In vitro effects of imidacloprid on honey bee sperm: evaluation using computer-aided sperm analysis (CASA)

References

• Aitken, R. J., Gibb, Z., Baker, M. A., Drevet, J., & Gharagozloo, P. (2016). Causes and consequences of oxidative stress in spermatozoa. Reproduction, Fertility, and Development, 28(1-2), 1–10. https://doi.org/10.1071/rd15325
   PubMed Web of Science ®Google Scholar
• Balieira, K. V. B., Mazzo, M., Bizerra, P. F. V., Guimarães, A. R., de, J. S., Nicodemo, D., & Mingatto, F. E. (2018). Imidacloprid-induced oxidative stress in honey bees and the antioxidant action of caffeine. Apidologie, 49(5), 562–572. https://doi.org/10.1007/s13592-018-0583-1
   Web of Science ®Google Scholar
• Baylay, A. J., Spurgeon, D. J., Svendsen, C., Griffin, J. L., Swain, S. C., Sturzenbaum, S. R., & Jones, O. A. H. (2012). A metabolomics based test of independent action and concentration addition using the earthworm Lumbricus rubellus. Ecotoxicology (London, England), 21(5), 1436–1447. https://doi.org/10.1007/s10646-012-0897-0
   PubMed Web of Science ®Google Scholar
• Ben Abdelkader, F., Kairo, G., Tchamitchian, S., Cousin, M., Senechal, J., Crauser, D., Vermandere, J. P., Alaux, C., Conte, Y. L., Belzunces, L. P., Barbouche, N., & Brunet, J.-L (2013). Semen quality of honey bee drones maintained from emergence to sexual maturity under laboratory, semi-field and field conditions. Apidologie, 45(2), 215–223. https://doi.org/10.1007/s13592-013-0240-7
   Web of Science ®Google Scholar
• Ben Abdelkader, F., & Barbouche, N. (2015). Effects of some insecticides on the viability and the ATP synthesis of honeybee drone’s spermatozoid in vitro exposed. Tunisian Journal of Plant Protection, 10(1), 79–93.
   Google Scholar
• Brittain, C. A., Vighi, M., Bommarco, R., Settele, J., & Potts, S. G. (2010). Impacts of a pesticide on pollinator species richness at different spatial scales. Basic and Applied Ecology, 11(2), 106–115. https://doi.org/10.1016/j.baae.2009.11.007
   Web of Science ®Google Scholar
• Buckingham, S., Lapied, B., Corronc, H., & Sattelle, F. S. (1997). Imidacloprid actions on insect neuronal acetylcholine receptors. The Journal of Experimental Biology, 200(Pt 21), 2685–2692.
   PubMed Web of Science ®Google Scholar
• Chaimanee, V., Evans, J. D., Chen, Y., Jackson, C., & Pettis, J. S. (2016). Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos. Journal of Insect Physiology, 89, 1–8. https://doi.org/10.1016/j.jinsphys.2016.03.004
   PubMed Web of Science ®Google Scholar
• Chakrabarti, P., Rana, S., Sarkar, S., Smith, B., & Basu, P. (2015). Pesticide-induced oxidative stress in laboratory and field populations of native honey bees along intensive agricultural landscapes in two Eastern Indian states. Apidologie, 46(1), 107–129. https://doi.org/10.1007/s13592-014-0308-z
   Web of Science ®Google Scholar
• Ciereszko, A., Wilde, J., Dietrich, G. J., Siuda, M., Bąk, B., Judycka, S., & Karol, H. (2017). Sperm parameters of honeybee drones exposed to imidacloprid. Apidologie, 48(2), 211–222. https://doi.org/10.1007/s13592-016-0466-2
