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Imidacloprid induces morphological and molecular damages on testis of lizard (Podarcis sicula)

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Abstract

The insecticide imidacloprid was evaluated under laboratory conditions in the adult male Italian wall lizards (Podarcis sicula) to assess its potential toxicity. By an acute oral test, LD50 was 503.76 mg/kg. Changes in spermatogenesis, plasma sex hormone levels and androgen and oestrogen receptor mRNAs were analysed by subchronic test and simulated environmental exposure. 15-days subchronic test, in which lizards were orally dosed on alternate days at 0, 10, 50, 100 mg/kg bw, showed a dose-dependent changes of testicular architecture and an increase of apoptotic processes. In a 30-days simulated environmental exposure spermatogenesis was arrested at secondary spermatocyte level and only few primary spermatocytes were TUNEL-positive. In all experimental groups imidacloprid was able to decrease both the level of sex hormones and the steroid receptor mRNAs. The results demonstrate that imidacloprid affects reproduction function of male lizards therefore precautions must be taken to minimize the harmful effects of this compound.

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References

  • Abou-Donia MB, Goldstein LB, Bullman S, Tu T, Khan WA, Dechkovskaia AM, Abdel-Rahman AA (2008) Imidacloprid induces neurobehavioral deficits and increases expression of glial fibrillary acidic protein in the motor cortex and hippocampus in offspring rats following in utero exposure. J Toxicol Environ Health A 71(2):119–130

    Article  CAS  Google Scholar 

  • Amaral MJ, Carretero MA, Bicho RC, Soares AM, Mann RM (2012a) The use of a lacertid lizard as a model for reptile ecotoxicology studies–part 1 field demographics and morphology. Chemosphere 87(7):757–764

    Article  CAS  Google Scholar 

  • Amaral MJ, Bicho RC, Carretero MA, Sanchez-Hernandez JC, Faustino AM, Soares AM, Mann RM (2012b) The use of a lacertid lizard as a model for reptile ecotoxicology studies: part 2–biomarkers of exposure and toxicity among pesticide exposed lizards. Chemosphere 87(7):765–774

    Article  CAS  Google Scholar 

  • Andò S, Panno ML, Ciarcia G, Imbrogno E, Buffone M, Beraldi E, Scisci D, Angelini F, Botte V (1990) Plasma sex hormone concentration during the reproductive cycle in the male lizard Podarcis s sicula. J Reprod Fertil 90:353–360

    Article  Google Scholar 

  • Angelini F, Botte V (1992) Spermatogenesis in reptiles, dynamic and regulatory aspect. In: Dallai R (ed) Sex origin and evolution. Mucchi Selected Symposia and Monographs UZI, Modena, pp 211–230

    Google Scholar 

  • Bal R, Naziroğlu M, Türk G, Yilmaz Ö, Kuloğlu T, Etem E, Baydas G (2012a) Insecticide imidacloprid induces morphological and DNA damage through oxidative toxicity on the reproductive organs of developing male rats. Cell Biochem Funct 30(6):492–499

    Article  CAS  Google Scholar 

  • Bal R, Türk G, Tuzcu M, Yilmaz O, Kuloglu T, Gundogdu R, Gür S, Agca A, Ulas M, Cambay Z, Tuzcu Z, Gencoglu H, Guvenc M, Ozsahin AD, Kocaman N, Aslan A, Etem E (2012b) Assessment of imidacloprid toxicity on reproductive organ system of adult male rats. J Environ Sci Health B 47(5):434–444

    Article  CAS  Google Scholar 

  • Balani T, Agrawal S, Thaker AM (2011) Hematological and biochemical changes due to short-term oral administration of imidacloprid. Toxicol Int 18:2–4

    Article  Google Scholar 

  • Bicho RC, Amaral MJ, Faustino AM, Power DM, Rêma A, Carretero MA, Soares AM, Mann RM (2013) Thyroid disruption in the lizard Podarcis bocagei exposed to a mixture of herbicides: a field study. Ecotoxicol 22(1):156–165

    Article  CAS  Google Scholar 

  • Bretveld R, Brouwers M, Ebisch I, Roeleveld N (2007) Influence of pesticides on male fertility. Scand J Work Environ Health 33(1):13–28

    Article  CAS  Google Scholar 

  • Bro E, Decors A, Millot F, Soyez D, Moinet M, Berny P, Mastain O (2010) Intoxications des perdrix grises en nature. Nouveau bilan de la surveillance « SAGIR». Faune Sauvage 289:26–32

    Google Scholar 

  • Capula M, Aloise G (2011) Extreme feeding behaviours in the Italian wall lizard, Podarcis siculus. Acta Herpet 6(1):11–14

