Risk assessment requires several bee species to address species-specific sensitivity to insecticides at field-realistic concentrations.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
18 Dec 2023
18 Dec 2023
Historique:
received:
24
05
2023
accepted:
30
11
2023
medline:
19
12
2023
pubmed:
19
12
2023
entrez:
18
12
2023
Statut:
epublish
Résumé
In the European registration process, pesticides are currently mainly tested on the honey bee. Since sensitivity data for other bee species are lacking for the majority of xenobiotics, it is unclear if and to which extent this model species can adequately serve as surrogate for all wild bees. Here, we investigated the effects of field-realistic contact exposure to a pyrethroid insecticide, containing lambda-cyhalothrin, on seven bee species (Andrena vaga, Bombus terrestris, Colletes cunicularius, Osmia bicornis, Osmia cornuta, Megachile rotundata, Apis mellifera) with different life history characteristics in a series of laboratory trials over two years. Our results on sensitivity showed significant species-specific responses to the pesticide at a field-realistic application rate (i.e., 7.5 g a.s./ha). Species did not group into distinct classes of high and low mortality. Bumble bee and mason bee survival was the least affected by the insecticide, and M. rotundata survival was the most affected with all individuals dead 48 h after application. Apis mellifera showed medium mortality compared to the other bee species. Most sublethal effects, i.e. behavioral abnormalities, were observed within the first hours after application. In some of the solitary species, for example O. bicornis and A. vaga, a higher percentage of individuals performed some abnormal behavior for longer until the end of the observation period. While individual bee weight explained some of the observed mortality patterns, differences are likely linked to additional ecological, phylogenetic or toxicogenomic parameters as well. Our results support the idea that honey bee data can be substitute for some bee species' sensitivity and may justify the usage of safety factors. To adequately cover more sensitive species, a larger set of bee species should be considered for risk assessment.
Identifiants
pubmed: 38110412
doi: 10.1038/s41598-023-48818-7
pii: 10.1038/s41598-023-48818-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
22533Informations de copyright
© 2023. The Author(s).
Références
Biesmeijer, J. C. et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354 (2006).
doi: 10.1126/science.1127863
pubmed: 16857940
Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, e0185809. https://doi.org/10.1371/journal.pone.0185809 (2017).
doi: 10.1371/journal.pone.0185809
pubmed: 29045418
pmcid: 5646769
Seibold, S. et al. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574, 671–674. https://doi.org/10.1038/s41586-019-1684-3 (2019).
doi: 10.1038/s41586-019-1684-3
pubmed: 31666721
Sánchez-Bayo, F. & Wyckhuys, K. A. Worldwide decline of the entomofauna: A review of its drivers. Biol. Conserv. 232, 8–27. https://doi.org/10.1016/j.biocon.2019.01.020 (2019).
doi: 10.1016/j.biocon.2019.01.020
Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957. https://doi.org/10.1126/science.1255957 (2015).
doi: 10.1126/science.1255957
pubmed: 25721506
Boyle, N. K. et al. Workshop on pesticide exposure assessment paradigm for non-Apis bees: Foundation and summaries. Environ. Entomol. 48, 4–11. https://doi.org/10.1093/ee/nvy103 (2019).
doi: 10.1093/ee/nvy103
pubmed: 30508116
Hinarejos, S. et al. Non-Apis bee exposure workshop: Industry participants’ view. Environ. Entomol. 48, 49–52. https://doi.org/10.1093/ee/nvy138 (2019).
doi: 10.1093/ee/nvy138
pubmed: 30517593
Potts, S. G. et al. Global pollinator declines: Trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353. https://doi.org/10.1016/j.tree.2010.01.007 (2010).
doi: 10.1016/j.tree.2010.01.007
pubmed: 20188434
Klein, A.-M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313. https://doi.org/10.1098/rspb.2006.3721 (2007).
doi: 10.1098/rspb.2006.3721
pubmed: 17164193
Garibaldi, L. A. et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611. https://doi.org/10.1126/science.1230200 (2013).
