Contact application of neonicotinoids suppresses the predation rate in different densities of prey and induces paralysis of common farmland spiders

. 2019 Apr 05 ; 9 (1) : 5724. [epub] 20190405

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30952926
Odkazy

PubMed 30952926
PubMed Central PMC6450932
DOI 10.1038/s41598-019-42258-y
PII: 10.1038/s41598-019-42258-y
Knihovny.cz E-zdroje

Neonicotinoids are very effective in controlling crop pests but have adverse effects on predators and pollinators. Spiders are less sensitive to neonicotinoids compared to insects because of the different structure of their acetylcholine receptors, the binding targets of neonicotinoids. We tested whether short-term exposure to neonicotinoids affected the predation rate in different densities of prey of spiders and led to their paralysis or eventual death. To examine these effects, we topically exposed dominant epigeic, epiphytic and sheet-weaving farmland spiders to four widely used neonicotinoids (imidacloprid, thiamethoxam, acetamiprid and thiacloprid). We applied the neonicotinoids at concentrations recommended by the manufacturers for spray application under field conditions. Short-term exposure to the formulations of all four tested neonicotinoids had adverse effects on the predation rate of spiders, with imidacloprid (Confidor) associated with the most severe effects on the predation rate and exhibiting partial acute lethality after one hour (15-32%). Acetamiprid also displayed strong sublethal effects, particularly when applied dorsally to Philodromus cespitum. Day-long exposure to dorsally applied acetamiprid or thiacloprid led to paralysis or death of multiple Linyphiidae spp., with the effects particularly prominent in males. To conclude, we provided multiple lines of evidence that short-term exposure to neonicotinoids, which were applied at recommended field concentrations, caused severe health effects or death in multiple families of spiders. Even acetamiprid caused strong effects, despite being subject to less strict regulations in the European Union, compared with those for imidacloprid because of claims of its negligible off-target toxicity.

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Poletti M, Maia AHN, Omoto C. Toxicity of neonicotinoid insecticides to Neoseiulus californicus and Phytoseiulus macropilis (Acari: Phytoseiidae) and their impact on functional response to Tetranychus urticae (Acari: Tetranychidae) Biol. Contr. 2007;40:30–36. doi: 10.1016/j.biocontrol.2006.09.001. DOI

Prabhaker N, Castle SJ, Naranjo SE, Toscano NC, Morse JG. Compatibility of two systemic neonicotinoids, imidacloprid and thiamethoxam, with various natural enemies of agricultural pests. J. Econ. Entomol. 2011;104:773–781. doi: 10.1603/EC10362. PubMed DOI

He YX, Zhao JW, Zheng Y, Desneux N, Wu KM. 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

Rundlöf M, et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature. 2015;521:77–80. doi: 10.1038/nature14420. PubMed DOI

Stanley DA, et al. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature. 2015;528:548–550. doi: 10.1038/nature16167. PubMed DOI PMC

Tsvetkov N, et al. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science. 2017;356:1395–1397. doi: 10.1126/science.aam7470. PubMed DOI

Woodcock BA, et al. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science. 2017;356:1393–1395. doi: 10.1126/science.aaa1190. PubMed DOI

Desneux N, Decourtye A, Delpuech J-M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 2007;52:81–106. doi: 10.1146/annurev.ento.52.110405.091440. PubMed 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 24th European Congress of Arachnology (eds Nentwig, W., Entling, M. & Kropf, C.) 25–29 (Bern, 2010).

