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Histopathological effects of carbaryl on testes of snake-eyed lizard, Ophisops elegans

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Abstract

Background, aim and scope

Due to their ecological niche and insectivore nature, lizards are of increased risk of exposure to pesticides in agricultural areas. In addition to their potential direct effects on non-target species, insecticides can also result in indirect impacts on lizard population by reducing their food source. Carbaryl is a common insecticide that is widely used in areas of Turkey that are home to a variety of reptiles. However, to date, little is known about the potential effects of the exposure of reptiles such as lizards or snakes to this pesticide. The aim of the study was to investigate toxic effects of carbaryl on the testes of snake-eyed lizard, Ophisops elegans that is common to regions in Turkey where Carbaryl is applied and that it can be easily cultured in the laboratory.

Material and methods

Adult male lizards were exposed to carbaryl once by oral gavage in concentrations of 2.5, 25 and 250 μg/g. After 96 h, lizards were euthanized and dissected. Histopathological changes were detected by randomly counting 100 tubules in each lizard. Seminiferous tubules were categorized as normal, sloughing and disorganized tubules. Diameters of tubules were also measured. The differences in histopathological changes and tubule diameters were compared for statistical significance by one-way ANOVA, using SPSS 16.0.

Results and discussion

Histopathological changes were more prominent in medium- (25 μg/g) and high-dose (250 μg/g) groups than in the low-dose (2.5 μg/g) group. In the medium-dose group, the hexagonal appearance of most tubules disappeared, and they took on an oval shape. Sloughing was the characteristic tubule appearance of the medium group. In the high-dose group, significant increases in the number of disorganized tubules and prominence of haemorrhages was observed.

Conclusion

Carbaryl caused histopathological defects on the testes of O. elegans, so it is clear that carbaryl affects male fertility in O. elegans.

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References

  • Afifi NA, Ramadan A, Abd-El-Aziz MI, Saki EE (1991) Influence of dimethoate on testicular and epididymal organs, testosterone plasma level and their tissue residues in rats. Dtsch Tierarztl Wochenschr 98:419–420

    CAS  Google Scholar 

  • Archana R, Sahai A, Srivastava AK, Anita R (2007) Carbaryl induce histopathological changes in the testis of albino rats. J Anat Soc India 56(1):4–6

    Google Scholar 

  • Bacchetta R, Mantecca P, Andrioletti M, Vismara C, Vailati G (2008) Axial-skeletal defects caused by carbaryl in Xenopus laevis embryos. Sci Total Environ 392:110–118

    Article  CAS  Google Scholar 

  • Bain D, Buttemer WA, Astheimer L, Fildes K, Hooper MJ (2004) Effects of sublethal fenitrothion ingestion on cholinesterase inhibition, standard metabolism, thermal preference, and prey-capture ability in the Australian central bearded dragon (Pogona vitticeps, Agamidae). Environ Toxicol Chem 23:109–116

    Article  CAS  Google Scholar 

  • Baron RL (1991) Carbamate insecticides. In: Hayes WJ Jr, Laws FL Jr (eds) Handbook of pesticide toxicology, vol. 3. Academic, New York, pp 1125–1189

    Google Scholar 

  • Boone MD, Bridges CM (2003) Effects of carbaryl on green frog (Rana clamitans) tadpoles: timing of exposure versus multiple exposures. Environ Toxicol Chem 22:2695–2702

    Article  CAS  Google Scholar 

  • Boone MD, Semlitsch RD, Fairchild JF, Rothermel BB (2004) Effects of an insecticide on amphibians in large-scale experimental ponds. Ecol Appl 14:685–691

    Article  Google Scholar 

  • Brasfield SM, Weber LP, Talent LG, Janz DM (2002) Dose-response and time course relationships for vitellogenin induction in male Western fence lizards (Sceloporus occidentalis) exposed to ethinylestradiol. Environ Toxicol Chem 21:1410–1416

    Article  CAS  Google Scholar 

  • Bridges CM (1997) Tadpole swimming performance and activity affected by acute exposure to sublethal levels of carbaryl. Environ Toxicol Chem 16:1935–1939

    Article  CAS  Google Scholar 

  • Bridges CM (2000) Long-term effects of pesticide exposure at various life stages of the southern leopard frog (Rana sphenocephala). Arch Environ Contam Toxicol 39(1):91–96

    Article  CAS  Google Scholar 

  • Budak A, Gocmen B (2008) Herpetoloji, Ege Üniversitesi Yayınları Fen Fakültesi Yayın No.194, Bornova, İzmir, pp 226

