Neonicotinoids are thought to have negligible repellent or anti-feeding effects. Based on our preliminary observations, we hypothesized that the contamination of spider prey with commonly used neonicotinoids has repellent or feeding deterrent effects on spiders. We tested this hypothesis by providing prey treated or not with field-realistic concentrations of neonicotinoids to the spiders and determining the number of (a) killed only and (b) killed and eaten prey. We exposed adult freshly molted and starved Pardosa agrestis, a common agrobiont lycosid species, to flies treated with neonicotinoids (acetamiprid, imidacloprid, thiacloprid and thiamethoxam) at field-realistic concentrations or with distilled water as a control. There were no effects of the exposure of the prey to neonicotinoids on the number of flies captured. However, the spiders consumed less of the prey treated with neonicotinoids compared to the ratio of control prey consumed, which resulted in increased overkilling (i.e., killing without feeding). In female P. agrestis, the overkilling increased from only 2.6% of control flies to 25-45% of neonicotinoid-treated flies. As the spiders avoided consuming the already captured neonicotinoid-treated prey, the sublethal effects of neonicotinoids extend beyond the simple attractivity/deterrence of the prey itself. The present study demonstrated that prey overkilling serves as a physiological response of spiders to the contact with the prey contaminated with agrochemicals. We speculate that primary contact with neonicotinoids during prey capture may play a role in this unexpected behavior.

Charles University 3rd Faculty of Medicine Prague Czech Republic

Crop Research Institute Functional Biodiversity Group Prague Czech Republic

Czech University of Life Sciences Prague Faculty of Agrobiology Food and Natural Resources Prague Czech Republic

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Kessler S, et al. Bees prefer foods containing neonicotinoid pesticides. Nature. 2015;521:74–76. doi: 10.1038/nature14414. PubMed DOI PMC

Easton AH, Goulson D. The neonicotinoid insecticide imidacloprid repels pollinating flies and beetles at field-realistic concentrations. PLoS ONE. 2013;8:e54819. doi: 10.1371/journal.pone.0054819. PubMed DOI PMC

Kostromytska OS, Scharf ME, Buss EA. Behavioral responses of pest mole crickets, Neoscapteriscus spp. (Orthoptera: Gryllotalpidae), to selected insecticides. Pest Manag. Sci. 2018;74:547–556. doi: 10.1002/ps.4732. PubMed DOI

White, G. B. Terminology of insect repellents in Insect repellents: principles, methods and uses (eds Bebboun, M., Frances, S. P. & Strickman, D. 31–46 (Taylor & Francis, Boca Raton, 2007).

Cooperband MF, Allan SA. Effects of different pyrethroids on landing behavior of female Aedes aegypti, Anopheles quedrimaculatus and Culex quiquefasciatus mosquitoes (Diptera: Culicidae) J. Med. Entomol. 2009;46:292–306. doi: 10.1603/033.046.0214. PubMed DOI

Miller JR, Siegert PY, Amimo FA, Walker ED. Designation of chemicals in terms of the locomotor responses they elicit from insects: an update of Dethier et al. (1960) J. Econ. Entomol. 2009;102:2056–2060. doi: 10.1603/029.102.0606. PubMed DOI

Pekár S, Haddad CR. Can agrobiont spiders (Araneae) avoid a surface with pesticide residues? Pest Manag. Sci. 2005;61:1179–1185. doi: 10.1002/ps.1110. PubMed DOI

Foelix RF. Chemosensitive hairs in spiders. J. Morph. 1970;132:313–334. doi: 10.1002/jmor.1051320306. PubMed DOI

Pekár S, Beneš J. Aged pesticide residues are detrimental to agrobiont spiders (Araneae) J. Appl. Entomol. 2008;132:614–622. doi: 10.1111/j.1439-0418.2008.01294.x. DOI

Evans SC, Shaw EM, Rypstra AL. Exposure to glyphosate-based herbicide affects agrobiont predatory arthropod behavior and long-term survival. Ecotoxicology. 2010;19:1249–1257. doi: 10.1007/s10646-010-0509-9. PubMed DOI

Michalková V, Pekár S. How glyphosate altered the behavior of agrobiont spiders (Araneae: Lycosidae) and beetles (Coleoptera: Carabidae) Biol. Control. 2009;51:444–449. doi: 10.1016/j.biocontrol.2009.08.003. DOI

Junker RR, Bretscher S, Dötterl S, Bluthgen N. Phytochemical cues affect hunting-dite choices of a nursery web spider (Pisaura mirabilis) but not a crab spider (Misumena vatia) J. Arachnol. 2011;39:113–117. doi: 10.1636/Hi10-14.1. DOI

Kumar P, Pandit SS, Steppuhn A, Baldwin IT. Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46’s role in a nicotine-mediated antipredator herbivore defense. Proc. Natl. Acad. Sci. USA. 2014;111:1245–1252. doi: 10.1073/pnas.1314848111. PubMed DOI PMC

Fischer A. Chemical communication in spiders – a methodological review. J. Arachnol. 2019;47:1–27. doi: 10.1636/0161-8202-47.1.1. DOI

Salem SA, Matter MM. Relative effects of neem seed oil and Deenate on the cotton leafworm, Spodoptera littoralis Boisd. and the most prevalent predators in cotton fields at Menoufyia Governorate. Bull. Fac. Sci. Cairo Univ. 1991;42:941–952.

