Recommendations for standardized oral toxicity test protocols for larvae of solitary bees, Osmia spp.
- 93 Downloads
Abstract
Effects of pesticides have been debated as one of the causes of worldwide declines of bee populations. Improving the risk assessment of pesticides on bees is important to halt these declines. Pesticide risk assessment today mainly focuses on one bee species, the honey bee. Because of differences in life cycles among bee species, this risk assessment needs to be adapted to take these differences into account. For both the adult and larval life stages, development of test protocols for solitary bees is required. Here, we summarize the current knowledge on larval tier 1 tests based on the first test protocols for solitary bee larvae available in the literature. As the ecology and rearing of solitary bees of the genus Osmia spp. are well known, we propose this genus as a model species in a first step to develop protocols for solitary species. In addition, we discuss guidelines, relevant endpoints, and research needs for the development of a standardized oral toxicity test protocol of solitary bee larvae.
Keywords
pesticides solitary bees Osmia spp. oral toxicity test ecotoxicologyNotes
Contributions
ME, MP and GS conceived the study goal. All authors contributed to writing of the manuscript and approved the final manuscript.
Funding information
The research was funded by the Research Foundation Flanders (FWO) PhD grants 1S71416N (ME) and 1S16917N (MP). The authors also thank support by the Special Research Fund of Ghent University.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
References
- Abbott, V. A., Nadeau, J. L., Higo, H. A., & Winston, M. L. (2008). Lethal and sublethal effects of imidacloprid on Osmia lignaria and clothianidin on Megachile rotundata (Hymenoptera: Megachilidae). J. Econ. Entomol., 101(3), 784–796. https://doi.org/10.1603/0022-0493(2008)101 CrossRefPubMedGoogle Scholar
- Anderson, N. L., & Harmon-Threatt, A. N. (2019). Chronic contact with realistic soil concentrations of imidacloprid affects the mass immature development speed, and adult longevity of solitary bees. Sci. Rep., 9(3724), 1–9. https://doi.org/10.1038/s41598-019-40031-9 CrossRefGoogle Scholar
- Arena, M., & Sgolastra, F. (2014). A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology, 23(3), 324–334. https://doi.org/10.1007/s10646-014-1190-1 CrossRefPubMedGoogle Scholar
- Beasley, D. A. E., Bonisoli-alquati, A., & Mousseau, T. A. (2013). The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: A meta-analysis. Ecol. Indic., 30, 218–226. https://doi.org/10.1016/j.ecolind.2013.02.024 CrossRefGoogle Scholar
- Becker, M.C. & Keller, A. (2015) Laboratory rearing of solitary bees and wasps. Insect Sci., 23, 1–6. https://doi.org/10.1111/1744-7917.12242 CrossRefGoogle Scholar
- Beekman, M., Stratum, P. Van, & Lingeman, R. (1998). Diapause survival and post-diapause performance in bumblebee queens (Bombus terrestris). Entomol. Exp. Appl., 89(3), 207–214. https://doi.org/10.1046/j.1570-7458.1998.00401.x CrossRefGoogle Scholar
- Biddinger, D. J., Robertson, J. L., Mullin, C., Frazier, J., Ashcraft, S. A., Rajotte, E. G., … Vaughn, M. (2013). Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS ONE, 8(9), e72587. https://doi.org/10.1371/journal.pone.0072587 CrossRefPubMedPubMedCentralGoogle Scholar
- Biesmeijer, J. C., Roberts, S. P. M., Reemer, M., Ohlemuller, R., Edwards, M., Peeters, T., … Kunin, W. E. (2006). Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313, 351–354. https://doi.org/10.1126/science.1127863 CrossRefPubMedPubMedCentralGoogle Scholar
- Bosch, J., & Blas, M. (1994). Effect of over-wintering and incubation temperatures on adult emergence in Osmia cornuta Latr (Hymenoptera, Megachilidae). Apidologie, 25(3), 265–277. https://doi.org/10.1051/apido:19940301 CrossRefGoogle Scholar
- Bosch, J. & Kemp, W.P. (2000) Development and emergence of the orchard pollinator Osmia lignaria (Hymenoptera: Megachilidae). Environ. Entomol., 29, 8–13. https://doi.org/10.1603/0046-225x-29.1.8 CrossRefGoogle Scholar
- Bosch, J., & Kemp, W. P. (2003). Effect of wintering duration and temperature on survival and emergence time in males of the orchard pollinator Osmia lignaria (Hymenoptera: Megachilidae). Environ. Entomol., 32(4), 711–716. https://doi.org/10.1603/0046-225X-32.4.711 CrossRefGoogle Scholar
- Bosch, J., & Kemp, W. P. (2004). Effect of pre-wintering and wintering temperature regimes on weight loss, survival, and emergence time in the mason bee Osmia cornuta (Hymenoptera: Megachilidae). Apidologie, 35(5), 469–479. https://doi.org/10.1051/apido CrossRefGoogle Scholar
