruk DD, Porto CS, Cheng CY (2009) Cadmium-induced testicular injury. Toxicol Appl Pharmacol 238:240–249

    Article  CAS  Google Scholar 

  35. Souza ACF, Marchesi SC, Liman GDA, Ferraz RP, Santos FC, da Matta SLP, Machado-Neves M (2016) Effects of sodium arsenite and arsenate in testicular histomorphometry and antioxidants enzymes activities in rats. Biol Trace Elem Res 171:354–362

    Article  CAS  Google Scholar 

  36. Swanepoel RE, Racey PA, Shore RF, Speakman JR (1999) Energetic effects of sublethal exposure to lindane on pipistrelle bats (Pipistrellus pipistrellus). Environ Pollut 104:169–177

    Article  CAS  Google Scholar 

  37. Taboga SR, Souza RS, Santos DC, Oliani SM (1999) Spontaneous germ cell death by apoptosis in epididymis of the adult bat Artibeus lituratus. Cytobios 99:3945

    Google Scholar 

  38. Taxvig C, Hass U, Axelstad M, Dalgaard M, Boberg J, Andeasen HR, Vinggaard AM (2007) Endocrine-disrupting activities in vivo of the fungicides tebuconazole and epoxiconazole. Toxicol Sci 100:464–473

    Article  CAS  Google Scholar 

  39. Vinggaard AM, Hnida C, Breinholt V, Larsen JC (2000) Screening of selected pesticides for inhibition of CYP19 aromatase activity in vitro. Toxicol in vitro 14:227–234

    Article  CAS  Google Scholar 

  40. Walker UJ, Nogués V (1994) Changes induced by treatment with aromatase inhibitors in testicular Leydig cells of rats and dogs. Exp Toxicol Pathol 46:211–213

    Article  CAS  Google Scholar 

  41. Zhao W, Uehera S, Tanaka K, Tadokoro S, Kusamori K, Katsumi H, Sakane T, Yamamoto A (2016) Effects of polyoxyethylene alkyl ethers on the intestinal transport and absorption of rhodamine 123: a P-glycoprotein substrate by in vitro and in vivo studies. J Pharm Sci 105:1526–1534

    Article  CAS  Google Scholar 

  42. Zhar JH (2010) Biostatistical analysis, 4th edn. Upper Saddle River, Prentice-Hall

    Google Scholar 

  43. Zhou J, Zhang J, Li F, Liu J (2016) Triazole fungicide tebuconazole disrupts human placental trophoblast cell functions. J Hazard Mater 308:294–302

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Master fellowship to MJON and DCM), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (APQ-02514-16 to MMN) and Conselho Nacional de Desenvolvimento Científico e Tecnlógico (448455/2014-5 to MMN; Postdoctoral fellowship 150333/2018-8 to ACFS).

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Correspondence to Mariana Machado-Neves.

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Machado-Neves, M., Neto, M.J.O., Miranda, D.C. et al. Dietary Exposure to Tebuconazole Affects Testicular and Epididymal Histomorphometry in Frugivorous Bats. Bull Environ Contam Toxicol 101, 197–204 (2018). https://doi.org/10.1007/s00128-018-2377-6

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Keywords

  • Reproductive toxicology
  • Fungicides
  • Testis
  • Epididymis
  • Stereology
  • Artibeus lituratus