doi: 10.1126/science.1230200
pubmed: 23449997
European Food Safety Authority. EFSA guidance document on the risk assessment of plant protection products on bees (Apis mellifera, Bumbus spp. and solitary bees). EFSA J. 11, 3295. https://doi.org/10.2903/j.efsa.2013.3295 (2013).
doi: 10.2903/j.efsa.2013.3295
Hladik, M. L., Vandever, M. & Smalling, K. L. Exposure of native bees foraging in an agricultural landscape to current-use pesticides. Sci. Total Environ. 542, 469–477. https://doi.org/10.1016/j.scitotenv.2015.10.077 (2016).
doi: 10.1016/j.scitotenv.2015.10.077
pubmed: 26520270
Heard, M. S. et al. Comparative toxicity of pesticides and environmental contaminants in bees: Are honey bees a useful proxy for wild bee species?. Sci. Total Environ. 578, 357–365. https://doi.org/10.1016/j.scitotenv.2016.10.180 (2017).
doi: 10.1016/j.scitotenv.2016.10.180
pubmed: 27847190
Dietzsch, A. C. & Jütte, T. Non-Apis bees as model organisms in laboratory, semi-field and field experiments. J. Kulturpflanzen 72, 162–172. https://doi.org/10.5073/JFK.2020.05.06 (2020).
doi: 10.5073/JFK.2020.05.06
Cane, J. H. Estimation of bee size using intertegular span (Apoidea). J. Kansas Entomol. Soc. 60, 145–147 (1987).
Gathmann, A. & Tscharntke, T. Foraging ranges of solitary bees. J. Anim. Ecol. 71, 757–764. https://doi.org/10.1046/j.1365-2656.2002.00641.x (2002).
doi: 10.1046/j.1365-2656.2002.00641.x
Kim, J.-Y. Female size and fitness in the leaf-cutter bee Megachile apicalis. Ecol. Entomol. 22, 275–282. https://doi.org/10.1046/j.1365-2311.1997.00062.x (1997).
doi: 10.1046/j.1365-2311.1997.00062.x
Thompson, H. M. Extrapolation of acute toxicity across bee species. Integr. Environ. Assess. Manag. 12, 622–626. https://doi.org/10.1002/ieam.1737 (2016).
doi: 10.1002/ieam.1737
pubmed: 26595163
Sgolastra, F. et al. Pesticide exposure assessment paradigm for solitary bees. Environ. Entomol. 48, 22–35. https://doi.org/10.1093/ee/nvy105 (2019).
doi: 10.1093/ee/nvy105
pubmed: 30508080
Roubik, D. W. (ed.) Pollinator Safety in Agriculture (Food and Agriculture Organization of the United Nations, 2014).
Julius Kühn-Institut. Wirkstoffmengen Apfel 2019. lambda-Cyhalothrin (2019). Available at https://papa.julius-kuehn.de/index.php?menuid=54&reporeid=349 .
Julius Kühn-Institut. Wirkstoffmengen Winterraps 2019. lambda-Cyhalothrin (2019). Available at https://papa.julius-kuehn.de/index.php?menuid=54&reporeid=361 .
European Food Safety Authority. Conclusion on the peer review of the pesticide risk assessment of the active substance lambda-cyhalothrin. EFSA J. 12, 3677. https://doi.org/10.2903/j.efsa.2014.3677 (2014).
doi: 10.2903/j.efsa.2014.3677
Schmolke, A. et al. Assessment of the vulnerability to pesticide exposures across bee species. Environ. Toxicol. Chem. 40, 2640–2651. https://doi.org/10.1002/etc.5150 (2021).
doi: 10.1002/etc.5150
pubmed: 34197661
Westrich, P. Die Wildbienen Deutschlands 2nd edn. (Verlag Eugen Ulmer, 2019).
Amiet, F. & Krebs, A. Bienen Mitteleuropas. Gattungen, Lebensweise, Beobachtung 3rd edn. (Haupt Verlag, 2019).
