Effect of the Insecticide Chlorpyrifos on Behavioral and Metabolic Aspects of the Spider Polybetes pythagoricus.
Chlorpyrifos
Hydrocarbons
Oxidative stress
Reactive oxygen species
Spider
Journal
Environmental toxicology and chemistry
ISSN: 1552-8618
Titre abrégé: Environ Toxicol Chem
Pays: United States
ID NLM: 8308958
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
revised:
09
02
2023
received:
22
12
2022
accepted:
13
03
2023
medline:
29
5
2023
pubmed:
16
3
2023
entrez:
15
3
2023
Statut:
ppublish
Résumé
The toxicity of pesticides to organisms depends on the total amount of chemical exposure. Toxicity can be minimized if the organism recognizes the pesticide and alters its behavior. Furthermore, the physical barrier of cuticular hydrocarbons can prevent the entrance of the pesticide into the organism. Finally, if the pesticide enters the body, the organism experiences physiological changes favoring detoxification and the maintenance of homeostasis. We analyzed the behavioral and metabolic response of the spider Polybetes pythagoricus at different times of exposure to the organophosphate pesticide chlorpyrifos. First we observed that the individuals are capable of recognizing and avoiding surfaces treated with pesticides based on a behavioral analysis. Subsequently, we characterized cuticular hydrocarbons as a possible barrier against pesticides. Then we observed that the pesticide provoked histological damage, mainly at the level of the midgut diverticula. Finally, we analyzed the activity of several of the spider's enzymes linked to oxidative stress after exposure to chlorpyrifos for different lengths of time (6, 24, and 48 h). We observed that catalase activity was high at the start, whereas the activity of superoxide dismutase and glutathione S-transferase changed significantly at 48 h. Lipid peroxidation became high at 6 h, but decreased at 48 h. In conclusion, although P. pythagoricus can avoid contact with chlorpyrifos, this pesticide causes activation of the antioxidant system when it enters the body. Our results make a significant contribution to the ecotoxicology of spiders. Environ Toxicol Chem 2023;42:1293-1308. © 2023 SETAC.
Substances chimiques
Insecticides
0
Chlorpyrifos
JCS58I644W
Catalase
EC 1.11.1.6
Pesticides
0
Antioxidants
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1293-1308Informations de copyright
© 2023 SETAC.
Références
Abdelfattah, E. A., & El-Bassiony, G. M. (2022). Impact of malathion toxicity on the oxidative stress parameters of the black soldier fy Hermetia illucens (Linnaeus, 1758) (Diptera: Stratiomyidae). Scientifc Reports, 12, 4583. https://doi.org/10.1038/s41598-022-08564-8
Adedara, I. A., Abolaji, A. O., Rocha, J. B. T., & Farombi, E. O. (2016). Diphenyl diselenide protects against mortality, locomotor deficits and oxidative stress in drosophila melanogaster model of manganese-induced neurotoxicity. Neurochemical Research, 41(6), 1430-1438.
Aebi, H. (1984). Catalasein vitro. Methods in Enzymology, 105, 121-126. https://doi.org/10.1016/s0076-6879(84)05016-3
Ahmed, F. A. G., & El-Sobki, A. E. A. M. (2021). Biochemical and histological responses of red palm weevil, Rhynchophorus ferrugineus exposed to sub-lethal levels of different insecticide classes. Egyptian Academic Journal of Biological Sciences, 13(1), 293-308. https://doi.org/10.21608/eajbsf.2021.211778
Aktar, M. W., Sengupta, D. S., & Chowdhury, A. (2009). Impact of pesticides use in agriculture: Their benefits and hazards. Interdisciplinary Toxicology, 2(1), 1-12. https://doi.org/10.2478/v10102-009-0001-7
Alzahrani, A. M. (2019). Ultrastructural damage and biochemical alterations in the testes of red palm weevils (Rhynchophorus ferrugineus) exposed to imidacloprid. Environmental Science and Pollution Research, 26(16), 16548-16555. https://doi.org/10.1007/s11356-019-04968-8
Arrighetti, F., Ambrosio, E., Astiz, M., Rodrigues Capítulo, A., & Lavarías, S. (2018). Differential response between histological and biochemical biomarkers in the apple snail Pomacea canaliculata (Gasteropoda: Amullariidae) exposed to cypermethrin. Aquatic Toxicology, 194, 140-151. https://doi.org/10.1016/j.aquatox.2017.11.014