    Google Scholar 

  • Cardone A (2012) Testicular toxicity of methyl thiophanate in the Italian wall lizard (Podarcis sicula): morphological and molecular evaluation. Ecotoxicol 21:512–523

    Article  CAS  Google Scholar 

  • Cardone A, Angelini F, Varriale B (1998) Autoregulation of estrogen and androgen receptor mRNAs and down regulation of androgen receptor mRNA by estrogen in primary cultures of lizard testis cells. Gen Comp Endocrinol 110:227–236

    Article  CAS  Google Scholar 

  • Cardone A, Comitato R, Bellini L, Angelini F (2002) Effects of the aromatase inhibitor fadrozole on plasma sex steroid secretion and spermatogenesis, and epididymis morphology in the lizard, Podarcis sicula. Mol Reprod Dev 63:63–70

  • Carreau S, Bouraima-Lelong H, Delalande C (2012) Estrogen, a female hormone involved in spermatogenesis. Adv Med Sc. 57(1):31–36

    Article  CAS  Google Scholar 

  • Carretero MA (2004) From set menu to a la carte. Linking issues in trophic ecology of Mediterranean lacertids. Ital J Zool 2:121–133

    Article  Google Scholar 

  • Chao SL, Casida JE (1997) Interaction of imidacloprid metabolites and analogues with the nicotinic acetylcholine receptor of mouse brain in relation to toxicity. Pest Biochem Physiol 58:77–88

    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 

  • de Snoo GR, Scheidegger NMI, de Jong FMW (1999) Vertebrate wildlife incidents with pesticides: a European survey. Pestic Sci 55:47–54

    Article  Google Scholar 

  • Frigato E, Vallone D, Bertolucci C, Foulkes NS (2006) Isolation and characterization of melanopsin and pinopsin expression within photoreceptive sites of reptiles. Naturwissenschaften 93(8):379–385

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Holdcraft RW, Braun RE (2004) Hormonal regulation of spermatogenesis. Int J Androl 27(6):335–342

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kapoor U, Srivastava MK, Srivastava LP (2011) Toxicological impact of technical imidacloprid on ovarian morphology hormones and antioxidant enzymes in female rats. Food Chem Toxicol 49:3086–3089

    Article  CAS  Google Scholar 

  • Latli B, D’Amour K, Casida JE (1999) Novel and potent 6-chloro-3-pyridinyl ligands for the α4β2 neuronal nicotinic acetylcholine receptor. J Med Chem 42:2227–2234

    Article  CAS  Google Scholar 

  • Maclean JA II, Wilkinson MF (2005) Gene regulation in spermatogenesis. Curr Top Dev Biol 71:131–197

    Article  CAS  Google Scholar 

  • Mathur PP, Huang L, Kashou A, Vaithinathan S, Agarwal A (2011) Environmental toxicants and testicular apoptosis. Open Reprod Sc. J 3:114–124

    Article  CAS  Google Scholar 

  • Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22(11):573–580

    Article  CAS  Google Scholar 

  • Matthews J, Zacharewski T (2000) Differential binding affinities of PCBs, HO-PCBs, and aroclors with recombinant human, rainbow trout (Onchorhynkiss mykiss), and green anole (Anolis carolinensis) estrogen receptors, using a semi-high throughput competitive binding assay. Toxicol Sci 53(2):326–339

    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 

  • Mencke N, Jeschke P (2002) Therapy and prevention of parasitic insects in veterinary medicine using imidacloprid. Curr Top Med Chem 2:701–715

    Article  CAS  Google Scholar 

  • Najafi GR, Razi M, Hoshyar A, Shahmohamadloo S, Feyzi S (2010) The effect of chronic exposure with imidacloprid insecticide on fertility in mature male rats. Inter J Steril Fertil 4:9–16

    Google Scholar 

  • Pauli BD, Money S, Sparling DW (2010) Ecotoxicology of pesticides in reptiles. In: Sparling DW, Linder G, Bishop CA, Krest S (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. CRC Press, Boca Raton, pp 203–224

    Chapter  Google Scholar 

  • Rich CN, Talent LG (2009) Soil ingestion may be an important route for the uptake of contaminants by some reptiles. Environ Toxicol Chem 28:311–315

    Article  CAS  Google Scholar 

  • Rosen G, O’Bryant E, Matthews J, Zacharewski T, Wade J (2002) Distribution of androgen receptor mRNA expression and immunoreactivity in the brain of the green anole lizard. J Neuroendocrinol 14(1):19–28

    Article  CAS  Google Scholar 

  • Rouchaud J, Gustin F, Wauters A (1994) Soil biodegradation and leaf transfer of insecticide imidacloprid applied in seed dressing in sugar beet crops. Bull Environ Contam Toxicol 53:344–350

