Acta Vet. Brno 2022, 91: 59-68

https://doi.org/10.2754/avb202291010059

Torpor/hibernation cycle may enhance the risk of insecticides for bats: an in vitro study

Miroslava Kaňová1, Hana Banďouchová1, Ehdaa E. E. Abdelsalam1, Petr Linhart1,2, Jana Sedláčková1, Veronika Seidlová1, Jan Zukal1,3, Jiří Pikula1

1University of Veterinary Sciences Brno, Faculty of Veterinary Hygiene and Ecology, Department of Ecology and Diseases of Zoo Animals, Game, Fish and Bees, Brno, Czech Republic
2University of Veterinary Sciences Brno, Faculty of Veterinary Hygiene and Ecology, Department of Animal Protection and Welfare, Brno, Czech Republic
3Institute of Vertebrate Biology of the Czech Academy of Sciences v.v.i., Brno, Czech Republic

Received October 10, 2021
Accepted November 23, 2021

References

1. Abdelsalam EEE, Bandouchova H, Heger T, Kanova M, Kobelkova K, Nemcova M, Piacek V, Sedlackova J, Seidlova V, Vitula F, Pikula J 2020: Polychlorinated biphenyl toxicity in the thyroid gland of wild ungulates: an in vitro model. Acta Vet Brno 89: 151-162 <https://doi.org/10.2754/avb202089020151>
2. Arendt T, Stieler J, Strijkstra AM, Hut RA, Rüdiger J, Van der Zee EA, Harkany T, Holzer M, Härtig W 2003: Reversible paired helical filament like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J Neurosci 23: 6972-6981 <https://doi.org/10.1523/JNEUROSCI.23-18-06972.2003>
3. Astashkina A, Mann B, Grainger DW 2012: A critical evaluation of in vitro cell culture models for high-throughput drug screening and toxicity. Pharmacol Ther 134: 82-106 <https://doi.org/10.1016/j.pharmthera.2012.01.001>
4. Bartonicka T, Zukal J 2003: Flight activity and habitat use of four bat species in a small town revealed by bat detectors. Folia Zool 52: 155-166
5. Bayat S, Geiser F, Kristiansen P, Wilson SC 2014: Organic contaminants in bats: Trends and new issues. Environ Int 63: 40-52 <https://doi.org/10.1016/j.envint.2013.10.009>
6. Berry RW 1977: The evaluation of permethrin for wood preservation. Pestic Sci 8: 284-290 <https://doi.org/10.1002/ps.2780080318>
7. Biggar KK, Storey KB 2009: Perspectives in cell cycle regulation: lessons from an anoxic vertebrate. Curr Genomics 10: 573-584 <https://doi.org/10.2174/138920209789503905>
8. Bouma HR, Carey HV, Kroese FGM 2010: Hibernation: the immune system at rest? J Leukoc Biol 88: 619-624 <https://doi.org/10.1189/jlb.0310174>
9. Brigham RM 2007: Bats in forests: conservation and management. In: Lacki ML, Hayes JP, Kurta A (Eds): What we know and what we need to learn. Johns Hopkins University Press, MD, Baltimore, pp. 1-15
10. Buckingham SD, Lapied B, Le Corronc H, Grolleau F, Sattelle DB 1997: Imidacloprid actions on insect neuronal acetylcholine receptors. J Exp Biol 200: 2685-2692 <https://doi.org/10.1242/jeb.200.21.2685>
11. Carey HV, Andrews MT, Martin SL 2003: Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83: 1153-1181 <https://doi.org/10.1152/physrev.00008.2003>
12. Chao LS, Casida JE 1997: Interaction of imidacloprid metabolites and analogs with the nicotinic acetylcholine receptor of mouse brain in relation to toxicity. Pestic Biochem Physiol 58: 77-88 <https://doi.org/10.1006/pest.1997.2284>
13. Clark DR, Shore RF 2001: Chiroptera. In: Shore RF, Battner BA (Eds): Ecotoxicology of wild mammals. John Wiley & Sons, Ltd., London, pp. 108-114