Aslanturk, A., Kalender, S., Uzunhisarcikli, M., & Kalender, Y. (2011). Effects of methidathion on antioxidant enzyme activities and malondialdehyde level in midgut tissues of Lymantria dispar (Lepidoptera) larvae. Journal of the Entomological Research Society, 13(3), 27-38. https://doi.org/10.81043/aperta.21151
Awasthi, M. D., & Prakash, N. B. (1999). Persistence of chlorpyrifos in soils under different moisture regimes. Pesticide Science, 50(1), 1-4. https://doi.org/10.1002/(sici)1096-9063(199705)50:13.0.co;2-x
Babczyńska, A., & Migula, P. (2002). Cadmium-fenitrothion interaction in the spider Pardosa lugubris and the fruit fly Drosophila melanogaster. Bulletin of Environmental Contamination and Toxicology, 69, 586-592. https://doi.org/10.1007/s00128-002-0101-y
Babczyńska, A., Wilczek, G., & Migula, P. (2006). Effects of dimethoate on spiders from metal pollution gradient. Science of the Total Environment, 370, 352-359. https://doi.org/10.1016/j.scitotenv.2006.06.024
Balabanidou, V., Grigoraki, L., & Vontas, V. (2018). Insect cuticle: A critical determinant of insecticide resistance. Current Opinion in Insect Science, 27, 68-74. https://doi.org/10.1016/j.cois.2018.03.001
Balabanidou, V., Kampouraki, A., MacLean, M., Blomquist, G., Tittiger, C., Juárez, M., Mijailovsky, S., Chalepakis, G., Anthousi, A., Lynd, A., Antoine, S., Hemingway, J., Ranson, H., Lycett, G., & Vontas, J. (2016). Cytochrome P450 associated with insecticide resistance catalyzes cuticular hydrocarbon production in Anopheles gambiae. Proceedings of the National Academy of Sciences of the United States of America, 113, 9268-9273. https://doi.org/10.1073/pnas.1821201116
Balabanidou, V., Mary Kefi, M., Aivaliotis, M., Koidou, V., Girotti, J. R., Mijailovsky, S., Juárez, M., Papadogiorgaki, E., Chalepakis, G., Kampouraki, A., Nikolaou, C., Ranson, H., & Vontas, J. (2019). Mosquitoes cloak their legs to resist insecticides. Proceedings of the Royal Society B: Biological Sciences, 286(1907), 20191091. https://doi.org/10.1098/rspb.2019.1091
Bass, C., Puinean, A., Zimmer, C., Denholm, I., Field, L., Foster, S., Gutbrod, O., Nauen, R., Slater, R., & Williamson, M. (2014). The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochemistry and Molecular Biology, 51, 41-51. https://doi.org/10.1016/j.ibmb.2014.05.003
Bayram, A., & Luff, M. L. (1993). Winter abundance and diversity of lycosids (Lycosidae, Araneae) and other spiders in grass tussocks in a field margin. Pedobiologia, 37(6), 357-364.
Beauvais, S. L., Atchison, G. J., Stenback, J. Z., & Crumpton, W. G. (1999). Use of cholinesterase activity to monitor exposure of Chironomus riparius (Diptera: Chironomidae) to a pesticide mixture in hypoxic wetland mesocosms. Hydrobiologia, 416, 163-170. https://doi.org/10.1023/a:1003819621659
Bellas, J., Beiras, R., Marino-Balsa, J., & Fernandez, N. (2005). Toxicity of organic compounds to marine invertebrate embryos and larvae: A comparison between the sea urchin embryogenesis bioassay and alternative test species. Ecotoxicology, 14(3), 337-353. https://doi.org/10.1007/s10646-004-6370-y
Boccioni, A. C. P., Lajmanovich, R. C., Peltzer, P. M., Attademo, A. M., & Martinuzzi, C. S. (2021). Toxicity assessment at different experimental scenarios with glyphosate, chlorpyrifos and antibiotics in Rhinella arenarum (Anura: Bufonidae) tadpoles. Chemosphere, 273, 128475. https://doi.org/10.1016/j.chemosphere.2020.128475
Booth, L. H., & O'Halloran, K. (2001). A comparison of biomarker responses in the earthworm Aporrectodea caliginosa to the organophosphorus insecticides diazinon and chlorpyrifos. Environmental Toxicology and Chemistry, 20(11), 2494-2502. https://doi.org/10.1002/etc.5620201115
Booth, L. H., Wratten, S. D., & Kehrli, P. (2007). Effects of reduced rates of two insecticides on enzyme activity and mortality of an aphid and its lacewing predator. Journal of Economic Entomology, 100, 11-19. https://doi.org/10.1603/0022-0493(2007)100[11:eorrot]2.0.co;2
Calberg, E., & Mannervik, A. (1985). Glutathione reductase. Methods Enzimol, 113, 484-495.
Carlson, D. A., Bernier, U. R., & Sutton, B. C. (1998). Elution patterns from capillary GC for methyl-branched alkanes. Journal of Chemical Ecology, 24, 1845-1865.
