Neonicotinoids suppress contact chemoreception in a common farmland spider

. 2020 Apr 27 ; 10 (1) : 7019. [epub] 20200427

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32341403
Odkazy

PubMed 32341403
PubMed Central PMC7184746
DOI 10.1038/s41598-020-63955-z
PII: 10.1038/s41598-020-63955-z
Knihovny.cz E-zdroje

Neonicotinoid insecticides are increasingly recognized for their role as information disruptors by modifying the chemical communication system of insects and therefore decreasing the chances of reproduction in target insects. However, data from spiders are lacking. In the present study, we tested the responses of males of a common agrobiont spider, Pardosa agrestis, to the application of field-realistic concentration of acetamiprid, which was formulated as Mospilan, and trace amounts of thiacloprid, which was formulated as Biscaya. We applied fresh or 24-h-old residues of Mospilan or Biscaya to the males just prior to the experiment or treated only the surface of a tunnel containing female draglines. We evaluated the ability of the males to recognize female cues from female dragline silk in a Y-maze. The field-realistic, sublethal doses of Mospilan altered pheromone-guided behavior. The choice of the tunnel with female draglines by males was hampered by tarsal treatment of the males with 24 h-old residues of Mospilan. The mating dance display was commonly initiated in control males that came into contact with female draglines and was suppressed by the Mospilan treatments in all three experimental settings. Some males only initiated the mating dance but did not manage to complete it; this was particularly true for males that were treated tarsally with fresh Mospilan residues, as none of these males managed to complete the mating dance. All three experimental settings with Mospilan decreased the frequency of males that managed to both select the tunnel with female draglines and complete the mating dance. The responses to the low-dose Biscaya were much milder and the study was not sufficiently powered to confirm the effects of Biscaya; however, the surprisingly observed trends in responses to very low Biscaya concentrations call for further analyses of long-term effects of trace amounts of neonicotinoids on the pheromone-guided behavior of spiders. These are the first conclusive data regarding the effects of commercially available formulations of neonicotinoid insecticides on the intraspecific chemical communication of spiders.

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Hedgekar BM, Dondale CD. A contact sex pheromone and some response parameters in lycosid spiders. Can. J. Zool. 1969;47:1–4. doi: 10.1139/z69-001. DOI

Schulz S. Semiochemistry of spiders. Adv. Insect Chem. Ecol. 2004;1:110–150. doi: 10.1017/CBO9780511542664.005. DOI

Gaskett AC. Spider sex pheromones: emission, reception, structures, and functions. Biol. Rev. Camb. Philos. Soc. 2007;82:27–48. doi: 10.1111/j.1469-185X.2006.00002.x. PubMed DOI

Beyer M, Czaczkes TJ, Tuni C. Does silk mediate chemical communication between the sexes in a nuptial feeding spider? Behav. Ecol. Sociobiol. 2018;72:49. doi: 10.1007/s00265-018-2454-1. DOI

Baruffaldi L, Costa FG, Rodríguez A, González A. Chemical communication in Schizocosa malitiosa: evidence of a female contact sex pheromone and persistence in the field. J. Chem. Ecol. 2010;36:759–767. doi: 10.1007/s10886-010-9819-x. PubMed DOI

Roberts JA, Uetz GW. Information content of female chemical signals in the wolf spider, Schizocosa ocreata: male discrimination of reproductive state and receptivity. Anim. Behav. 2005;70:217–223. doi: 10.1016/j.anbehav.2004.09.026. DOI

Rypstra AL, Schlosser AM, Sutton PL, Persons MH. Multimodal signaling: the relative importance of chemical and visual cues from females to the behavior of male wolf spiders (Lycosidae) Anim. Behav. 2009;77:937–947. doi: 10.1016/j.anbehav.2008.12.026. DOI

Stoltz JA, McNeil JN, Andrade MCB. Males assess chemical signals to discriminate just-mated females from virgins in redback spiders. Anim. Behav. 2007;74:1669–1674. doi: 10.1016/j.anbehav.2007.03.011. DOI

Bradbury, J. W. & Vehrencamp, S. L. Principles of animal communication (Sinauer, Sunderland, 2011).