Tschanz, P., Vogel, S., Walter, A., Keller, T. & Albrecht, M. Nesting of ground-nesting bees in arable fields is not associated with tillage system per se, but with distance to field edge, crop cover, soil and landscape context. J. Appl. Ecol. 60, 158–169. https://doi.org/10.1111/1365-2664.14317 (2023).
doi: 10.1111/1365-2664.14317
Wernecke, A., Frommberger, M., Forster, R. & Pistorius, J. Lethal effects of various tank mixtures including insecticides, fungicides and fertilizers on honey bees under laboratory, semi-field and field conditions. J. Consum. Prot. Food Saf. 14, 239–249. https://doi.org/10.1007/s00003-019-01233-5 (2019).
doi: 10.1007/s00003-019-01233-5
Wernecke, A., Eckert, J. H., Forster, R., Kurlemann, N. & Odemer, R. Inert agricultural spray adjuvants may increase the adverse effects of selected insecticides on honey bees (Apis mellifera L.) under laboratory conditions. J. Plant Dis. Prot. 129, 93–105. https://doi.org/10.1007/s41348-021-00541-z (2022).
doi: 10.1007/s41348-021-00541-z
OECD. Test No. 214: Honeybees, acute contact toxicity test. In OECD Guidelines for the Testing of Chemicals (Organisation for Economic Co-operation and Development, 1998).
OECD. Test No. 246: Bumblebee, acute contact toxicity test. In OECD Guidelines for the Testing of Chemicals (Organisation for Economic Co-operation and Development, 2017).
OECD. Test No. 245: Honey bee (Apis mellifera L.) chronic oral toxicity test (10-day feeding) In OECD Guidelines for the Testing of Chemicals (Organisation for Economic Co-operation and Development, 2017).
Uhl, P., Awanbor, O., Schulz, R. S. & Brühl, C. A. Is Osmia bicornis an adequate regulatory surrogate? Comparing its acute contact sensitivity to Apis mellifera. PLoS ONE 14, e0201081. https://doi.org/10.1371/journal.pone.0201081 (2019).
doi: 10.1371/journal.pone.0201081
pubmed: 31393875
pmcid: 6687126
Roessink, I. et al. (eds) Solitary Bee, Acute Contact Toxicity Test. Version: March 2016 (ICPPR workgroup non-Apis bees, 2016).
Therneau, T. M. coxme: Mixed-Effects Cox Models. R package coxme version 2.2–18.1 (2022). https://cran.ms.unimelb.edu.au/web/packages/coxme/ .
Stel, V. S., Dekker, F. W., Tripepi, G., Zoccali, C. & Jager, K. J. Survival analysis II: Cox regression. Nephron Clin. Pract. 119, c255–c260. https://doi.org/10.1159/000328916 (2011).
doi: 10.1159/000328916
pubmed: 21921637
Lenth, R. V. Confidence Intervals and Tests in Emmeans. Emmeans: Estimated Marginal Means, Aka Least-Squares Means; R package version 1.8.2 (2022).
Pipper, C. B., Ritz, C. & Bisgaard, H. A versatile method for confirmatory evaluation of the effects of a covariate in multiple models. J. R. Stat. Soc. C Appl. Stat. 61, 315–326. https://doi.org/10.1111/j.1467-9876.2011.01005.x (2012).
doi: 10.1111/j.1467-9876.2011.01005.x
Dosch, C. et al. The gut microbiota can provide viral tolerance in the honey bee. Microorganisms 9, 871. https://doi.org/10.3390/microorganisms9040871 (2021).
doi: 10.3390/microorganisms9040871
pubmed: 33920692
pmcid: 8072606
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2022).
Therneau, T. M. A Package for Survival Analysis in R. R package version 3.4–0 (2022). https://CRAN.R-project.org/package=survival .
Lenth, R. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.8.2 (2022). https://CRAN.R-project.org/package=emmeans .