Carvalho, F. P. (2017). Pesticides, environment, and food safety. Food and Energy Security, 6(2), 48-60. https://doi.org/10.1002/fes3.108
Cunningham, M. L., Garcia, C. F., Gonzales-Baró, M. R., Garda, H., & Pollero, R. (2002). Organophosphorus insecticide fenitrothion alters the lipid dynamics in the spider Polybetes pythagoricus high density lipoproteins. Pesticide Biochemistry and Physiology, 73, 37-47. https://doi.org/10.1016/S0048-3575(02)00016-0
Dar, M. A., Kaushika, G., & Villarreal-Chiub, J. F. (2019). Pollution status and bioremediation of chlorpyrifos in environmental matrices by the application of bacterial communities: A review. Journal of Environmental Management, 239, 124-136. https://doi.org/10.1016/j.jenvman.2019.03.048
Day, K. E., & Scott, I. M. (1990). Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides. Aquatic Toxicology, 18(2), 101-113. https://doi.org/10.1016/0166-445x(90)90021-g
Degrendele, C., Okonski, K., Melymuk, L., Landlová, L., Kukucka, P., Audy, O., Kohoutek, J., Cupr, P., & Klánová, J. (2016). Pesticides in the atmosphere: A comparison of gas-particle partitioning and particle size distribution of legacy and current-use pesticides. Atmospheric Chemistry and Physics (Print), 16, 1531-1544. https://doi.org/10.5194/acp-16-1531-2016
Di Nica, V., González, A. B. M., Lencioni, V., & Villa, S. (2019). Behavioural and biochemical alterations by chlorpyrifos in aquatic insects: An emerging environmental concern for pristine Alpine habitats. Environmental Science and Pollution Research, 27, 30918-30926. https://doi.org/10.1007/s11356-019-06467-2
Díaz-Barriga Arceo, S., Martínez-Tabche, L., Álvarez-González, I., López López, E., & Madrigal-Bujaidar, E. (2015). Toxicity induced by dieldrin and chlorpyrifos in the freshwater crayfish Cambarellus montezumae (Cambaridae). Revista de biología tropical, 63(1), 83-96. https://doi.org/10.15517/rbt.v63i1.13665
Ding, T., Zhang, Y., Zhu, Y., Du, S., Zhang, J., Cao, Y., Wang, Y., Wang, G., & He, L. (2019). Deriving water quality criteria for China for the organophosphorus pesticides dichlorvos and malathion. Environmental Science and Pollution Research, 26(33), 34622-34632. https://doi.org/10.1007/s11356-019-06546-4
Dinter, A., & Poehling, H.-M. (1995). Side-effects of insecticides on two erigonid spider species. Entomologia Experimentalis et Applicata, 74(2), 151-163. https://doi.org/10.1111/j.1570-7458.1995.tb01887.x
dos Santos Junior, V. C., Martínez, L. C., Plata-Rueda, A., Fernandes, F. L., de Souza Tavares, W., Zanuncio, J. C., & Serr, J. E. (2020). Histopathological and cytotoxic changes induced by spinosad on midgut cells of the non-target predator Podisus nigrispinus Dallas (Heteroptera: Pentatomidae). Chemosphere, 238, 124585. https://doi.org/10.1016/j.chemosphere.2019.124585
Edwards, C. A., & Fisher, S. W. (1991). The use of cholinesterase measurements in assessing the impact of pesticides on terrestrial and aquatic invertebrates. In P. Mineau (Ed.), “Cholinesterase inhibiting insecticides-Impacts on wildlife and environment”. Elsevier.
El-Khouly, N. M., Rahil, A. A., & Dwidar, E. F. (2016). Effect of three inseticides on some biological and histological aspect of the spider Anelosimus aulicus (Koch). Fayoum Journal of Agricultural Research and Development, 30(2), 37-52.
El-Saad, A. M. A., Kheirallah, D. A., & El-Samad, L. M. (2017). Biochemical and histological biomarkers in the midgut of Apis mellifera from polluted environment at Beheira Governorate, Egypt. Environmental Science and Pollution Research, 24, 3181-3193. https://doi.org/10.1007/s11356-016-8059-1
Ellman, G. L., & Callaway, E. (1961). Erythrocyte cholinesterase-levels in mental patients. Nature, 192, 1216.
Engenheiro, E. L., Hankard, P. K., Sousa, J. P., Lemos, M. F., Weeks, J. M., & Soares, A. M. V. M. (2005). Influence of dimethoate on acetylcholinesterase activity and locomotor function in terrestrial isopods. Environmental Toxicology and Chemistry, 24, 603-609. https://doi.org/10.1897/04-131r.1
Erban, T., Sopko, B., Vaclavikova, M., Tomesova, D., Halesova, T., & Rezac, M. (2019). Pesticide comparison of Phylloneta impressa (Araneae: Theridiidae) females, cocoons and webs with prey remnants collected from a rape field before the harvest. Pest Management Science, 76, 1128-1133.
Evans, S. C., Shaw, E. M., & Rypstra, A. L. (2010). Exposure to a glyphosate-based herbicide affects agrobiont predatory arthropod behaviour and long-term survival. Ecotoxicology, 19, 1249-1257. https://doi.org/10.1007/s10646-010-0509-9
Everts, J. W., Aukema, B., Mulliré, W. C., van Gemerden, A., Rottier, A., van Katz, R., & van Gestel, C. A. M. (1991). Exposure of the ground dwelling spider Oedothorax apicatus (Blackwall) (Erigonidae) to spray and residues of deltamethrin. Archives of Environmental Contamination and Toxicology, 20, 13-19. https://doi.org/10.1007/BF01065322
Fairbrother A., Marden, B., Bennett, J., & Hooper, M. (1991). Methods used in determination of cholinesterase activity. In P. Mineau (Ed.), Cholinesterase inhibiting insecticides: Their impact on wildife and the environment (pp. 35-72). Chemicals in Agriculture, Vol. 2. Elsevier.