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

Gaafar N, El-Wakeil N, Abdel-Moniem ASH, Volkmar C. Feldstudie zum Nachweis und zur Regulation von Weizenschädlingen und natürlichen Antagonisten. Gesunde Pflanzen. 2014;66:121–128. doi: 10.1007/s10343-014-0325-x. DOI

Douglas MR, Tooker JF. Meta-analysis reveals that seed-applied neonicotinoids and pyrethroids have similar negative effects on abundance of arthropod natural enemies. PeerJ. 2016;4:e2776. doi: 10.7717/peerj.2776. PubMed DOI PMC

Bao HB, Meng XK, Liu ZW. Spider acetylcholine binding proteins: an alternative model to study the interaction between insect nAchRs and neonicotinoids. Insect Biochem. Mol. Biol. 2017;90:82–89. doi: 10.1016/j.ibmb.2017.09.014. PubMed DOI

Meng XK, Zhang YX, Bao HB, Liu ZW. Sequence analysis of insecticide action and detoxification-related genes in the insect pest natural enemy Pardosa pseudoannulata. PLoS One. 2015;10:e0125242. doi: 10.1371/journal.pone.0125242. PubMed DOI PMC

Song F, et al. Specific loops D, E and F of nicotinic acetylcholine receptor β1 subunit may confer imidacloprid selectivity between Myzus persicae and its predatory enemy Pardosa pseudoannulata. Insect Biochem. Mol. Biol. 2009;39:833–841. doi: 10.1016/j.ibmb.2009.09.009. PubMed DOI

Widiarta IN, Matsumura M, Suzuki Y, Nakasuji F. Effects of sublethal doses of imidacloprid on the fecundity of green leafhoppers, Nephotettix spp. (Hemiptera: Cicadellidae) and their natural enemies. Appl. Entomol. Zool. 2001;36:501–507. doi: 10.1303/aez.2001.501. DOI

Uhl P, Bucher R, Schäfer RB, Entling MH. Sublethal effects of imidacloprid on interactions in a tritrophic system of non-target species. Chemosphere. 2015;132:152–158. doi: 10.1016/j.chemosphere.2015.03.027. PubMed DOI

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

Simon-Delso N, et al. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ. Sci. Pollut. Res. Int. 2015;22:5–34. doi: 10.1007/s11356-014-3470-y. PubMed DOI PMC

Cressey D. Neonics vs bees. Nature. 2017;551:156–158. doi: 10.1038/551156a. PubMed DOI

Woodcock BA, et al. Neonicotinoid residues in UK honey despite European Union moratorium. PLoS One. 2018;13:e0189681. doi: 10.1371/journal.pone.0189681. PubMed DOI PMC

Stokstad E. European Union expands ban of three neonicotinoid pesticides. Science, on-line first. 2018 doi: 10.1126/science.aau0152. DOI

Hallmann CA, Foppen RPB, van Turnhout CAM, de Kroon H, Jongejans E. Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature. 2014;511:341–343. doi: 10.1038/nature13531. PubMed DOI

van Dijk TC, van Staaduinen MA, van der Sluijs JP. Macro-invertebrate decline in surface water polluted with imidacloprid. PLoS One. 2013;8:e62374. doi: 10.1371/journal.pone.0062374. 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

Roessink I, Merga LB, Zweers HJ, van den Brink PJ. The neonitonoid imidacloprid shows high chronic toxicity to mayfly nymphs. Environ. Toxicol. Chem. 2013;32:1096–1100. doi: 10.1002/etc.2201. PubMed DOI

Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One. 2012;7:e29268. doi: 10.1371/journal.pone.0029268. PubMed DOI PMC

Bonmatin JM, et al. Environmental fate and exposure; neonicotinoids and fipronil. Environ. Sci. Pollut. Res. Int. 2015;22:35–67. doi: 10.1007/s11356-014-3332-7. PubMed DOI PMC

Botías C, David A, Hill EM, Goulson D. Contamination of wild plants near neonicotinoid seed-treated crops, and implications for non-target insects. Sci. Tot. Environ. 2016;566–567:269–278. doi: 10.1016/j.scitotenv.2016.05.065. PubMed DOI

Müller C. Impacts of sublethal insecticide exposure on insects – Facts and knowledge gaps. Basic App. Ecol. 2018;30:1–10. doi: 10.1016/j.baae.2018.05.001. DOI