   Web of Science ®Google Scholar
• Costa, E. M., Araujo, E. L., Maia, A. V. P., Silva, F. E. L., Bezerra, C. E. S., & Silva, G. J. (2014). Toxicity of insecticides used in the Brazilianmelon crop to the honey bee Apis mellifera under laboratory conditions. Apidologie, 45(1), 34–44. https://doi.org/10.1007/s13592-013-0226-5
   Web of Science ®Google Scholar
• Decourtye, A., Devillers, J., Cluzeau, S., Charreton, M., & Pham-Delègue, M. H. (2004). Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicology and Environmental Safety, 57(3), 410–419. https://doi.org/10.1016/j.ecoenv.2003.08.001
   PubMed Web of Science ®Google Scholar
• Di Prisco, G., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F., Gargiulo, G., & Pennacchio, F. (2013). Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences of the United States of America, 110(46), 18466–18471. https://doi.org/10.1073/pnas.1314923110
   PubMed Web of Science ®Google Scholar
• Duty, S. M., Calafat, A. M., Silva, M. J., Brock, J. W., Ryan, L., Chen, Z., Overstreet, J., & Hauser, R. (2004). The relationship between environmental exposure to phthalates and computer-aided sperm analysis motion parameters. Journal of Andrology, 25(2), 293–302. https://doi.org/10.1002/j.1939-4640.2004.tb02790.x
   PubMedGoogle Scholar
• Elbert, A., Becker, B., Hartwig, J., & Erdelen, C. (1991). Imidacloprid – A new systemic insecticide. Pflanzenschutz- Nachrichten Bayer, 44(2), 113–136.
   Google Scholar
• Elbert, A., Haas, M., Springer, B., Thielert, W., & Nauen, R. (2008). Applied aspects of neonicotinoid uses in crop protection. Pest Management Science, 64(11), 1099–1105. https://doi.org/10.1002/ps.1616
   PubMed Web of Science ®Google Scholar
• Faucon, J.-P., Aurières, C., Drajnudel, P., Mathieu, L., Ribière, M., Martel, A.-C., Zeggane, S., Chauzat, M.-P., & Aubert, M. F. A. (2005). Experimental study on the toxicity of imidacloprid given in syrup to honey bee (Apis mellifera) colonies. Pest Management Science, 61(2), 111–125. https://doi.org/10.1002/ps.957
   PubMed Web of Science ®Google Scholar
• Frazer, L., Holoday, D., & Srezezek, J. (1999). Use of computer assisted semen analysis (CASA). System to determine changes in motion characteristics in boar spermatozoa. Polish Journal of Veterinary Sciences, 2(3), 103–107.
   Google Scholar
• Gavella, M., Lipovac, V., Vučić, M., & Ročić, B. (2009). Relationship of sperm superoxide dismutase-like activity with other sperm-specific enzymes and experimentally induced lipid peroxidation in infertile men. Andrologia, 28(4), 223–229. https://doi.org/10.1111/j.1439-0272.1996.tb02787.x
   Google Scholar
• Henderson, C., Tarver, L., Plummer, D., Seccomb, R., Debnam, S., Rice, S., Bromenshenk, J., & Glassy, J. (2007). U.S. national bee colony loss survey www.beesurvey.com preliminary findings with respect to colony collapse disorder (CCD). American Bee Journal, 147(5), 381–384.