14. Clark DR 1981: Special Scientific Report Wildlife. Bats and Environmental Contaminants: A Review. US Department of the Interior, Fish and Wildlife Service, Washington DC, 235 p.
15. Clark JM, Matsumura F 1982: Two different types of inhibitory effects of pyrethroids on nerve Ca− and Ca+Mg-atpase activity in the squid, Loligo pealei. Pestic Biochem Physiol 18:180-190 <https://doi.org/10.1016/0048-3575(82)90104-3>
16. Crayton SM, Wood PB, Brown DJ, Millikin AR, McManus TJ, Simpson TJ, Kang-Mo Ku Yong-Lak Park 2020: Bioaccumulation of the pesticide imidacloprid in stream organisms and sublethal effects on salamanders. GECCO 24: e01292
17. Crosby EB, Bailey JM, Oliveri AN, Levinb ED 2015: Neurobehavioral impairments caused by developmental imidacloprid exposure in zebrafish. Neurotoxicol Teratol 49: 81-90 <https://doi.org/10.1016/j.ntt.2015.04.006>
18. Dong K 2007: Insect sodium channels and insecticide resistance. Invert Neurosci 7: 17-30 <https://doi.org/10.1007/s10158-006-0036-9>
19. Fenton MB 1983: Just Bats. Toronto Buffalo, University of Toronto, London, 165 p.
20. Flieger M, Bandouchova H, Cerny J, Chudíčková M, Kolarik M, Kovacova V, Martínková N, Novák P, Šebesta O, Stodůlková E, Pikula J 2016: Vitamin B2 as a virulence factor in Pseudogymnoascus destructans skin infection. Sci Rep 6: 33200 <https://doi.org/10.1038/srep33200>
21. Gaisler J, Zukal J, Řehák Z, Homolka M 1998: Habitat preference and flight activity of bats in a city. J Zool 244: 439-445 <https://doi.org/10.1111/j.1469-7998.1998.tb00048.x>
22. Gleadhill A 2004: Permethrin toxicity in cats. Vet Rec 155: 648
23. Hajkova P, Pikula J 2007: Veterinary treatment of evening bats (Vespertilionidae) in the Czech Republic. Vet Rec 161: 139-140 <https://doi.org/10.1136/vr.161.4.139>
24. He X, Korytar T, Zhu Y, Pikula J, Bandouchova H, Zukal J, Köllner B 2014: Establishment of Myotis myotis cell lines - model for investigation of host-pathogen interaction in a natural host for emerging viruses. Plos One 9: e109795 <https://doi.org/10.1371/journal.pone.0109795>
25. Heger T, Zukal J, Seidlova V, Nemcova M, Necas D, Papezikova I, Piacek V, Zajickova R, Bandouchova H, Pikula J 2020: Measurement of phagocyte activity in heterotherms. Acta Vet Brno 89: 79-87 <https://doi.org/10.2754/avb202089010079>
26. Kalcounis-Rueppell MC, Payne VH, Huff SR, Boyko AL 2007: Effects of wastewater treatment plant effluent on bat foraging activity in an urban stream system. Biol Conserv 134: 120-130 <https://doi.org/10.1016/j.biocon.2007.04.009>
27. Klement W, Oliviero F, Gangarossa G, Zub E, De Bock F, Forner-Piquer I, Blaquiere M, Lasserre F, Pascussi J-M, Maurice T, Audinat E, Ellero-Simatos S, Gamet-Payrastre L, Mselli-Lakhal L, Marchi N 2020: Life-long Dietary Pesticide Cocktail Induces Astrogliosis Along with Behavioral Adaptations and Activates p450 Metabolic Pathways. J Neurosci 446: 225-237 <https://doi.org/10.1016/j.neuroscience.2020.07.039>
28. Kovacova V, Abdelsalam EEE, Bandouchova H, Brichta J, Havelkova B, Piacek V, Vitula F, Pikula J 2016: Cytotoxicity of ketamine, xylazine and Hellabrunn mixture in liver-, heart- and kidney-derived cells from fallow deer. Neuroendocrinol Lett 37: 78-83
29. Kunz TH, Braun de Torrez E, Bauer D, Lobova T, Fleming T 2011: Ecosystem services provided by bats. Ann. N.Y. Acad Sci 1223: 1-38 <https://doi.org/10.1111/j.1749-6632.2011.06004.x>