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).
doi: 10.1007/978-3-319-24277-4
Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.4.6 (2022). https://CRAN.R-project.org/package=DHARMa .
Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated Generalized Linear Mixed Modeling. R J. 9, 378–400. https://doi.org/10.32614/RJ-2017-066 (2017).
doi: 10.32614/RJ-2017-066
Wood, S. & Scheipl, F. gamm4: Generalized Additive Mixed Models using ‘mgcv’ and ‘lme4’. R package version 0.2–6 (2020). https://CRAN.R-project.org/package=gamm4 .
Auguie, B. gridExtra: Miscellaneous Functions for “Grid” Graphics. R package version 2.3 (2017).
Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biometric. J. 50, 346–363 (2008).
doi: 10.1002/bimj.200810425
Kassambara, A. ggpubr: ‘ggplot2’ Based Publication Ready Plots. R package version 0.6.0 (2023).
Wernecke, A. et al. A selected organosilicone spray adjuvant does not enhance lethal effects of a pyrethroid and carbamate insecticide on honey bees. Front. Physiol. 14, 1171817. https://doi.org/10.3389/fphys.2023.1171817 (2023).
doi: 10.3389/fphys.2023.1171817
pubmed: 37324382
pmcid: 10267468
O’Reilly, A. D. & Stanley, D. A. Non-neonicotinoid pesticides impact bumblebee activity and pollen provisioning. J. Appl. Ecol. 60, 1673–1683. https://doi.org/10.1111/1365-2664.14444 (2023).
doi: 10.1111/1365-2664.14444
O’Reilly, A. D. & Stanley, D. A. Solitary bee behaviour and pollination service delivery is differentially impacted by neonicotinoid and pyrethroid insecticides. Sci. Total Environ. 894, 164399. https://doi.org/10.1016/j.scitotenv.2023.164399 (2023).
doi: 10.1016/j.scitotenv.2023.164399
pubmed: 37245806
Thompson, H. Behavioural effects of pesticides in bees - their potential for use in risk assessment. Ecotoxicology 12, 317–330 (2003).
doi: 10.1023/A:1022575315413
pubmed: 12739878
Tosi, S., Sfeir, C., Carnesecchi, E., van Engelsdorp, D. & Chauzat, M.-P. Lethal, sublethal, and combined effects of pesticides on bees: a meta-analysis and new risk assessment tools. Sci. Total Environ. 844, 156857. https://doi.org/10.1016/j.scitotenv.2022.156857 (2022).
doi: 10.1016/j.scitotenv.2022.156857
pubmed: 35760183
Chmiel, J. A., Daisley, B. A., Pitek, A. P., Thompson, G. J. & Reid, G. Understanding the effects of sublethal pesticide exposure on honey bees: A role for probiotics as mediators of environmental stress. Front. Ecol. Evol. 8, 22. https://doi.org/10.3389/fevo.2020.00022 (2020).
doi: 10.3389/fevo.2020.00022
Uhl, P. et al. Interspecific sensitivity of bees towards dimethoate and implications for environmental risk assessment. Sci. Rep. 6, 34439. https://doi.org/10.1038/srep34439 (2016).
doi: 10.1038/srep34439
pubmed: 27686060
pmcid: 5043368
Pamminger, T. Extrapolating acute contact bee sensitivity to insecticides based on body weight using a phylogenetically informed interspecies scaling framework. Environ. Toxicol. Chem. 40, 2044–2052. https://doi.org/10.1002/etc.5045 (2021).
doi: 10.1002/etc.5045
pubmed: 33749874
Lourencetti, A. P. S., Azevedo, P., Miotelo, L., Malaspina, O. & Nocelli, R. C. F. Surrogate species in pesticide risk assessments: Toxicological data of three stingless bees species. Environ. Pollut. 318, 120842. https://doi.org/10.1016/j.envpol.2022.120842 (2023).