   Google Scholar
• Iguer-Ouada, M., & Verstegen, J. P. (2001). Evaluation of the Hamilton Thorn computer-based automated system for dog semen analysis. Theriogenology, 55(3), 733–749. https://doi.org/10.1016/S0093-691X(01)00440-X
   PubMed Web of Science ®Google Scholar
• İnanç, M. E., Çil, B., Tekin, K., Alemdar, H., & Daşkin, A. (2018). The combination of CASA kinetic parameters and fluorescein staining as a fertility tool in cryopreserved bull semen. Turkish Journal of Veterinary and Animal Sciences, 42(5), 452–458. https://doi.org/10.3906/vet-1801-83
   Web of Science ®Google Scholar
• Jones, R., Mann, T., & Sherins, R. (1979). Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertility and Sterility, 31(5), 531–537. https://doi.org/10.1016/S0015-0282(16)43999-3
   PubMed Web of Science ®Google Scholar
• Kairo, G., Provost, B., Tchamitchian, S., Ben Abdelkader, F., Bonnet, M., Cousin, M., Sénéchal, J., Benet, P., Kretzschmar, A., Belzunces, L. P., & Brunet, J.-L. (2016). Drone exposure to the systemic insecticide Fipronil indirectly impairs queen reproductive potential. Scientific Reports, 6(1), 31904. https://doi.org/10.1038/srep31904
   PubMedGoogle Scholar
• Klimowicz, M. D., Nizanski, W., Batkowski, F., & Savic, M. A. (2008). The comparison of assessment of pigeon semen motility and sperm concentration by conventional methods and the CASA system (HTM IVOS). Theriogenology, 70(1), 77–82. https://doi.org/10.1016/j.theriogenology.2008.02.006
   PubMed Web of Science ®Google Scholar
• Lambin, M., Armengaud, C., Raymond, S., & Gauthier, M. (2001). Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. Archives of Insect Biochemistry and Physiology, 48(3), 129–134. https://doi.org/10.1002/arch.1065
   PubMed Web of Science ®Google Scholar
• Locke, S. J., & Peng, Y. S. (1993). The effects of drone age, semen storage and contamination on semen quality in the honey bee (Apis mellifera). Physiological Entomology, 18(2), 144–148. https://doi.org/10.1111/j.1365-3032.1993.tb00461.x
   Web of Science ®Google Scholar
• Mani, U., Islam, F., Prasad, A. K., Kumar, P., Kumar, V. S., Maji, B. K., & Dutta, K. K. (2002). Steroidogenic alterations in testes and sera of rats exposed to formulated Fenvalerate by inhalation. Human & Experimental Toxicology, 21(11), 593–597. https://doi.org/10.1191/0960327102ht298oa
   PubMed Web of Science ®Google Scholar
• Matsuda, K., Buckingham, S. D., Kleier, D., Rauh, J. J., Grauso, M., & Sattelle, D. B. (2001). Neonicotinoids: Insecticides acting on insect nicotinic acetylcholine receptors. Trends in Pharmacological Sciences, 22(11), 573–580. https://doi.org/10.1016/S0165-6147(00)01820-4
   PubMed Web of Science ®Google Scholar
• Matsuda, K., Shimomura, M., Ihara, M., Akamatsu, M., & Sattelle, D. B. (2005). Neonicotinoids show selective and diverse actions on their nicotinic receptor targets: Electrophysiology, molecular biology, and receptor modeling studies. Bioscience, Biotechnology, and Biochemistry, 69(8), 1442–1452. https://doi.org/10.1271/bbb.69.1442
   PubMed Web of Science ®Google Scholar
• Medrzycki, P., Montanari, R., Bortolotti, L., SabatinI, A. G., Maini, S., & Porrin, C. (2003). Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests. Bulletin of Insectology, 56(1), 59–62.
   Google Scholar
• Mengoni Goñalons, C., & Farina, W. M. (2015). Effects of sublethal doses of imidacloprid on young adult honeybee behaviour. PLoS One, 10(10), e0140814. https://doi.org/10.1371/journal.pone.0140814
   PubMed Web of Science ®Google Scholar
• Methorst, C., & Huyghe, E. (2014). Stress oxydant et infertilité masculine: Physiopathologie et intérêt thérapeutique des antioxydants. Progres en Urologie, 24(suppl 3), 4–10. doi: PUROL-09-2014-24-HS3-1166-7087-101019-201400269
   Google Scholar
• Mommaerts, V., Reynders, S., Boulet, J., Besard, L., Sterk, G., & Smagghe, G. (2010). Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology (London, England), 19(1), 207–215. https://doi.org/10.1007/s10646-009-0406-2
   PubMed Web of Science ®Google Scholar
• Mortimer, D. (1997). Role of laboratory testing in diagnosis and management. In V. Gomel & P. C. K. Leung (Eds.), In vitro fertilization and assisted reproduction (pp. 489–495). Monduzzi Editori.