Flohé, L., & Gunzler, W. A. (1984). Assays of glutathione peroxidase. Methods Enzimology, 105, 114-121. https://doi.org/10.1016/s0076-6879(84)05015-1
Foelix, R. F., & Chu-Wang, I. W. (1973). The morphology of spider sensilla II. chemoreceptors. Tissue and Cell, 5(3), 461-478. https://doi.org/10.1016/S0040-8166(73)80038-2
Food Safety News. (2019). EU votes against renew chlorpyrifos approval. https://www.foodsafetynews.com/2019/12/eu-votes-against-renewingchlorpyrifos-approval/
Foong, S. Y., Ma, N. L., Lam, S. S., Peng, W., Low, F., Lee, B. H. K., Alstrup, A. K. O., & Sonne, C. (2020). A recent global review of hazardous chlorpyrifos pesticide in fruit and vegetables: Prevalence, remediation and actions needed. Journal of Hazardous Materials, 400, 123006. https://doi.org/10.1016/j.jhazmat.2020.123006
Galloway, T., & Handy, R. (2003). Immunotoxicity of organophosphorous pesticides. Ecotoxicology and Environmental Safety, 12, 345-363. https://doi.org/10.1023/a:1022579416322
Gibbs, A., & Pomonis, J. G. (1995). Physical properties of insect cuticular hydrocarbons: The effects of chain length, methyl-branching and unsaturation. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 112(2), 243-249. https://doi.org/10.1016/0305-0491(95)00081-X
Gomes, H. D. O., Menezes, J. M. C., da Costa, J. G. M., Coutinho, H. D. M., Teixeira, R. N. P., & do Nascimento, R. F. (2020). A socio-environmental perspective on pesticide use and food production. Ecotoxicology and Environmental Safety, 197, 11062. https://doi.org/10.1016/j.ecoenv.2020.110627
Goven, A. J., Fitzpatrick, L. C., Eyambe, G. S., Venables, B. J., & Cooper, E. L. (1993). Cellular biomarkers for measuring toxicity of xenobiotics: Effects of polychlorinated biphenyls on earthworm Lumbricus terrestris coelomocytes. Environmental Toxicology and Chemistry, 12(5), 863-870. https://doi.org/10.1002/etc.5620120510
Habig, W., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 22, 7130-7139. https://doi.org/10.1016/S0021-9258(19)42083-8
Halliwell, B. J., & Gutteridge, J. (2007). Free radicals in biology and medicine, 4th ed. Oxford University Press.
Hayes, J. D., & Pulford, D. J. (1995). The glutathione S-transferase supergene family: Regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Critical Reviews in Biochernisty and Molecular Biology, 30(6), 445-600. https://doi.org/10.3109/10409239509083491
Hemingway, J. (2000). The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochemistry and Molecular Biology, 30(11), 1009-1015. https://doi.org/10.1016/s0965-1748(00)00079-5
Hermes-Lima, M., Ramos-VAsconcelos, G. R., Cardoso, L. A., Rivera, P. M., & Drew, K. L. (2004). Animal adaptability to oxidative stress: Gastropod estivation and mammalian hibernation. In “Life in the Cold: Evolution, Mechanisms, Adaptation, and Application. Twelfth International Hibernation Symposium”. Biological Papers of the University of Alaska.
Huang, X., Cui, H., & Duan, W. (2020). Ecotoxicity of chlorpyrifos to aquatic organisms: A review. Ecotoxicology and Environmental Safety, 200, 110731. https://doi.org/10.1016/j.ecoenv.2020.110731
Hyne, R. V., & Maher, W. A. (2003). Invertebrate biomarkers: Links to toxicosis that predict population decline. Ecotoxicology and Environmental Safety, 54(3), 366-374. https://doi.org/10.1016/S0147-6513(02)00119-7
Janssens, R., & Stoks, L. (2017). Chlorpyrifos-induced oxidative damage is reduced under warming and predation risk: Explaining antagonistic interactions with a pesticide. Environmental Pollution, 226, 79-88. https://doi.org/10.1016/j.envpol.2017.04.012
John, E. M., & Shaike, J. M. (2015). Chlorpyrifos: Pollution and remediation. Environmental Chemistry Letters, 13(3), 269-291. https://doi.org/10.1007/s10311-015-0513-7
Juárez, M. P., Pedrini, N., Girotti, J. R., & Mijailovsky, S. J. (2010). Pyrethroid resistance in Chagas disease vectors: The case of Triatoma infestans cuticle. Review. In “Resistant Pest Management Newsletter”, (Vol. 19, pp. 59-61). Center for Integrated Plant Systems (CIPS) Insecticide Resistance Action Committee (IRAC) Western Regional Coordinating Committee (WRCC-60).
Juárez, P. (1994). Inhibition of cuticular lipid synthesis and its effect on insect survival. Archives of Insect Biochemistry and Physiology, 25(3), 177-191. https://doi.org/10.1002/arch.940250302
Kalita, M. K., Haloi, K., & Devi, D. (2016). Larval exposure to chlorpyrifos affects nutritional physiology and induces genotoxicity in silkworm Philosamia ricini (Lepidoptera: Saturniidae. Frontiers in Physiology, 7, 535. https://doi.org/10.3389/fphys.2016.00535
Kammon, A. M., Brar, R. S., Banga, H. S., & Sodhi, S. (2010). Patho-biochemical studies on hepatotoxicity and nephrotoxicity on exposure to chlorpyrifos and imidacloprid in layer chickens. Veterinarski Arhiv, 80(5), 663-672. https://hrcak.srce.hr/62160
Ketterer, B., Coles, B., & Meyer, D. J. (1983). The role of glutathione in detoxication. Environmental Health Perspectives, 49, 59-69.