Foelix RF, Chu-Wang I. The morphology of spider sensilla II. Chemoreceptors. Tissue Cell. 1973;5:461–478. doi: 10.1016/S0040-8166(73)80038-2. PubMed DOI

Kronestedt T. Study on chemosensitive hairs in wolf spiders (Araneae, Lycosidae) by scanning electron microscopy. Zool. Scripta. 1979;8:279–285. doi: 10.1111/j.1463-6409.1979.tb00639.x. DOI

Bell RD, Roberts JA. Trail-following behavior by males of the wolf spider, Schizocosa ocreata (Hentz) J. Ethol. 2017;35:29–36. doi: 10.1007/s10164-016-0486-4. DOI

Uhl, G. & Elias, D. O. Communication in Spider behavior: flexibility and versatility (ed. Herberstein, M. E.) 127–189 (Cambridge University Press, New York, 2011).

Schulz S. Spider pheromones – a structural perspective. J. Chem. Ecol. 2013;39:1–14. doi: 10.1007/s10886-012-0231-6. PubMed DOI

Trabalon, M. Chemical communication and contact cuticular compounds in spiders in Spider ecophysiology (ed. Nentwig, W.) 125–140 (Springer, Berlin, 2013).

Searcy LE, Rypstra AL, Persons MH. Airborne chemical communication in the wolf spider Pardosa milvina. J. Chem. Ecol. 1999;25:2527–2533. doi: 10.1023/A:1020878225553. DOI

Leccia F, et al. Disruption of the chemical communication of the European agrobiont ground-dwelling spider Pardosa agrestis by pesticides. J. Appl. Entomol. 2016;140:609–616. doi: 10.1111/jen.12288. DOI

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

Benamú M, et al. Nanostructural and mechanical property changes to spider silk as a consequence of insecticide exposure. Chemosphere. 2017;181:241–249. doi: 10.1016/j.chemosphere.2017.04.079. PubMed DOI

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

Chiarle A, Kronestedt T, Isaia M. Courtship behavior in European species of the genus Pardosa (Araneae, Lycosidae) J. Arachnol. 2013;41:108–125. doi: 10.1636/Hi12-09.1. DOI

Rabhi KK, et al. Low doses of a neonicotinoid insecticide modify pheromone response of central but not peripheral olfactory neurons in a pest insect. Proc. Biol. Sci. 2016;283:20152987. doi: 10.1098/rspb.2015.2987. PubMed DOI PMC

Moffat C, et al. Neonicotinoids target distinct nicotinic acetylcholine receptors and neurons, leading to differential risks to bumblebees. Sci. Rep. 2016;6:24764. doi: 10.1038/srep24764. PubMed DOI PMC

Andrione M, Vallortigara G, Antolini R, Haase A. Neonicotinoid-induced impairment of odour coding in the honeybee. Sci. Rep. 2016;6:38110. doi: 10.1038/srep38110. PubMed DOI PMC

Schott M, et al. Temporal dynamics of whole body residues of the neonicotinoid insecticide imidacloprid in live or dead honeybees. Sci. Rep. 2017;7:6288. doi: 10.1038/s41598-017-06259-z. PubMed DOI PMC

Moffat C, et al. Chronic exposure to neonicotinoids increases neuronal vulnerability to mitochondrial dysfunction in the bumblebee (Bombus terrestris) FASEB J. 2015;29:2112–2119. doi: 10.1096/fj.14-267179. PubMed DOI PMC

Rabhi KK, et al. Unexpected effects of low doses of a neonicotinoid insecticide on behavioral responses to sex pheromone in a pest insect. PLoS ONE. 2014;9:e114411. doi: 10.1371/journal.pone.0114411. PubMed DOI PMC