Desneux N, Decourtye A, Delpuech J-M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 2007;525:81–106. doi: 10.1146/annurev.ento.52.110405.091440. PubMed DOI

Tietjen W, Cady AB. Sublethal exposure to a neurotoxic pesticide affects activity rhythms and patterns of four spider species. J. Arachnol. 2007;35:396–406. doi: 10.1636/S04-62.1. DOI

Pekár S. Spiders (Araneae) in the pesticide world: an ecotoxicological review. Pest Manag. Sci. 2012;68:1438–1446. doi: 10.1002/ps.3397. PubMed DOI

Pekár S. Predatory characteristics of ant-eating Zodarion spiders (Araneae: Zodariidae): Potential biological control agents. Biol. Control. 2005;34:196–203. doi: 10.1016/j.biocontrol.2005.05.008. DOI

Pekár S. Predatory behavior of two European ant-eating spiders (Araneae, Zodariidae) J. Arachnol. 2004;32:31–41. doi: 10.1636/S02-15. DOI

Maupin JL, Riechert S. Superfluous killing in spiders: a consequence of adaptation to food-limited environments? Behav. Ecol. 2001;12:569–576. doi: 10.1093/beheco/12.5.569. DOI

Riechert, S. E. & Maupin, J. L. Spider effects on prey: tests for superfluous killing in five web-builders) in Proceedings of the 17thEuropean Colloquium of Arachnology, Edinburgh, 1997 (ed. Selden, P.A.) 203–210 (British Arachnological Society, Bucks, 1998).

Samu F, Bíró Z. Functional response, multiple feeding, and wasteful killing in a wolf spider (Araneae: Lycosidae) Eur. J. Entomol. 1993;90:471–476.

Smith, R. B. & Wellington, W. G. The functional response of a juvenile orb-weaving spider in Proceedings of the Ninth International Congress of Arachnology, Panama, 1983 (eds Eberhard, W. G., Lubin, Y. D. & Robinson, B. C.) 275–279 (Smithsonian Institution Press, Washington, D. C., 1986).

Conover RJ. Factors affecting the assimilation of organic matter by zooplankton and the question of superfluous feeding. Limnol. Oceanogr. 1966;11:346–354. doi: 10.4319/lo.1966.11.3.0346. DOI

Mansour F, Heimbach U. Evaluation of lycosid, micryphantid and linyphiid spiders as predators of Rhopalosiphum padi (Hom.: Aphdidae) and their functional response to prey density-laboratory experiments. Entomophaga. 1993;38:79–87. doi: 10.1007/BF02373142. DOI

Benhadi-Marín J, Pereira JA, Sousa JP, Santos SAP. Functional responses of three guilds of spiders: comparing single- and multiprey approaches. Ann. Appl. Biol. 2019;175:202–214. doi: 10.1111/aab.12530. DOI

Pompozzi G, García L, Petráková L, Pekár S. Distinct feeding strategies of generalist and specialist spiders. Ecol. Entomol. 2019;44:129–139. doi: 10.1111/een.12683. DOI

Bernays EA. The value of being a resource specialist: behavioral support for a neural hypothesis. Am. Nat. 1998;151:451–464. doi: 10.1086/286132. PubMed DOI

Bernays EA, Funk DJ. Specialists make faster decisions than generalists: experiments with aphids. Proc. R. Soc. Lond. B. 1999;266:151–156. doi: 10.1098/rspb.1999.0615. DOI

Michalko R, Řežucha R. Top predator’s aggressiveness and mesopredator’s risk-aversion additively determine probability of predation. Behav. Ecol. Sociobiol. 2018;72:105. doi: 10.1007/s00265-018-2520-8. DOI

Michalko R, Pekár S, Entling MH. An updated perspective on spiders as generalist predators in biological control. Oecologia. 2019;189:21–36. doi: 10.1007/s00442-018-4313-1. PubMed DOI

Tahir HM, Butt A. Predatory potential of three hunting spiders inhabiting the rice ecosystems. J. Pest Sci. 2009;82:217–225. doi: 10.1007/s10340-008-0242-9. DOI

Isaia, M., Beikes, S., Paschetta, M., Sarvajayakesevalu, S. & Badino, G. Spiders as potential biological controllers in apple orchards infested by Cydia spp. (Lepidoptera: Tortricidae) in Proceedings of 24thEuropean Congress of Arachnology (eds Nentwig, W., Entling, M. & Kropf, C.) 25–29 (European Society of Arachnology, Bern, 2010).