Khan, M. M., Hafeez, M., Elgizawy, K., Wang, H., Zhao, J., Cai, W., Ma, W., & Hua, H. (2021). Sublethal effects of chlorantraniliprole on Paederus fuscipes (Staphylinidae: Coleoptera), a general predator in paddle field. Environmental Pollution, 291, 118171. https://doi.org/10.1016/j.envpol.2021.118171
Kidd, P. M. (1997). Glutathione: Systemic protectant against oxidative and free radical damage. Alternative Medicine Review, 2(3), 155-176.
Kostaropoulos, I., Papadopoulos, A. I., Metaxakis, A., Boukouvala, E., & Papadopoulou-Mourkidou, E. (2001). Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochemistry and Molecular Biology, 31(4-5), 313-319. https://doi.org/10.1016/s0965-1748(00)00123-5
Kovats, E. (1965). Gas chromatographic comparison of organic substances in the retention index system. Advances in Chromatography, 1, 229-247.
Kralj, M. B., Černigoj, U., Franko, M., & Trebše, P. (2007). Comparison of photocatalysis and photolysis of malathion, isomalathion, malaoxon, and commercial malathion-Products and toxicity studies. Water Research, 41(19), 4504-4514. https://doi.org/10.1016/j.watres.2007.06.016
Lacava, M., García, L. F., Viera, C., & Michalko, R. (2021). The pest-specific effects of glyphosate on functional response of a wolf spider. Chemosphere, 262, 127785. https://doi.org/10.1016/j.chemosphere.2020.127785
Laino, A., Cunningham, M. L., Garcia, F., & Heras, H. (2009). First insight into the lipid uptake, storage and mobilization in arachnids: Role of midgut diverticula and lipoproteins. Journal of Insect Physiology, 55(12), 1118-1124. https://doi.org/10.1016/j.jinsphys.2009.08.005
Laino, A., & Garcia, C. F. (2020). Study of the effect of cypermethrin on the spider Polybetes phytagoricus in different energy states. Pesticide Biochemistry and Physiology, 165, 104559. https://doi.org/10.1016/j.pestbp.2020.104559
Laino, A., Romero, S., Cunningham, M., Molina, G., Gabellone, C., Trabalon, M., & Garcia, C. F. (2021). Can wolf spider mothers detect insecticides in the environment? Does the silk of the egg-sac protect juveniles from insecticides? Environmental Toxicology and Chemistry, 40(10), 2861-2873. https://doi.org/10.1002/etc.5157
Lavarías, S., Arrighetti, F., & Siri, A. (2017). Histopathological effects of cypermethrin and Bacillus thuringiensis var. israelensis on midgut of Chironomus calligraphus larvae (Diptera: Chironomidae). Pesticide Biochemistry and Physiology, 139, 9-16. https://doi.org/10.1016/j.pestbp.2017.04.002
Lowry, O. H., Rosenbrough, N. J., Farr, A. L., & Randall, R. (1951). Protein measurement with the Folin phenol reagent. Journal of Biology and Chemistry, 193, 265-275.
Mahmood, S., Khan, N., Iqbal, K. J., Ashraf, M., & Khalique, A. (2018). Evaluation of water hyacinth (Eichhornia crassipes) supplemented diets on the growth, digestibility and histology of grass carp (Ctenopharyngodon idella) fingerlings. Journal of Applied Animal Research, 46(1), 24-28. https://doi.org/10.1080/09712119.2016.1256291
Maloney, D., Drummond, F. A., & Alford, R. (2003). Spider predation in agroecosystems: Can spiders effectively control pest populations? Maine Agricultural and Forest Experiment Station Technical Bulletin.
Mannervik, B., & Danielson, U. H. (1988). Glutathione transferases-Structure and catalytic activity. Critical Reviews in Biochemistry, 23(3), 283-337. https://doi.org/10.3109/10409238809088226
Ministry of Agriculture and Rural Affairs of the People's Republic of China. (2013). Announcement No. 2032 (In Chinese). http://www.moa.gov.cn/govpublic/ZZYGLS/201312/t20131219_3718683.htm
Mesnage, R., & Antoniou, M. N. (2018). Ignoring adjuvant toxicity falsifies the safety profile of commercial pesticides. Frontiers in Public Health, 5, 361. https://doi.org/10.3389/fpubh.2017.00361
Michalko, R., & Košulič, O. (2015). Temperature-dependent effect of two neurotoxic insecticides on predatory potential of Philodromus spiders. Journal of Pest Science, 89(2), 517-527. https://doi.org/10.1007/s10340-015-0696-5
Michalko, R., Pekár, S., & Entling, M. H. (2018). An updated perspective on spiders as generalist predators in biological control. Oecologia, 189, 21-36. https://doi.org/10.1007/s00442-018-4313-1
Michalková, V., & Pekár, S. (2009). How glyphosate altered the behaviour of agrobiont spiders (Araneae: Lycosidae) and beetles (Coleoptera: Carabidae). Biological Control, 51, 444-449.