doi: 10.1016/j.envpol.2022.120842
pubmed: 36509344
Kueh Tai, F. et al. Honey bee toxicological responses do not accurately predict environmental risk of imidacloprid to a solitary ground-nesting bee species. Sci. Total Environ. 839, 156398. https://doi.org/10.1016/j.scitotenv.2022.156398 (2022).
doi: 10.1016/j.scitotenv.2022.156398
pubmed: 35654201
Ansell, G. R., Frewin, A. J., Gradish, A. E. & Scott-Dupree, C. D. Contact toxicity of three insecticides for use in tier I pesticide risk assessments with Megachile rotundata (Hymenoptera: Megachilidae). PeerJ 9, e10744. https://doi.org/10.7717/peerj.10744 (2021).
doi: 10.7717/peerj.10744
pubmed: 33665008
pmcid: 7908870
Linguadoca, A. et al. Intra-specific variation in sensitivity of Bombus terrestris and Osmia bicornis to three pesticides. Sci. Rep. 12, 17311. https://doi.org/10.1038/s41598-022-22239-4 (2022).
doi: 10.1038/s41598-022-22239-4
pubmed: 36243795
pmcid: 9569340
Haas, J. et al. Phylogenomic and functional characterization of an evolutionary conserved cytochrome P450-based insecticide detoxification mechanism in bees. Proc. Natl. Acad. Sci. U.S.A. 119, e2205850119. https://doi.org/10.1073/pnas.2205850119 (2022).
doi: 10.1073/pnas.2205850119
pubmed: 35733268
pmcid: 9245717
Mokkapati, J. S., Bednarska, A. J. & Laskowski, R. Physiological and biochemical response of the solitary bee Osmia bicornis exposed to three insecticide-based agrochemicals. Ecotoxicol. Environ. Saf. 230, 113095. https://doi.org/10.1016/j.ecoenv.2021.113095 (2021).
doi: 10.1016/j.ecoenv.2021.113095
pubmed: 34953273
Troczka, B. J. et al. Identification and functional characterisation of a novel N-cyanoamidine neonicotinoid metabolising cytochrome P450, CYP9Q6, from the buff-tailed bumblebee Bombus terrestris. Insect Biochem. Mol. Biol. 111, 103171. https://doi.org/10.1016/j.ibmb.2019.05.006 (2019).
doi: 10.1016/j.ibmb.2019.05.006
pubmed: 31136794
pmcid: 6675907
Beadle, K. et al. Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. PLoS Genet. 15, e1007903. https://doi.org/10.1371/journal.pgen.1007903 (2019).
doi: 10.1371/journal.pgen.1007903
pubmed: 30716069
pmcid: 6375640
Manjon, C. et al. Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Curr. Biol. 28, 1137–1143. https://doi.org/10.1016/j.cub.2018.02.045 (2018).
doi: 10.1016/j.cub.2018.02.045
pubmed: 29576476
pmcid: 5887109
Zimmer, C. T. et al. Molecular and functional characterization of CYP6BQ23, a cytochrome P450 conferring resistance to pyrethroids in European populations of pollen beetle, Meligethes aeneus. Insect Biochem. Mol. Biol. 45, 18–29. https://doi.org/10.1016/j.ibmb.2013.11.008 (2014).
doi: 10.1016/j.ibmb.2013.11.008
pubmed: 24316412
Zhang, X. et al. Knockdown of cytochrome P450 CYP6 family genes increases susceptibility to carbamates and pyrethroids in the migratory locust, Locusta migratoria. Chemosphere 223, 48–57. https://doi.org/10.1016/j.chemosphere.2019.02.011 (2019).
doi: 10.1016/j.chemosphere.2019.02.011
pubmed: 30763915
Zhang, W. et al. The roles of four novel P450 genes in pesticides resistance in Apis cerana cerana Fabricius: Expression levels and detoxification efficiency. Front. Genet. 10, 1000. https://doi.org/10.3389/fgene.2019.01000 (2019).