Kuusk AK, Ekbom B. Feeding habits of lycosid spiders in field habitats. J. Pest Sci. 2012;85:253–260. doi: 10.1007/s10340-012-0431-4. DOI

Pekár S, Michalko R, Loverre P, Líznarová E, Černecká Ľ. Biological control in winter: novel evidence for the importance of generalist predators. J. Appl. Ecol. 2015;52:270–279. doi: 10.1111/1365-2664.12363. DOI

Suenaga H, Hamamura T. Effects of manipulated density of the wolf spider, Pardosa astrigera (Araneae: Lycosidae), on pest populations and cabbage yields: a field enclosure experiment. Appl. Entomol. Zool. 2015;50:89–97. doi: 10.1007/s13355-014-0310-y. DOI

Nentwig, W., Blick, T., Gloor, D., Hänggi, A. & Kropf, C. Spiders of Europe. Available from, http://www.araneae.unibe.ch (2018).

Wehling A, et al. Method for testing effects of plant protection agents on spiders of genus Pardosa (Araneae, Lycosidae) in the laboratory. IOBC Bull. 1998;21:109–117.

Foelix, R. F. Biology of spiders. Oxford University Press, New York (1996).

Kleiber, C. & Zeileis, A. Applied Econometrics with R. Springer-Verlag, New York (2008).

Crawley, M. J. The R book. John Wiley & sons, Chichester (2007).

Řezáč M, Pekár S, Stará J. The negative effect of some selective biocides on the functional response of a potential biological control agent, the spider Philodromus cespitum. BioControl. 2010;55:503–510. doi: 10.1007/s10526-010-9272-3. DOI

El Hassani AK, Dacher M, Gauthier M, Armengaud C. Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera) Pharmacol. Biochem. Behav. 2005;82:30–39. doi: 10.1016/j.pbb.2005.07.008. PubMed DOI

El Hassani AK, Dupuis JP, Gauthier M, Armengaud C. Glutamatergic and GABAergic effects of fipronil on olfactory learning and memory in the honeybee. Invert. Neurosci. 2009;9:91–100. doi: 10.1007/s10158-009-0092-z. PubMed DOI

Colin ME, et al. A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticides. Arch. Environ. Contam. Toxicol. 2004;47:387–395. doi: 10.1007/s00244-004-3052-y. PubMed DOI

Pilling E, Campbell P, Coulson M, Ruddle N, Tornier I. A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam. PLoS ONE. 2013;8:e77193. doi: 10.1371/journal.pone.0077193. PubMed DOI PMC

Řezáč M, Řezáčová V, Heneberg P. Contact application of neonicotinoids suppresses the predation rate in different densities of prey and induces paralysis of common farmland spiders. Sci. Rep. 2019;9:5724. doi: 10.1038/s41598-019-42258-y. PubMed DOI PMC

Smith JA, Pereira RM, Koehler PG. Relative repellency and lethality of the neonicotinoids thiamethoxam and acetamiprid and an acetamiprid/bifenthrin combination to Reticulitermes flavipes termites. J. Econ. Entomol. 2008;101:1881–1887. doi: 10.1603/0022-0493-101.6.1881. PubMed DOI

Rust MK, Saran RK. Toxicity, repellency, and effects of acetamiprid on western subterranean termite (Isoptera: Rhinotermitidae) J. Econ. Entomol. 2008;101:1360–1366. doi: 10.1093/jee/101.4.1360. PubMed DOI

Thompson HM, Wilkins S, Harkin S, Milner S, Walters KFAW. Neonicotinoids and bumblebees (Bombus terrestris): effects on nectar consumption in individual workers. Pest Manag. Sci. 2015;71:946–950. doi: 10.1002/ps.3868. PubMed DOI

Drinkwater TW. Comparison of imidacloprid with carbamate insecticides, and the role of planting depth in the control of false wireworms, Somaticus species, in maize. Crop Protect. 1994;13:341–345. doi: 10.1016/0261-2194(94)90048-5. DOI

Marklund SK, et al. Influence of imidacloprid, a chloronicotinyl insecticide, on host choice and movement patterns of Bemisia argentifolii (Homoptera: Aleyrodidae) on cantaloupe plants (Cucumis melo L.) J. Kansas Entomol. Soc. 2003;76:672–675.