Misra, H. P., & Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry, 247, 3170-3175.
Motoyama, N., Suganuma, T., & Maekoshi, Y. (1992). Biochemical and physiologial characteristics of insecticide resistance in diamondback moth. Proceedings of the Second International Workshop, 1990, 411-418.
Mullié, W. C., & Everts, J. W. (1991). Uptake and elimination of [14C]deltamethrin by Oedothorax apicatus (Arachnida; Erigonidae) with respect to bioavailability. Pesticide Biochemistry and Physiology, 39(1), 27-34. https://doi.org/10.1016/0048-3575(91)90210-D
Nguyen Hong, S., Viet, T. Q., Dang Hoang, O., Do Phuong, C., Lan Huong, B., Dinh Tien, D., & Nguyen Huy, M. (2015). Acute toxic and hepatopancreas syndrome caused by chlopyrifos ethyl to black tiger shrimp (Penaeus monodon) and white shrimp (Litopenaeus vannamei) in Mekong River Delta of Vietnam. International Journal of Agricultural Technology, 11(5), 1097-1108.
Nikinmaa, M., & Anttila, K. (2019). Individual variation in aquatic toxicology: Not only unwanted noise. Aquatic Toxicology, 207, 29-33. https://doi.org/10.1016/j.aquatox.2018.11.021
Nyffeler, M. (1999). Prey selection of spiders in the field. In M. H. Greenstone & K. D. Sunderland (Eds.), Spiders in agroecosystems. Ecological processes and biological control. Journal of Arachnology, 27(1), 1-400.
Nyffeler, M., & Sterling, W. L. (1994). Comparison of the feeding niche of polyphagous insectivores (Araneae) in a Texas cotton plantation: Estimates of niche breadth and overlap. Environmental Entomology, 23(5), 1294-1303.
Nyffeler, M., & Sunderland, K. D. (2003). Composition, abundance and pest control potential of spider communities in agroecosystems: A comparison of European and US studies. Agriculture, Ecosystems & Environment, 95(2-3), 579-612. https://doi.org/10.1016/s0167-8809(02)00181-0
Ohkawa, H., Ohishi, N., & Yagi, K. (1979). Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Annales of Biochemistry, 95, 351-358.
Patil, R., Patil, Y., Salunkhe, P., & Patil, P. (2020). Diversity and distribution of agrobiont spiders (Arachnida: Araneae) from different agro-ecosistems of Anjani village, M.S. (India). International Journal of Research and Analytical Reviews, April, 455-460. https://doi.org/10.1729/Journal.20966
Pedrini, N., Mijailovsky, S. J., Girotti, J. R., Stariolo, R., Cardozo, R. M., Gentile, A., & Juárez, M. P. (2009). Control of pyrethroid-resistant chagas disease vectors with entomopathogenic fungi. PLoS Neglected Tropical Diseases, 3(5), e434. https://doi.org/10.1371/journal.pntd.0000434
Pekár, S. (2012). Spiders (Araneae) in the pesticide world: An ecotoxicological review. Pest Management Science, 68(11), 1438-1446. https://doi.org/10.1002/ps.3397
Pekár, S. (2013). Side effect of synthetic pesticides on spider. In W. Nentwing (Ed.), Spider ecophysiology. Springer.
Pekár, S., & Benes, J. (2008). Aged pesticide residues are detrimental to agrobiont spiders (Araneae). Journal of Applied Entomology, 132(8), 614-622. https://doi.org/10.1111/j.1439-0418.2008.01294.x
Pekár, S., & Haddad, C. R. (2005). Can agrobiont spiders (Araneae) avoid a surface with pesticide residues. Pest Management Science, 61(12), 1179-1185. https://doi.org/10.1002/ps.1110
Pimentel, D., Acquay, H., Biltonen, M., Rice, P., Silva, M., Nelson, J., Lipner, V., Giordano, S., Horowitz, A., & D'Amore, M. (1992). Environmental and economic costs of pesticide use. BioScience, 42(10), 750-760. https://doi.org/10.2307/1311994
Plata-Rueda, A., Martins de Menezesa, C. H., dos Santos Cunha, W., Alvarenga, T. M., Barbosa, B. F., Zanuncio, J. C., Martínez, L. C. & Serrão, J. E. (2020). Side-effects caused by chlorpyrifos in the velvetbean caterpillar Anticarsia gemmatalis (Lepidoptera: Noctuidae). Chemosphere, 259, 127530. https://doi.org/10.1016/j.chemosphere.2020.12
Prajapati, J. N., Patel, S. R., Surani, P. M., & Radadia, G. G. (2018). Agrobiont spiders (Araneae) from five ecosystems of Navsari Agricultural University, Navsari, Gujarat, India. International Journal of Chenical Studies, 6(3), 2547-2550.
Rain, F. F., Howlader, A. J., & Bashar, K. (2016). Diversity and abundance of spider fauna at different habitats of Jahangirnagar University Campus, Bangladesh. Journal of Entomology and Zoology Studies, 4(5), 87-93.