doi: 10.3389/fgene.2019.01000
pubmed: 31803222
pmcid: 6873825
Hayward, A. et al. The leafcutter bee, Megachile rotundata, is more sensitive to N-cyanoamidine neonicotinoid and butenolide insecticides than other managed bees. Nat. Ecol. Evol. 3, 1521–1524. https://doi.org/10.1038/s41559-019-1011-2 (2019).
doi: 10.1038/s41559-019-1011-2
pubmed: 31666734
de Lange, H. J., van der Pol, J., Lahr, J. & Faber, J. H. Ecological Vulnerability in Wildlife; A Conceptual Approach to Assess Impact of Environmental Stressors (Wageningen, 2006).
de Lange, H. J., Sala, S., Vighi, M. & Faber, J. H. Ecological vulnerability in risk assessment—A review and perspectives. Sci. Total Environ. 408, 3871–3879. https://doi.org/10.1016/j.scitotenv.2009.11.009 (2010).
doi: 10.1016/j.scitotenv.2009.11.009
pubmed: 20004002
Williams, N. M. et al. Ecological and life-history traits predict bee species responses to environmental disturbances. Biol. Conserv. 143, 2280–2291. https://doi.org/10.1016/j.biocon.2010.03.024 (2010).
doi: 10.1016/j.biocon.2010.03.024
Bogusch, P. et al. Difference in pollen specialisation in spring bees Andrena vaga (Andrenidae) and Colletes cunicularius (Colletidae) during their nesting season. Arthropod Plant Interact. 16, 459–467. https://doi.org/10.1007/s11829-022-09910-3 (2022).
doi: 10.1007/s11829-022-09910-3
Anderson, N. L. & Harmon-Threatt, A. N. Chronic contact with realistic soil concentrations of imidacloprid affects the mass, immature development speed, and adult longevity of solitary bees. Sci. Rep. 9, 3724. https://doi.org/10.1038/s41598-019-40031-9 (2019).
doi: 10.1038/s41598-019-40031-9
pubmed: 30842465
pmcid: 6403430
Sponsler, D. B. & Johnson, R. M. Mechanistic modeling of pesticide exposure: The missing keystone of honey bee toxicology. Environ. Toxicol Chem 36, 871–881. https://doi.org/10.1002/etc.3661 (2017).
doi: 10.1002/etc.3661
pubmed: 27769096
Stavert, J. R. et al. Hairiness: the missing link between pollinators and pollination. PeerJ 4, e2779. https://doi.org/10.7717/peerj.2779 (2016).
doi: 10.7717/peerj.2779
pubmed: 28028464
pmcid: 5180583
Pardee, G. L. et al. Life-history traits predict responses of wild bees to climate variation. Proc. R. Soc. B 289, 20212697. https://doi.org/10.1098/rspb.2021.2697 (2022).
doi: 10.1098/rspb.2021.2697
pubmed: 35440209
pmcid: 9019520
Bartomeus, I., Cariveau, D. P., Harrison, T. & Winfree, R. On the inconsistency of pollinator species traits for predicting either response to land-use change or functional contribution. Oikos 127, 306–315. https://doi.org/10.1111/oik.04507 (2018).
doi: 10.1111/oik.04507
Orr, M. C., Jakob, M., Harmon-Threatt, A. & Mupepele, A.-C. A review of global trends in the study types used to investigate bee nesting biology. Basic Appl. Ecol. 62, 12–21. https://doi.org/10.1016/j.baae.2022.03.012 (2022).
doi: 10.1016/j.baae.2022.03.012
Brandt, A. et al. Immunosuppression response to the neonicotinoid insecticide thiacloprid in females and males of the red mason bee Osmia bicornis L. Sci. Rep. 10, 4670. https://doi.org/10.1038/s41598-020-61445-w (2020).
doi: 10.1038/s41598-020-61445-w
pubmed: 32170171
pmcid: 7070012
Farruggia, F. T. et al. A retrospective analysis of honey bee (Apis mellifera) pesticide toxicity data. PLoS ONE 17, e0265962. https://doi.org/10.1371/journal.pone.0265962 (2022).