    Article  CAS  Google Scholar 

  • Saradha PP, Mathur B (2006) Effect of environmental contaminants on male reproduction. Environ Toxicol Pharmacol 21:34–41

    Article  CAS  Google Scholar 

  • Schirmer SU, Eckhardt I, Lau H, Klein J, DeGraaf YC, Lips KS, Pineau C, Gibbins IL, Kummer W, Meinhardt A, Haberberger RV (2011) The cholinergic system in rat testis is of non-neuronal origin. Reproduction 142(1):157–166

    Article  CAS  Google Scholar 

  • Siddiqui A, Choudhary M, Goriya HV, Bhavsar SK, Thaker AM (2007) Evaluation of immunotoxic effect of short-term administration of quinalphos and imidacloprid in white leghorn cockerels. Toxicol Int 14:15–19

    CAS  Google Scholar 

  • Sparling DW, Linder G, Bishop CA, Krest SK (2010) Recent advancements in amphibian and reptile ecotoxicology. In: Sparling DW, Linder G, Bishop CA, Krest S (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. CRC Press, Boca Raton, pp 1–14

    Chapter  Google Scholar 

  • Sumida K, Ooe N, Saito K, Kaneko H (2001) Molecular cloning and characterization of reptilian estrogen receptor cDNAs. Mol Cell Endocrinol 183(1–2):33–39

    Article  CAS  Google Scholar 

  • Tabb MM, Blumberg B (2006) New modes of action for endocrine-disrupting chemicals. Mol Endocrinol 20(3):475–482

    Article  CAS  Google Scholar 

  • Todd BD, Wilson JD, Gibbons JW (2010) The global status of reptiles and causes of their decline. In: Sparling DW, Linder G, Bishop CA, Krest S (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. CRC Press, Boca Raton, pp 69–104

    Google Scholar 

  • Tomizawa M (2004) Neonicotinoids and derivatives: effects in mammalian cells and mice. J Pestic Sci 29(3):177–183

    Article  CAS  Google Scholar 

  • Tomizawa M, Casida JE (2000) Imidacloprid, thiacloprid, and their imine derivatives up-regulate the α4β2 nicotinic acetylcholine receptor in M10 cells. Toxicol App Pharmacol 169:114–120

    Article  CAS  Google Scholar 

  • Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–268

    Article  CAS  Google Scholar 

  • Tomlin C (2009) The pesticide manual: a world compendium, 15th edn. British Crop Protection Council, London

    Google Scholar 

  • TSK (Trimmed Spearman-Karber) program, (1991) Environmental Monitoring Systems Laboratory, US Environmental Protection Agency, Cincinnati, OH 45268, USA

  • Weir SM, Suski JG, Salice CJ (2010) Ecological risk of anthropogenic pollutants to reptiles: evaluating assumptions of sensitivity and exposure. Environ Pollut 158:3596–3606

    Article  CAS  Google Scholar 

  • Yeh IJ, Lin TJ, Hwang DY (2010) Acute multiple organ failure with imidacloprid and alcohol ingestion. Am J Emerg Med 28(255):e1–e3

    Google Scholar 

  • Young LJ, Godwin J, Grammer M, Gahr M, Crews D (1995) Reptilian sex steroid receptors: amplification, sequence and expression analysis. J Steroid Biochem Mol Biol 55(2):261–269

    Article  CAS  Google Scholar 

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Acknowledgments

The author wish to thank Mr. Mark Walters for linguistic revision. This work was supported by intramural funds of Biology Department to A.C.

Conflict of interest

The author declare they have no competing interests, be it financial, personal or professional.

Ethical standards

All animals were captured with the authorization of 06/01/2000 No. SCN/2D/2000/9213 of the Italian Ministry of the Environment. The experiments were carried out in compliance with the ethical provisions enforced by the European Union and authorized by the National Committee of the Italian Ministry of Health on in vivo experimentation ( Dept. for Veterinary Public Health, Nutrition and Food Safety). All efforts were made to avoid animal suffering and to minimize the number of specimens used. The animals were maintained in accordance with the institutional guidelines for care and use of laboratory animals.

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  1. Laboratory of Endocrinology, Department of Biology, University of Naples Federico II, Via Mezzocannone, 8, 80134, Naples, Italy

    Anna Cardone

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  1. Anna Cardone
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Correspondence to Anna Cardone.

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This paper is dedicated to the memory of Giuseppe Falcone, an unforgettable friend who died prematurely, in recognition of his devotion to the pursuit of perfection in photography and digital art-work.

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Cardone, A. Imidacloprid induces morphological and molecular damages on testis of lizard (Podarcis sicula). Ecotoxicology 24, 94–105 (2015). https://doi.org/10.1007/s10646-014-1361-0

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