Ramesthagam, P., & Ramasamy, P. (2006). Antioxidant and membrane bound enzymes activity in WSSV-infected Penaeus monodon Fabricius. Aquaculture, 254, 32-39. https://doi.org/10.1016/j.aquaculture.2005.10.011
Rezac, M., Pekar, S., & Jitka, S. (2010). The negative effect of some selective insecticides on the functional response of a potential biological control agent, the spider Philodromus cespitum. Bio Control, 55, 503-510.
Ribeiro, S., Guilhermino, L., Sousa, J. P., & Soares, A. M. V. M. (1999). Novel bioassay based on acetylcholinesterase and lactate dehydrogenase activities to evaluate the toxicity of chemicals to soil isopods. Ecotoxicology and Environmental Safety, 44(3), 287-293. https://doi.org/10.1006/eesa.1999.1837
Riechert, S. E., & Lockley, T. (1984). Spiders as biological control agents. Annual Review of Entomology, 29, 229-320.
Rikans, L. E., & Hornbrook, K. R. (1997). Lipid peroxidation, antioxidant protection and aging. Biochimica et Biophysica Acta, 1362(2-3), 116-127. https://doi.org/10.1016/s0925-4439(97)00067-7
Rodrigues, A. R. S., Siqueira, H. A. A., & Torres, J. B. (2014). Enzymes mediating resistance to lambda-cyhalothrin in Eriopis connexa (Coleoptera: Coccinellidae). Environmental Pollution, 110, 36-43. https://doi.org/10.1016/j.pestbp.2014.02.005
Sandahl, J. F., Baldwin, D. H., Jenkins, J. J., & Scholz, N. L. (2005). Comparative thresholds for acetylcholinesterase inhibition and behavioral impairment in coho salmon exposed to chlorpyrifos. Environmental Toxicology and Chemistry, 24(1), 136-145. https://doi.org/10.1897/04-195r.1
Sarikaya, S. B. O., Topal, F., Şentürk, M., Gülçin, İ., & Supuran, C. T. (2011). In vitro inhibition of α-carbonic anhydrase isozymes by some phenolic compounds. Bioorganic and Medicinal Chemistry Letters, 21(14), 4259-4262. https://doi.org/10.1016/j.bmcl.2011.05.071
Scott-Fordsmand, J. J., & Weeks, J. M. (2000). Biomarkers in earthworms. Reviews of Environmental Contamination and Toxicology, 165, 117-159. https://doi.org/10.1002/etc.5620120510
Serra, R. S., Cossolin, J. F. S., Santos de Resende, M. T. C., de Castro, M. A., Oliveira, A. H., Martínez, L. C., & Serrão, J. E. (2021). Spiromesifen induces histopathological and cytotoxic changes in the midgut of the honeybee Apis mellifera (Hymenoptera: Apidae). Chemosphere, 270, 129439. https://doi.org/10.1016/j.chemosphere.2020.129439
Sessa, L., Calderón-Fernández, G. M., Abreo, E., Altier, N., Mijailovsky, S. J., Girotti, J. R., & Pedrini, N. (2021). Epicuticular hydrocarbons of the redbanded stink bug Piezodorus guildinii (Heteroptera: Pentatomidae): Sexual dimorphism and alterations in insects collected in insecticide-treated soybean crops. Pest Management Science, 77(11), 4892-4902. https://doi.org/10.1002/ps.6528
Shaffo, F. C., Grodzki, A. C., Schelegle, E. S., & Lein, P. J. (2018). The organophosphorus pesticide chlorpyrifos induces sex-specific airway hyperreactivity in adult rats. Toxicological Sciences, 165(1), 244-253. https://doi.org/10.1093/toxsci/kfy158
Sharaf, H. M., Salama, M. A., & Abd El-Atti, M. S. (2013). Biochemical and histological alterations in the digestive gland of the land snail Helicella vestalis (Locard, 1882) exposed to methiocarb and chlorpyrifos in the laboratory. International Journal of Science and Research, 4(7), 2319-7064. https://doi.org/10.4172/2157-7099.1000327
Shivanandappa, T., & Rajendran, S. (1987). Induction of glutathione S-transterase by fumigants in larvae of the Khapra beetle, Trogoderma granarium (E.). Pesticide Biochemistry and Physiology, 28(1), 121-126. https://doi.org/10.1016/0048-3575(87)90120-9
Solanki, R., & Kumar, D. (2014). Effect of pesticides on spider population in cotton agro-system of Vadodara (Gujarat). Journal of Science & Technology, 3(1), 48-52.
Stentiford, G. D., & Feist, S. W. (2005). A histopathological survey of shore crab (Carcinus maenas) and brown shrimp (Crangon crangon) from six estuaries in the United Kingdom. Journal of Invertebrate Pathology, 88, 136-146. https://doi.org/10.1016/j.jip.2005.01.006
Sumon, K. A., Rashid, H., Peeters, E. T., Bosma, R. H., & Van den Brink, P. J. (2018). Environmental monitoring and risk assessment of organophosphate pesticides in aquatic ecosystems of north-west Bangladesh. Chemosphere, 206, 92-100. https://doi.org/10.1016/j.chemosphere.2018.04.167
Tahir, H. M., Khizar, F., Naseem, S., Yaqoob, R., & Samiullah, K. (2016). Insecticide resistance in the ground spider Pardosa sumatra (Thorell, 1890; Araneae: Lycosidae). Insect Biochemistry and Physiology, 93(1), 55-64. https://doi.org/10.1002/arch.21341
Tahir, H. M., Yaqoob, R., Naseem, S., Sherawat, S. M., & Zahra, K. (2015). Effects of insecticides on predatory performance of spiders. Biologia (Pakistan), 61(1), 127-131.