  • Buono S, Cristiano L, D’Angelo B, Cimini A, Putti R (2007) PPARα mediates the effects of the pesticide methyl thiophanate on the liver of the lizard Podarcis sicula. Comp Biochem Physiol C 145:306–314

    CAS  Google Scholar 

  • Creasy DM (2001) Pathogenesis of male reproductive toxicity. Toxicol Pathol 29(1):64–76

    Article  CAS  Google Scholar 

  • Davidson C, Benard MF, Shaffer HB, Parker JM, O’leary C, Conlon JM, Rollins-Smith LA (2007) Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs. Environ Sci Technol 41:1771–1776

    Article  CAS  Google Scholar 

  • De Falco M, Sciarrillo R, Capaldo A, Russo T, Gay F, Valiante S, Varano L, Laforgia V (2007) The effects of the fungicide methyl thiophanate on adrenal gland morphophysiology of the lizard, Podarcis sicula. Arch Environ Contam Toxicol 53:241–248

    Article  CAS  Google Scholar 

  • Delen N, Durmusoglu E, Guncan A, Gungor N, Turgut C, Burcak A (2005) Turkey Agricultural Engineering 6. Technical Congress, pp 1–21

  • D'Souza UJA (2003) Tamoxifen induced multinucleated cells (symplasts) and distortion of seminiferous tubules in rat testis. Asian J Androl 5:217–220

    Google Scholar 

  • Dunnick JK, Gupta BN, Harris MW, Lamb JC (1984) Reproductive toxicity of dimethyl methylphosphate in the male fisher 344 rat. Toxicol Appl Pharmacol 72:379–387

    Article  CAS  Google Scholar 

  • DuRant SE, Hopkins WA, Talent LG (2007) Impaired terrestrial and arboreal locomotor performance in the western fence lizard (Sceloporus occidentalis) after exposure to an AChE-inhibiting pesticide. Environ Pollut 149:18–24

    Article  CAS  Google Scholar 

  • Dutta HM, Misquitta D, Khan S (2006) The effects of endosulfan on testes of Bluegill Fish, Lepomis macrochirus: A histopathological study. Arch Environ Contam Toxicol 51:149–156

    Article  CAS  Google Scholar 

  • EPA (2004) Carbaryl Interim Reregistration Eligibility Decision (IRED) Facts. EPA, Office of Pesticide Programs, pp 318

  • Ewing RD (1999) Diminishing returns: Salmon decline and pesticides. Funded by the Oregon Pesticide Education Network, Biotech Research and Consulting, Inc, Corvallis, OR, pp 55

  • Fair JM, Kennedy PL, McEwen LC (1995) Effects of carbaryl grasshopper control on nesting killdeer in North Dakota. Environ Toxicol Chem 14:881–890

    Article  CAS  Google Scholar 

  • Ghosh P, Bhattacharya S, Bhattacharya S (1990) Impairment of the regulation of gonadal function in Channa punctatus by metacid-50 and carbaryl under laboratory and field conditions. Biomed Environ Sci 3:106–112

    CAS  Google Scholar 

  • Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, Deja Vu amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  • Gibbs KE, Mingo TM, Courtmanch DL (1984) Persistence of carbaryl (Sevin-4-Oil) in woodland ponds and its effects on pond macroinvertebrates following forest spraying. Can Entomol 116:203–213

    Article  CAS  Google Scholar 

  • Gruber SJ, Munn MD (1998) Organophosphate and carbamate insecticides in agricultural waters and cholinesterase (Che) inhibition in common carp (Cyprinus carpio). Arch Environ Contam Toxicol 35:391–396

    Article  CAS  Google Scholar 

  • Gupta RC (2006) Endocrine disruption by organophosphate and carbamate pesticides: toxicology of organophosphate & carbamate Compounds. Elsevier, Amsterdam, p 489

    Google Scholar 

  • Hall RJ (1980) Effects of environmental contaminants on reptiles: a review. United States Department of the Interior, Fish and Wildlife Service, special scientific report—wildlife no. 228. Washington D.C., USA pp 12

  • Hess RA, Nakai M (2000) Histopathology of the male reproductive system induced by the fungicide benomyl. Histol Histopathol 15:207–224

    CAS  Google Scholar 

  • Hess RA, Moore BJ, Forrer J, Linder RE, Abuel-Atta AA (1991) The fungicide benomyl (Methyl1-(Butylcarbamoyl)-2-benzimidazolecarbamate) causes testicular dysfunction by inducing the sloughing of germ cells and occlusion of efferent ductules. Toxicol Sci 17(4):733–745