30. Kunz TH, Wrazen JA, Burnett CD 1998: Changes in body mass and fat reserves in prehibernating little brown bats (Myotis lucifugus). Écoscience 5: 8-17 <https://doi.org/10.1080/11956860.1998.11682443>
31. LeCluyse EL, Witek RP, Andersen ME, Powers MJ 2012: Organotypic liver culture models: Meeting current challenges in toxicity testing. Crit Rev Toxicol 42: 501-548 <https://doi.org/10.3109/10408444.2012.682115>
32. Linhart P, Bandouchova H, Zukal J, Votýpka J, Kokurewicz T, Dundarova H, Apoznański G, Heger T, Kubickova A, Nemcova M, Piacek V, Sedlackova J, Seidlova V, Berkova H, Hanzal V, Pikula J 2020: Trypanosomes in Eastern and Central European bats. Acta Vet Brno 89: 69-78 <https://doi.org/10.2754/avb202089010069>
33. Lyman CP, Willis JS, Malan A, Wang LCH 1982: Hibernation in mammals and birds. Academic Press, New York, 320 p.
34. Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB 2001: Neonicotinoids: insecticides acting on insect nicotinicacetylcholine receptors. Trends Pharmacol Sci 22: 573-580 <https://doi.org/10.1016/S0165-6147(00)01820-4>
35. McFarland CA 1998: Potential agricultural insecticide exposure of Indiana bats (Myotis sodalis) in Missouri. University of Missouri, Missouri, Colombia, 256 p.
36. Mencke N 2006: Acaricidal and repellent properties of permethrin, its role in reducing transmission of vector-borne pathogens. Parassitologia 48: 139-140
37. Mineau P, Callaghan C 2018: Neonicotinoid insecticides and bats: an assessment of the direct and indirect risks. Canadian Wildlife Federation, 87 p.
38. Mitchell-Jones AJ, Cooke AS, Boyd I.L, Stebbings RE 1989: Bats and remedial timber treatment chemicals a review. Mamm Rev 19: 93-110 <https://doi.org/10.1111/j.1365-2907.1989.tb00405.x>
39. Moore MS, Reichard JD, Murtha TD, Nabhan ML, Pian RE, Ferreira JS, Kunz TH 2013: Hibernating little brown myotis (Myotis lucifugus) show variable immunological responses to white-nose syndrome. PLoS ONE 8: 58976 <https://doi.org/10.1371/journal.pone.0058976>
40. Nelson CJ, Otis JP, Martin SL, Carey HV 2008: Analysis of the hibernation cycle using LC-MS-based metabolomics in ground squirrel liver. Physiol Genomics 37: 43-51 <https://doi.org/10.1152/physiolgenomics.90323.2008>
41. Nemcova M, Pikula J, Zukal J, Seidlova V 2020: Diclofenac-induced cytotoxicity in cultured carp leukocytes. Physiol Res 69: 607-618 <https://doi.org/10.33549/physiolres.934609>
42. Park K 2015: Mitigating the impacts of agriculture on biodiversity: bats and theirpotential role as bioindicators. Mamm Biol 80: 191-204 <https://doi.org/10.1016/j.mambio.2014.10.004>
43. Pikula J, Heger T, Bandouchova H, Kovacova V, Nemcova M, Papezikova I, Piacek V, Zajíčková R, Zukal J 2020: Phagocyte activity reflects mammalian homeo- and hetero-thermic physiological states. BMC Vet Res 16: 232 <https://doi.org/10.1186/s12917-020-02450-z>
44. Ransome RD 1989: Population changes of greater horseshoe bats studied near Bristol over the past twenty-six years. Biol J Linn Soc 38: 71-82 <https://doi.org/10.1111/j.1095-8312.1989.tb01564.x>
45. Russo D, Ancillotto L 2015: Sensitivity of bats to urbanization: a review. Mamm Biol 80: 205-212 <https://doi.org/10.1016/j.mambio.2014.10.003>
46. Sheets LP 2002: The Neonicotinoid Insecticides. In: Massaro EJ (Ed.): Handbook of Neurotoxicology Vol. 1. Chapter 6, NJ: Humana Press, Totowa, pp. 79-87