Trabalon, M., Bagnéres, A. G., Hartman, N., & Vallet, A. M. (1996). Change in cuticular compounds composition during the gregarious period and after dispersal of the young in Tegenaria atrica, (Araneae, Agelinidae). Insect Biochemistry and Molecular Biology, 26, 77-84. https://doi.org/10.1016/0965-1748(95)00065-8
Trabalon, M., Bagnères, A. G., & Roland, C. (1997). Contact sex signals in two sympatric spider species, Tegenaria domestica and Tegenaria pagana. Journal of Chemical Ecology, 23, 747-758. https://doi.org/10.1023/B:JOEC.0000006408.60663.db
Trabalon, M., & Garcia, C. F. (2021). Transport pathways of hydrocarbon and free fatty acids to the cuticle in arthropods and hypothetical models in spiders. Comparative Biochemistry and Physiology, Part B, 252, 110541. https://doi.org/10.1016/j.cbpb.2020.110541
US Envirronmental Protection Agency. (2012). Pesticide product label. 2012. “Chlorpyrifos 2.5%”. 12202012. https://www3.epa.gov/pesticides/chem_search/ppls/000829-00292-20121220.pdf
Van den Bossche, P. (1996). Laboratory bioassays of deltamethrin, topically applied, during the hunger cycle of male Glossina tachinoides. Revue d'Elevage et de Medecine Veterinaire des Pays Tropicaux, 49(4), 329-333.
Van Erp, S., Booth, L., Gooneratne, R., & K., O. H. (2002). Sublethal responses of wolf spiders (Lycosidae) to organophosphorous insecticides. Environmental Toxicology, 17, 449-456.
Verma, D. K., Tripathi, R., Das, V. K., & Pandey, R. K. (2020). Histopathological changes in liver and kidney of Heteropneustes fossilis (Bloch) on chlorpyrifos exposure. The Scientific Temper, 11(1-2), 141-147.
Wilczek, G., Babczyńska, A., & Wilczek, P. (2013). Antioxidative responses in females and males of the spider Xerolycosa nemoralis (Lycosidae) exposed to natural and anthropogenic stressors. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 157, 119-131.
Wilczek, G., Babczynska, A., Wilczek, P., Dolezych, B., Migula, P., & Mlynska, H. (2008). Cellular stress reactions assessed by gender and species in spiders from areas variously polluted with heavy metals. Ecotoxicology and Environmental Safety, 70(1), 127-37. https://doi.org/10.1016/j.ecoenv.2007.03.005
World Spider Catalog. (2022). World Spider Catalog. Ver 23.5. (N. H. M. Bern, Ed.).
Wrinn, K. M., Evans, S. C., & Rypstra, A. L. (2012). Predator cues and an herbicide affect activity and emigration in an agrobiont wolf spider. Chemosphere, 87(4), 390-396. https://doi.org/10.1016/j.chemosphere.2011.12.030
Wu, H., Zhang, R., Liu, J., Guo, Y., & Ma, E. (2011). Effects of malathion and chlorpyrifos on acetylcholinesterase and antioxidant defense system in Oxya chinensis (Thunberg) (Orthoptera: Acrididae). Chemosphere, 83(4), 599-604. https://doi.org/10.1016/j.chemosphere.2010.12.004
Yadav, I. C., Devi, N. L., Syed, J. H., Cheng, Z., Li, J., Zhang, G., & Jones, K. C. (2015). Current status of persistent organic pesticides residues in air, water, and soil, and their possible effect on neighboring countries: A comprehensive review of India. Science of the Total Environment, 511, 123-137. https://doi.org/10.1016/j.scitotenv.2014.12.041
Yen, J., Donerly, S., Levin, E. D., & Linney, E. A. (2011). Differential acetylcholinesterase inhibition of chlorpyrifos, diazinon and parathion in larval zebrafish. Neurotoxicology and Teratology, 33(6), 735-741. https://doi.org/10.1016/j.ntt.2011.10.004
Yuan, J., Guo, J., Wang, W., Guo, G., Lian, Q., & Gu, Z. (2019). Acute toxicity of cypermethrin on the juvenile of red claw crayfish Cherax quadricarinatus. Chemosphere, 237, 124468. https://doi.org/10.1016/j.chemosphere.2019.124468
Zhou, C., Zhu, C. X., Fu, H., Li, X., Chen, L., Lin, Y., Lai, Z., & Guo, Y. (2019). Genome-wide investigation of superoxide dismutase (SOD) gene family and their regulatory miRNAs reveal the involvement in abiotic stress and hormone response in tea plant (Camellia sinensis). PLoS One, 14(10), e0223609. https://doi.org/10.1371/journal.pone.0223609
Zhu, F., Gujar, H., Gordon, J., Haynes, K., Potter, M. & Palli, S. (2013). Bed bugs evolved unique adaptive strategy to resist pyrethroid insecticides. Scientific Reports, 3, 1456. https://doi.org/10.1038/srep01456