Lürling M, Scheffer M. Info-disruption: pollution and the transfer of chemical information between organisms. Trends Ecol. Evol. 2007;22:374–379. doi: 10.1016/j.tree.2007.04.002. PubMed DOI

Zhou H, Du J, Huang Y. Effects of sublethal doses of malathion on responses to sex pheromones by male Asian corn borer moths, Ostrinia furnacalis (Guenée) J. Chem. Ecol. 2005;31:1645–1656. doi: 10.1007/s10886-005-5804-1. PubMed DOI

Wei H, Du J. Sublethal effects of larval treatment with deltamethrin on moth sex pheromone communication system of the Asian corn borer, Ostrinia furnacalis. Pest Biochem. Physiol. 2004;80:12–20. doi: 10.1016/j.pestbp.2004.05.001. DOI

Lalouette L, et al. Unexpected effects of sublethal doses of insecticide on the peripheral olfactory response and sexual behavior in a pest insect. Environ. Sci. Pollut. Res. Int. 2016;23:3073–3085. doi: 10.1007/s11356-015-5923-3. PubMed DOI

Wang DS, Lu LH, He YR. Effects of insecticides on sex pheromone communication and mating behavior in Trichogramma chilonis. J. Pest Sci. 2018;91:65–78. doi: 10.1007/s10340-017-0864-x. DOI

Müller T, Römer CI, Müller C. Parental sublethal insecticide exposure prolongs mating response and decreases reproductive output in offspring. J. Appl. Ecol. 2019;56:1528–1537. doi: 10.1111/1365-2664.13398. DOI

Delpuech J-M, et al. Inhibition of sex pheromone communications of Trichogramma brassicae (Hymenoptera) by the insecticide chlorpyrifos. Environ. Toxicol. Chem. 1998;17:1107–1113. doi: 10.1002/etc.5620170617. DOI

Delpuech J-M, Gareau E, Terrier O, Fouillet P. Sublethal effects of the insecticide chlorpyrifos on the sex-pheromonal communication of Trichogramma brassicae. Chemosphere. 1998;36:1775–1785. doi: 10.1016/S0045-6535(97)10071-6. DOI

Tappert L, Pokorny T, Hofferberth J, Ruther J. Sublethal doses of imidacloprid disrupt sexual communication and host finding in a parasitoid wasp. Sci. Rep. 2017;7:42756. doi: 10.1038/srep42756. PubMed DOI PMC

Navarro-Roldán MA, Gemeno C. Sublethal effects of neonicotinoid insecticide on calling behavior and pheromone production of tortricid moths. J. Chem. Ecol. 2017;43:881–890. doi: 10.1007/s10886-017-0883-3. PubMed DOI

Kremer AN, King BH. A neonicotinoid affects the mating behavior of Spalangia endius (Hymenoptera: Pteromalidae), a biological control agent of filth flies. Environ. Entomol. 2019;48:489–495. doi: 10.1093/ee/nvz015. PubMed DOI

Navarro-Roldán MA, Amat C, Bau J, Gemeno C. Extremely low neonicotinoid doses alter navigation of pest insects along pheromone plumes. Sci. Rep. 2019;9:8150. doi: 10.1038/s41598-019-44581-w. PubMed DOI PMC

Young, H. K., Denecke, S. M., Robin, C. & Fournier-Level, A. Sublethal larval exposure to imidacloprid impacts adult behavior in Drosophila melanogaster. J. Evol. Biol.33, 51–64 (2020). PubMed

Korenko S, Saska P, Kysilková K, Řezáč M, Heneberg P. Prey contaminated with neonicotinoids induces feeding deterrent behavior of a common farmland spider. Sci. Rep. 2019;9:15895. doi: 10.1038/s41598-019-52302-6. PubMed DOI PMC

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