47. Sheets LP 2014: Imidacloprid. In: Anderson B, de Peyster A, Shayne CG, Hakkinen PJ, Kamrin M, Locey B, Mehendale HM, Pope C, Shugart L (Eds): Encyclopedia of Toxicology, pp. 1000-1003
48. Soldatow VY, Lecluyse EL, Griffith LG, Rusyn I 2013: In vitro models for liver toxicity testing. Tox Res 2: 23-39 <https://doi.org/10.1039/C2TX20051A>
49. Stebbings RE, Griffiths F 1986: Distribution and status of bats in Europe. Institute of Terrestrial Ecology, Huntingdon, 142 p.
50. Tišler T, Jemec A, Mozetic B, Trebše P 2009: Hazard identification of imidacloprid to aquatic environment. Chemosphere 76: 907-914 <https://doi.org/10.1016/j.chemosphere.2009.05.002>
51. Tomizawa M, Casida JE 1999: Minor structural changes in nicotinic insecticides confer differential subtype selectivity for mammalian nicotinic acetylcholine receptors. Br J Pharmacol 127: 115-122 <https://doi.org/10.1038/sj.bjp.0702526>
52. Tomlin CDS 2006: The Pesticide Manual, a World Compendium. 14th edn; British Crop Protection Council, Surry, England, pp. 598-599
53. Vignet C, Cappello T, Fu Q, Lajoie K, De Marco G, Clérandeau C, Mottaz H, Maisano M, Hollender J, Schirmer K, Cachot J 2019: Imidacloprid induces adverse effects on fish early life stages that are more severe in Japanese medaka (Oryzias latipes) than in zebrafish (Danio rerio). Chemosphere 225: 470-478 <https://doi.org/10.1016/j.chemosphere.2019.03.002>
54. Webb PI, Speakman JR, Racey PA 1996: How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can J Zool 74: 761-765 <https://doi.org/10.1139/z96-087>
55. Webb RE, Frank JR, Raupp MJ 2003: Eastern hemlock recovery from hemlock woolly adelgid damage following imidacloprid therapy. J Arboric 29: 298-302
56. Werner I, Moran K 2008: Effects of pyrethroid insecticides on aquatic organisms. ACS Symp Ser 991: 310-334 <https://doi.org/10.1021/bk-2008-0991.ch014>
57. Williams DR, Epperson LE, Li W, Hughes MA, Taylor R, Rogers J, Martin SL, Cossins AR, Gracey AY 2005: Seasonally hibernating phenotype assessed through transcript screening. Physiol Genomics 24: 13-22 <https://doi.org/10.1152/physiolgenomics.00301.2004>
58. Wu CH, Lin CL, Wang SE, Lu CW 2020: Effects of imidacloprid, a neonicotinoid insecticide, on the echolocation system of insectivorous bats. Pestic Biochem Physiol 163: 94-101 <https://doi.org/10.1016/j.pestbp.2019.10.010>
59. Xiao Y, Wu Y, Sun K, Wang H, Zhang B, Song S et al. 2015: Differential Expression of Hepatic Genes of the Greater Horseshoe Bat (Rhinolophus ferrumequinum) between the Summer Active and Winter Torpid States. PLoS ONE 10: 0145702
60. Zamariola N, Toledo Netto P, da Silva Franchi CA, de Camargo JLV, de Marchi MRR 2017: QuEChERS-Based Method for Pesticides Analysis in Adipose Tissue Associated with Rat Ovaries. J Anal Toxicol 41: 399-406 <https://doi.org/10.1093/jat/bkx023>
61. Zeidan Q, Hart GW 2010: The intersections between O-GlcNAcylation and phosphorylation: implications for multiple signaling pathways. J Cell Sci 23: 13-22 <https://doi.org/10.1242/jcs.053678>
62. Zukal J, Pikula J, Bandouchova H 2015: Bats as bioindicators of heavy metal pollution: history and prospect. Mamm Biol 80: 220-227 <https://doi.org/10.1016/j.mambio.2015.01.001>
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