   Google Scholar
• Mortimer, S. T. (2000). CASA-practical aspects. Journal of Andrology, 21(4), 515–524. https://doi.org/ https://doi.org/10.1002/j.1939-4640.2000.tb02116.x
   PubMedGoogle Scholar
• Mullin, C. A., Frazier, M., Frazier, J. L., Ashcraft, S., Simonds, R., vanEngelsdorp, D., & Pettis, J. S. (2010). High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health. PLoS One, 5(3), e9754. https://doi.org/10.1371/journal.pone.0009754
   Google Scholar
• Nahar, N., & Ohtani, T. (2015). Imidacloprid and Fipronil induced abnormal behavior and disturbed homing of forager honey bees Apis mellifera. Journal of Entomology and Zoology Studies, 3(2), 65–72.
   Google Scholar
• Pati, P. C., & Bhunya, S. P. (1989). Cytogenetic effects of fenvalerate in mammalian in vivo test system. Mutation Research/Genetic Toxicology, 222(3), 149–154. https://doi.org/10.1016/0165-1218(89)90130-4
   PubMedGoogle Scholar
• Phiancharoen, M., Wongsiri, S., Koeniger, N., & Koeniger, G. (2004). Instrumental insemination of Apis mellifera queens with hetero- and conspecific spermatozoa results in different sperm survival. Apidologie, 35(5), 503–129. https://doi.org/10.1051/apido:2004043
   Web of Science ®Google Scholar
• Qiao, D., Seidler, F. J., & Slotkin, T. A. (2005). Oxidative mechanisms contributing to the developmental neurotoxicity of nicotine and chlorpyrifos. Toxicology and Applied Pharmacology, 206(1), 17–26. https://doi.org/10.1016/j.taap.2004.11.003
   PubMed Web of Science ®Google Scholar
• Ramazzini, C. (2009). Collegium Ramazzini statement on the control of pesticides in the European Union: A call for action to protect human health. American Journal of Industrial Medicine, 52(2), 176–177. https://doi.org/10.1002/ajim.20654
   PubMed Web of Science ®Google Scholar
• Ramirez-Romero, R., Chaufaux, J., & Pham-Delègue, M. H. (2005). Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie, 36(4), 601–611. https://doi.org/10.1051/apido:2005039
   Web of Science ®Google Scholar
• Ruiz-Pesini, E., Diez, C., Lapeña, A. C., Pérez-Martos, A., Montoya, J., Alvarez, E., Arenas, J., & López-Pérez, M. (1998). Correlation of sperm motility with mitochondrial enzymatic enzymatic activities. Clinical Chemistry, 44(8 Pt 1), 1616–1620. https://doi.org/10.1093/clinchem/44.8.1616
   PubMed Web of Science ®Google Scholar
• Schettgen, T., Koch, H. M., Drexler, H., & Angerer, J. (2002). New gas chromatographic-mass spectrometric method for the determination of urinary pyrethroid metabolites in environmental medicine. Journal of Chromatography B Analytical Technologies in the Biomedical and Life Sciences, 778(1-2), 121–130. https://doi.org/10.1016/S0378-4347(01)00452-2
   PubMed Web of Science ®Google Scholar
• Simon-Delso, N., Amaral-Rogers, V., Belzunces, L. P., Bonmatin, J. M., Chagnon, M., Downs, C., Furlan, L., Gibbons, D. W., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D. P., Krupke, C. H., Liess, M., Long, E., McField, M., Mineau, P., Mitchell, E. A. D., Morrissey, C. A., … Wiemers, M. (2015). Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environmental Science and Pollution Research International, 22(1), 5–34. https://doi.org/10.1007/s11356-014-3470-y
   PubMed Web of Science ®Google Scholar
• Straub, L., Villamar-Bouza, L., Bruckner, S., Chantawannakul, P., Gauthier, L., Khongphinitbunjong, K., Retschnig, G., Troxler, A., Vidondo, B., Neumann, P., & Williams, G. R. (2016). Neonicotinoid insecticides can serve as inadvertent insect contraceptives. Proceedings of the Royal Society B: Biological Sciences, 283(1835), 20160506. https://doi.org/10.1098/rspb.2016.0506
   PubMed Web of Science ®Google Scholar
• Sur, R., & Stork, A. (2003). Uptake, translocation and metabolism of imidacloprid in plants. Bulletin of Insectology, 56(1), 35–40. https://doi.org/10.1.1.571.5098
   Google Scholar
• Tan, K., Chen, W., Dong, S., Liu, X., Wang, Y., & Nieh, J. C. (2014). Imidacloprid alters foraging and decreases bee avoidance of predators. PLoS One, 9(7), e102725. https://doi.org/10.1371/journal.pone.0102725
   PubMed Web of Science ®Google Scholar
• Thany, S. H. (2010). Neonicotinoid insecticides: Historical evaluation and resistance mechanisms. Advances in Experimental Medicine and Biology, 683, 75–83.