Miranda MP, Yamamoto PT, Garcia RB, Lopes JPA, Lopes JRS. Thiamethoxam and imidacloprid drench applications on sweet orange nursery trees disrupt the feeding and settling behavior of Diaphorina citri (Hemiptera: Liviidae) Pest Manag. Sci. 2016;72:1785–1793. doi: 10.1002/ps.4213. PubMed DOI

Nyman A-M, Hintermeister A, Schirmer K, Ashauer R. The insecticide imidacloprid causes mortality of the freshwater amphipod Gammarus pulex by interfering with feeding behavior. PLoS ONE. 2013;8:e62472. doi: 10.1371/journal.pone.0062472. PubMed DOI PMC

Azevedo-Pereira HVS, Lemos ML, Soares AVM. Behaviour and growth of Chironomus riparius Meigen (Diptera: Chironomidae) under imidacloprid pulse and constant exposure scenarios. Water Air Soil Pollut. 2011;219:215–224. doi: 10.1007/s11270-010-0700-x. DOI

Alexander AC, Culp JM, Liber K, Cessna AJ. Effects of insecticide exposure on feeding inhibition in mayflies and oligochaetes. Environ. Toxicol. Chem. 2007;26:1726–1732. doi: 10.1897/07-015R.1. PubMed DOI

Nauen R. Behaviour modifying effects of low systemic concentrations of imidacloprid on Myzus persicae with special reference to an antifeeding response. Pestic. Sci. 1995;44:145–153. doi: 10.1002/ps.2780440207. DOI

Nauen R, Koob B, Elbert A. Antifeedant effects of sublethal dosages of imidacloprid on Bemisia tabaci. Entomol. Exp. Applic. 1998;88:287–293. doi: 10.1046/j.1570-7458.1998.00373.x. DOI

Poland TM, Haack RA, Bauer LS. Laboratory evaluation of the toxicity of systemic insecticides for control of Anoplophora glabripennis and Plectrodera scalator (Coleoptera: Cerambycidae) J. Econ. Entomol. 2006;99:85–93. doi: 10.1603/0022-0493(2006)099[0085:LEOTTO]2.0.CO;2. PubMed DOI

He Y, Zhao K, Zheng Y, Desneux N, Wu K. Lethal effect of imidacloprid on the coccinellid predator Serangium japonicum and sublethal effects on predator voracity and on functional response to the whitefly Bemisia tabaci. Ecotoxicology. 2012;21:1291–1300. doi: 10.1007/s10646-012-0883-6. PubMed DOI

Neumann, N. Lethal and sublethal effects of insecticides on mortality, migration and host searching behaviour of tersilochine parasitoids on winter oilseed rape. PhD thesis, University of Göttingen (2010).

Gharalari AH, et al. Knockdown mortality, repellency, and residual effects of insecticides for control of adult Bactericera cockerelli (Hemiptera: Psyllidae) J. Econ. Entomol. 2009;102:1032–1038. doi: 10.1603/029.102.0322. PubMed DOI

Iqbal N, Evans TA. Evaluation of fipronil and imidacloprid as bait active ingredients against fungus-growing termites (Blattodea: Termitidae: Macrotermitinae) Bull. Entomol. Res. 2018;108:14–22. doi: 10.1017/S000748531700044X. PubMed DOI

Gahlhoff JE, Jr., Koehler PG. Penetration of the eastern subterranean termite into soil treated at various thicknesses and concentrations of Dursban TC and Premise 75. J. Econ. Entomol. 2001;94:486–491. doi: 10.1603/0022-0493-94.2.486. PubMed DOI

Tison L, et al. Honey bees’ behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field. Environ. Sci. Technol. 2016;50:7218–7227. doi: 10.1021/acs.est.6b02658. PubMed DOI

van Herk WG, et al. Contact behavior and mortality of wireworms exposed to six classes of insecticide applied to wheat seed. J. Pest Sci. 2015;88:717–739. doi: 10.1007/s10340-015-0697-4. DOI

Mason G, Rancati M, Bosco D. The effect of thiamethoxam, a second generation neonicotinoid insecticide, in preventing transmission of tomato yellow leaf curl geminivirus (TYLCV) by the whitefly Bemisia tabaci (Gennadius) Crop Protect. 2000;19:473–479. doi: 10.1016/S0261-2194(00)00042-9. DOI

Remmen LN, Su NY. Tunneling and mortality of eastern and Formosan subterranean termites (Isoptera: Rhinotermitidae) in sand treated with thiamethoxam or fipronil. J. Econ. Entomol. 2005;98:906–910. doi: 10.1603/0022-0493-98.3.906. PubMed DOI

Low concentrations of acetamiprid, deltamethrin, and sulfoxaflor, three commonly used insecticides, adversely affect ant queen survival and egg laying

The sublethal effects of neonicotinoids on spiders are independent of their nutritional status

Neonicotinoids suppress contact chemoreception in a common farmland spider