    Article  CAS  Google Scholar 

  • Holem RR, Hopkins WA, Talent LG (2006) Effect of acute exposure to malathion and lead on sprint performance of the western fence lizard (Sceloporus occidentalis). Arch Environ Contam Toxicol 51:111–116

    Article  CAS  Google Scholar 

  • Holem RR, Hopkins WA, Talent LG (2008) Effects of repeated exposure to malathion on growth, food consumption, and locomotor performance of the western fence lizard (Sceloporus occidentalis). Environ Pollut 152(1):92–98

    Article  CAS  Google Scholar 

  • Hopkins WA (2000) Reptile toxicology: challenges and opportunities on the last frontier in vertebrate ecotoxicology. Environ Toxicol Chem 19(10):2391–2393

    Article  CAS  Google Scholar 

  • Hopkins WA, Winne CT (2008) Influence of body size on swimming performance of four species of neonatal natricine snakes acutely exposed to an acetylcholinesterase-inhibiting pesticide. Environ Toxicol Chem 25:1208–1213

    Article  Google Scholar 

  • Hopkins WA, Winne CT, DuRant SE (2005) Differential swimming performance of two natricine snakes exposed to a cholinesterase-inhibiting pesticide. Environ Pollut 33:531–540

    Article  Google Scholar 

  • Kang HS, Park CJ, Gye MC (2010) Effect of carbaryl on survival and development in Bombina orientalis (Boulenger) embryos. Bull Environ Contam Toxicol 84:550–553

    Article  CAS  Google Scholar 

  • Khalaf KD, Morales-Rubio A, de la Guardia M (1993) Simple and rapid flow injection spectrophotometric determination of carbaryl after liquid-liquid extraction. Anal Chim Acta 280:231–238

    Article  CAS  Google Scholar 

  • Kulreshtha SK, Arora N (1984) Impairments induced by sublethal doses of 2 pesticides in the ovaries of a freshwater teleost Channa striatus. Toxic Lett (Shannon) 20:93–98

    Article  Google Scholar 

  • Liu D, Thomson K, Strachan WMJ (1981) Biodegradation of carbaryl in a simulated aquatic environment. Bull Environ Contam Toxicol 27:412–417

    Article  CAS  Google Scholar 

  • Matos P, Fontainhas-Fernandes A, Peixoto F, Carrola J, Rocha E (2007) Biochemical and histological hepatic changes of Nile tilapia Oreochromis niloticus exposed to carbaryl. Pesticide Biochem Physiol 89:73–80

    Article  CAS  Google Scholar 

  • McFarland CA, Quinn MJ Jr, Boyce J, Bazar MA, Talent LG, Johnson MS (2009) Toxic effects of oral hexahydro-1,3,5-triazine in the western fence lizard (Sceloporus occidentalis). Environ Toxicol Chem 28:1043–1050

    Article  CAS  Google Scholar 

  • McFarland CA, Quinn MJ Jr, Boyce J, LaFiandra EM, Bazar MA, Talent LG, Johnson MS (2011) Toxic effects of oral 2-amino-4,6-dinitrotoluene in the western fence lizard (Sceloporus occidentalis). Environ Pollut 159:466–473

    Article  CAS  Google Scholar 

  • Metts BS, Hopkins WA, Nestor JP (2005) Interaction of an insecticide with larval density in pond-breeding salamanders (Ambystoma). Freshwater Biol 50:685–696

    Article  CAS  Google Scholar 

  • Mora BR, Martinez-Tabche L, Sanchez-Hidalgo E, Hernandez GC, Ruiz MC, Murrieta FF (2000) Relationship between toxicokinetics of carbaryl and effect on acetylcholinesterase activity in Pomacea patula snail. Ecotoxicol Environ Saf 46(2):234–239

    Article  CAS  Google Scholar 

  • Nakai M, Hess RA (1994) Morphological changes in the rat sertoli cell induced by the microtubule poison carbendazim. Tissue Cell 26(6):917–927

    Article  CAS  Google Scholar 

  • Narayana K, Prashanthi N, Nayanatara A, Bairy LK, D’Souza JA (2006) An organophosphate inseticide methyl parathion (0-0-dimethyl 0-4-nitrophenyl phosphorothiote) induces cytotoxic damage and tubular atrophy in the testis despite elevated testosterone level in the rat. J Toxicol Sci 31(3):177–189

    Article  CAS  Google Scholar 

  • Ozelmas U, Akay MT (1995) Histopathological investigations of the effects of malathion on dwarf lizards (Lacerta parva Boulenger 1887). Bull Environ Contam Toxicol 55:730–737