Blacquière T, Smagghe G, van Gestel CA, Mommaerts V. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology. 2012;21:973–992. doi: 10.1007/s10646-012-0863-x. PubMed DOI PMC

Henry M, et al. A common pesticide decreases foraging success and survival in honey bees. Science. 2012;336:348–350. doi: 10.1126/science.1215039. PubMed DOI

Williamson SM, Wright GA. Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J. Exp. Biol. 2013;216:1799–1807. doi: 10.1242/jeb.083931. PubMed DOI PMC

Wang SY, et al. Sublethal and transgenerational effects of short-term and chronic exposures to the neonicotinoid nitenpyram on the cotton aphid Aphis gossypii. J. Pest Sci. 2017;90:389–396. doi: 10.1007/s10340-016-0770-7. DOI

Qu Y, et al. Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology. 2015;24:479–487. doi: 10.1007/s10646-014-1396-2. PubMed DOI

Yao F-L, et al. Lethal and sublethal effects of thiamethoxam on the whitefly predator Serangium japonicum (Coleoptera: Coccinellidae) through different exposure routes. Chemosphere. 2015;128:49–55. doi: 10.1016/j.chemosphere.2015.01.010. PubMed DOI

Rondeau G, et al. Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci. Rep. 2014;4:5566. doi: 10.1038/srep05566. PubMed DOI PMC

Dechaume-Moncharmont F-X, Decourtye A, Hennequet-Hantier C, Pons O, Ming-Ha P-D. Statistical analysis of honeybee survival after chronic exposure to insecticides. Environ. Toxicol. Chem. 2003;22:3088–3094. doi: 10.1897/02-578. PubMed DOI

Růžička V. Pavouci České republiky. Pavouk. 2018;43:3–4.

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

Mohammed AAAH, et al. Impact of imidacloprid and natural enemies on cereal aphids: Integration or ecosystem service disruption? Entomol. Gener. 2018;37:47–61.

Kagabu S. Chloronicotinyl insecticides - discovery, application and future perspective. Rev. Toxicol. 1997;1:75–129.

Pistorius J, Bischoff G, Heimbach U, Stähler M. Bee poisoning incidents in Germany in spring 2008 caused by abrasion of active substance from treated seeds during sowing of maize. Julius-Kühn-Archiv. 2009;423:118–126.

Williamson SM, Willis SJ, Wright GA. Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology. 2014;23:1409–1418. doi: 10.1007/s10646-014-1283-x. 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

Moser SE, Obrycki JJ. Non-target effects of neonicotinoid seed treatments; mortality of coccinellid larvae related to zoophytophagy. Biol. Contr. 2009;51:487–492. doi: 10.1016/j.biocontrol.2009.09.001. DOI

Albajes R, López C, Pons X. Predatory fauna in cornfields and response to imidacloprid seed treatment. J. Econ. Entomol. 2003;96:1805–1813. doi: 10.1093/jee/96.6.1805. PubMed DOI

Denno RF, Gratton C, Döbel H, Finke DL. Predation risk affects relative strength of top-down and bottom-up impacts on insect herbivores. Ecology. 2003;84:1032–1044. doi: 10.1890/0012-9658(2003)084[1032:PRARSO]2.0.CO;2. DOI

Goulson D. An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 2013;50:977–987. doi: 10.1111/1365-2664.12111. DOI

Bogya S, Szinetár C, Markó V. Species composition of spider (Araneae) assemblages in apple and pear orchards in Carpathian Basin. Acta Phytopathol. Hung. 1999;34:99–122.

Pekár S. Change in the community of epigeal spiders and harvestmen (Araneae, Opiliones) with the age of an apple orchard. Plant Soil Environ. 2003;49:81–88. doi: 10.17221/4094-PSE. DOI

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

World Spider Catalog. The world spider catalog, version 18.5. Available from, http://www.wsc.nmbe.ch/ (2018).

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