   PubMed Web of Science ®Google Scholar
• Tomizawa, M., & Yamamoto, I. (1992). Binding of nicotinoids and the related compounds to the insect nicotinic acetyicholine receptor. Journal of Pesticide Science, 17(4), 231–236. https://doi.org/10.1584/jpestics.17.4_231
   Web of Science ®Google Scholar
• Tomlin, C. D. S. (Ed.) (1997). World compendium: The pesticide manual, incorporating the agrochemicals handbook (11th ed., pp. 1437–1439). British Crop Protection Council.
   Google Scholar
• Van Dame, R., Meled, M., Colin, M. E., & Belzunces, L. P. (1995). Alteration of the homing-flight in the honey bee Apis mellifera L. exposed to sublethal dose of deltamethrin. Environmental Toxicology and Chemistry, 14(5), 855–860. https://doi.org/10.1002/etc.5620140517
   Web of Science ®Google Scholar
• Wegener, J., May, T., Knollmann, U., Kamp, G., Müller, K., & Bienefeld, K. (2012). In vivo validation of in vitro quality tests for cryopreserved honey bee semen. Cryobiology, 65(2), 126–131. https://doi.org/10.1016/j.cryobiol.2012.04.010
   PubMed Web of Science ®Google Scholar
• Williams, G. R., Troxler, A., Retschnig, G., Roth, K., Yañez, O., Shutler, D., Neumann, P., & Gauthier, L. (2015). Neonicotinoid pesticides severely affect honey bee queens. Scientific Reports, 5, 14621. https://doi.org/10.1038/srep14621
   PubMed Web of Science ®Google Scholar
• Williamson, S. M., Baker, D. D., & Wright, G. A. (2013). Acute exposure to a sublethal dose of imidacloprid and coumaphos enhances olfactory learning and memory in the honeybee Apis mellifera. Invertebrate Neuroscience, 13(1), 63–70. https://doi.org/10.1007/s10158-012-0144-7
   PubMed Web of Science ®Google Scholar
• Williamson, S. M., Willis, S. J., & Wright, G. A. (2014). Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology (London, England), 23(8), 1409–1418. https://doi.org/10.1007/s10646-014-1283-x
   PubMed Web of Science ®Google Scholar
• Wu, Y. Y., Zhou, T., Wubie, A. J., Wang, Q., Dai, P. L., & Jia, H. R. (2014). Apoptosis in the nerve cells of adult honeybee (Apis mellifera ligustica) brain induced by imidacloprid. Acta Entomologica Sinica, 57, 194–203.
   Google Scholar
• Zenzes, M., & Bielecki, R. (2004). Nicotine-induced disturbances of meiotic maturation in cultured mouse oocytes: Alterations of spindle integrity and chromosome alignment. Tobacco Induced Diseases, 2(3), 151–161. https://doi.org/10.1186/1617-9625-2-3-151
   PubMedGoogle Scholar