    Article  CAS  Google Scholar 

  • Pant N, Prasad AK, Srivastava SC, Shankar R, Srivastava SP (1995) Effect of oral administration of carbofuran on male reproductive system of rat. Hum Exp Toxicol 14(11):889–894

    Article  CAS  Google Scholar 

  • Pant N, Shankar R, Srivastava SP (1996) Spermatotoxic effects of carbaryl in rats. Hum Exp Toxicol 15:736–738

    Article  CAS  Google Scholar 

  • Relyea RA (2003) Predator cues and pesticides: a double dose of danger for amphibians. Ecol Appl 13:1515–1521

    Article  Google Scholar 

  • Relyea RA (2005) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15:618–627

    Article  Google Scholar 

  • Relyea RA, Mills N (2001) Predator-induced stress makes the pesticide carbaryl more deadly to grey treefrog tadpoles (Hyla versicolor). Proc Nat Acad Sci USA 98:2491–2496

    Article  CAS  Google Scholar 

  • Ribera D, Narbonne JF, Saint-Denis M (2001) Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil: effects of carbaryl. Soil Biol Biochem 33:1123–1130

    Article  CAS  Google Scholar 

  • Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy TM, Niedzwiecki JH, Sager T, Sih A, Palmer BD (2003) Lethal and sublethal effects of atrazine, carbaryl, endosulfan, and octylphenol on the streamside salamander (Ambystoma barbouri). Environ Toxicol Chem 22(10):2385–2392

    Article  CAS  Google Scholar 

  • Sarkar R, Mohanakumar KP, Chowdhury M (2000) Effects of an organophosphate pesticide, quinalphos, on the hypothalamo–pituitary-gonadal axis in adult male rats. J Reprod Fertil 118:29–38

    Article  CAS  Google Scholar 

  • Sayim F (2007) Histopathological effects of dimethoate on testes of rats. Bull Environ Contam Toxicol 78:479–484

    Article  CAS  Google Scholar 

  • Sciarrillo R, De Falco M, Virgilio F, Laforgia V, Capaldo A, Gay F, Valiante S, Varano L (2008) Morphological and functional changes in the thyroid gland of methyl thiophanate-injected lizards, Podarcis sicula. Arch Environ Contam Toxicol 55:254–261

    Article  CAS  Google Scholar 

  • Shimada H, Narumi R, Nagano M, Yasutake A, Waalkes MP, Imamura Y (2009) Strain difference of cadmium-induced testicular toxicity in inbred Wistar-Imamichi and Fischer 344 rats. Arch Toxicol 83:647–652

    Article  CAS  Google Scholar 

  • Suski JG, Salice C, Houpt JT, Bazar MA, Talent LG (2008) Dose-related effects following oral exposure of 2,4-dinitrotoluene on the western fence lizard, Sceloporus occidentalis. Environ Toxicol Chem 27:352–359

    Article  CAS  Google Scholar 

  • Timbrell J (2002) Pesticides: Introduction to Toxicology, 3rd edn. Taylor and Francis, New York, pp 109–110

    Google Scholar 

  • Toppari J, Larsen JC, Christiansen P, Giwercman A, Grandjean P, Guillette LJ Jr, Jegou B, Jensen TK, Jouannet P, Keiding N et al (1996) Male reproductive health and environmental xenoestrogens. Environ Health Perspect 104(Suppl 4):741–803

    Article  CAS  Google Scholar 

  • Ware GW (1994) The pesticide book, 4th edn. Thomson, Fresno, p 386

    Google Scholar 

  • Watts P, Wilkinson GR (1977) The interaction of carbamates with acetylcholinesterase. Biochem Pharmacol 26:757–761

    Article  CAS  Google Scholar 

  • Wilson GD, d’Arcy Doherty M, Cohen GM (1985) Selective toxicity of 1-naphthol to human colorectal tumour tissue. Br J Cancer 51:853–863

    Article  CAS  Google Scholar 

  • Wyrobek AJ, Watchmaker G, Gordon L, Wong K, Moore D II, Whorton D (1981) Sperm shape abnormalities in carbaryl-exposed employees. Environ Health Perspect 40:255–265

    Article  CAS  Google Scholar 

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  1. Science Faculty, Biology Department, Zoology Section 35100, Ege University, Bornova-Izmir, Turkey

    Ozlem Cakici & Esra Akat

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  1. Ozlem Cakici
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  2. Esra Akat
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Cakici, O., Akat, E. Histopathological effects of carbaryl on testes of snake-eyed lizard, Ophisops elegans . Environ Sci Pollut Res 19, 64–71 (2012). https://doi.org/10.1007/s11356-011-0541-1

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