doi: 10.1371/journal.pone.0265962
pubmed: 35390011
pmcid: 8989193
Zhu, Y. C., Caren, J., Reddy, G. V. P., Li, W. & Yao, J. Effect of age on insecticide susceptibility and enzymatic activities of three detoxification enzymes and one invertase in honey bee workers (Apis mellifera). Biochem. Physiol. C Toxicol. Pharmacol. 238, 108844. https://doi.org/10.1016/j.cbpc.2020.108844 (2020).
doi: 10.1016/j.cbpc.2020.108844
Arena, M. & Sgolastra, F. A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23, 324–334. https://doi.org/10.1007/s10646-014-1190-1 (2014).
doi: 10.1007/s10646-014-1190-1
pubmed: 24435220
Berenbaum, M. R. & Johnson, R. M. Xenobiotic detoxification pathways in honey bees. Curr. Opin. Insect Sci. 10, 51–58. https://doi.org/10.1016/j.cois.2015.03.005 (2015).
doi: 10.1016/j.cois.2015.03.005
pubmed: 29588014
Rondeau, S., Baert, N., McArt, S. & Raine, N. E. Quantifying exposure of bumblebee (Bombus spp.) queens to pesticide residues when hibernating in agricultural soils. Environ. Pollut. 309, 119722. https://doi.org/10.1016/j.envpol.2022.119722 (2022).
doi: 10.1016/j.envpol.2022.119722
pubmed: 35809712
Leza, M., Watrous, K. M., Bratu, J. & Woodard, S. H. Effects of neonicotinoid insecticide exposure and monofloral diet on nest-founding bumblebee queens. Proc. R. Soc. B 285, 20180761. https://doi.org/10.1098/rspb.2018.0761 (2018).
doi: 10.1098/rspb.2018.0761
pubmed: 29899072
pmcid: 6015844
Kopit, A. M. & Pitts-Singer, T. L. Routes of pesticide exposure in solitary, cavity-nesting bees. Environ. Entomol. 47, 499–510. https://doi.org/10.1093/ee/nvy034 (2018).
doi: 10.1093/ee/nvy034
Hamer, M. Ecological risk assessment for agricultural pesticides. Environ. Monit. Assess. 2, 104N-109N. https://doi.org/10.1039/b008962l (2000).
doi: 10.1039/b008962l
Siviter, H., Linguadoca, A., Ippolito, A. & Muth, F. Pesticide licensing in the EU and protecting pollinators. Curr. Biol. 33, R44–R48. https://doi.org/10.1016/j.cub.2022.12.002 (2023).
doi: 10.1016/j.cub.2022.12.002
pubmed: 36693303
Cullen, M. G., Thompson, L. J., Carolan, J. C., Stout, J. C. & Stanley, D. A. Fungicides, herbicides and bees: A systematic review of existing research and methods. PLoS ONE 14, e0225743. https://doi.org/10.1371/journal.pone.0225743 (2019).
doi: 10.1371/journal.pone.0225743
pubmed: 31821341
pmcid: 6903747
Thompson, H., Santos, G. & Cione, A. Letter to the editor regarding Lourencetti et al. Surrogate species in pesticide risk assessments: Toxicological data of three stingless bees species. Environ. Pollut. 319, 121011. https://doi.org/10.1016/j.envpol.2023.121011 (2023).
doi: 10.1016/j.envpol.2023.121011
pubmed: 36608726
Wood, T. J. et al. Managed honey bees as a radar for wild bee decline?. Apidologie 51, 1100–1116. https://doi.org/10.1007/s13592-020-00788-9 (2020).
doi: 10.1007/s13592-020-00788-9
Jütte, T., Wernecke, A., Klaus, F., Pistorius, J. & Dietzsch, A. C. Dataset: Risk assessment requires several bee species to address species-specific sensitivity to insecticides at field-realistic concentrations. OpenAgrar https://doi.org/10.5073/20231124-160110-0 (2023).
doi: 10.5073/20231124-160110-0