- Bosch, J. & Vicens, N. (2002). Body size as an estimator of production costs in a solitary bee. Ecol. Entomol. 27, 129-137.CrossRefGoogle Scholar
- Bosch, J., & Vicens, N. (2006). Relationship between body size, provisioning rate, longevity and reproductive success in females of the solitary bee Osmia cornuta. Behav. Ecol. Sociobiol., 60(1), 26–33. https://doi.org/10.1007/s00265-005-0134-4 CrossRefGoogle Scholar
- Bosch, J., Kemp, W.P. & Peterson, S.S. (2000) Management of Osmia lignaria (Hymenoptera: Megachilidae) populations for almond pollination: methods to advance bee emergence. Environ. Entomol., 29, 874–883. https://doi.org/10.1603/0046-225x-29.5.874 CrossRefGoogle Scholar
- Botias, C., David, A., Horwood, J., Abdul-sada, A., Nicholls, E., Hill, E., & Goulson, D. (2015). Neonicotinoid residues in wild flowers, a potential route of chronic exposure for bees. Environ. Sci. Technol., 49, 12731−12740. https://doi.org/10.1021/acs.est.5b03459 CrossRefPubMedGoogle Scholar
- Bukovinszky, T., Rikken, I., Evers, S., Wäckers, F.L., Biesmeijer, J.C., Prins, H.H.T., et al. (2017). Effects of pollen species composition on the foraging behaviour and offspring performance of the mason bee Osmia bicornis (L.). Basic Appl. Ecol., 18, 21–30. https://doi.org/10.1016/j.baae.2016.11.001 CrossRefGoogle Scholar
- Cabrera, A. R., Almanza, T., Cutler, G. C., Fischer, D. L., Hinarejos, S., Lewis, G., … Steen, J. Van Der. (2016). Initial recommendations for higher-tier risk assessment protocols for bumble bees, Bombus spp. (Hymenoptera: Apidae). Integr. Environ. Assess. Manag., 12(2), 222–229. https://doi.org/10.1002/ieam.1675 CrossRefPubMedGoogle Scholar
- Carvalheiro, L., Gigante, S., Kunin, W. E., Keil, P., Aguirre-Gutiérrez J. … Biesmeijer, J. C. (2013). Species richness declines and biotic homogenization have slowed down for NW-European pollinators and plants. Ecol. Lett., 16(7), 870–878. https://doi.org/10.1111/ele.12121 CrossRefPubMedPubMedCentralGoogle Scholar
- Dainese, M., Riedinger, V., Holzschuh, A., Kleijn, D., Scheper, J. & Steffan-Dewenter, I. (2018) Managing trap-nesting bees as crop pollinators: Spatiotemporal effects of floral resources and antagonists. J. Appl. Ecol., 55, 195–204. https://doi.org/10.1111/1365-2664.12930 CrossRefGoogle Scholar
- David, A., Botías, C., Abdul-sada, A., Nicholls, E., Rotheray, E. L., Hill, E. M., & Goulson, D. (2016). Widespread contamination of wild flower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ. Int., 88, 169–178. https://doi.org/10.1016/j.envint.2015.12.011 CrossRefPubMedGoogle Scholar
- Dietemann, V., Ellis, K. D., Neumann, P. (2013) The COLOSS BEEBOOK Volume I, Standard methods for Apis mellifera research. J. Apic. Res., 52:4, 1-4, https://doi.org/10.3896/IBRA.1.52.4.23 CrossRefGoogle Scholar
- EFSA (2013) Guidance on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J. 11.Google Scholar
- Fauser, A., Sandrock, C., Neumann, P., & Sadd, B. S. (2017). Neonicotinoids override a parasite exposure impact on hibernation success of a key bumblebee pollinator. Ecol. Entomol., 42(3), 306–314. https://doi.org/10.1111/een.12385 CrossRefGoogle Scholar
- Fogel, M. N., Ine, M., Ronco, A. E., & Desneux, N. (2013). Impact of the neonicotinoid acetamiprid on immature stages of the predator Eriopis connexa (Coleoptera: Coccinellidae). Ecotoxicology, 22(6), 1063–1071. https://doi.org/10.1007/s10646-013-1094-5 CrossRefPubMedGoogle Scholar
- Forrest, J.R.K. & Thomson, J. D. (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol. Monogr., 81, 469–491. https://doi.org/10.1890/10-1885.1 CrossRefGoogle Scholar
- Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., Aizen, M. A., Bommarco, R., Cunningham, S. A., … Klein, A. M. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339(6127), 1608–1611. https://doi.org/10.1126/science.1230200 CrossRefPubMedGoogle Scholar
- Gerard, M., Michez, D., Debat, V., Fullgrabe, L., Meeus, I., Piot, N., Sculfort, O., Vastrade, M., Smagghe, G. & Vanderplanck (2018). Stressful conditions reveal decrease in size, modification of shape but relatively stable asymmetry in bumblebee wings. Sci. Rep., 8, 15169. https://doi.org/10.1038/s41598-018-33429-4 CrossRefPubMedPubMedCentralGoogle Scholar
- Goulson, D., Nicholls, E., Botías, C., Rotheray, E.L., (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science (80- ). 347, 1–16. https://doi.org/10.1126/science.1255957 CrossRefGoogle Scholar
- Gradish, A. E., Scott-Dupree, C. D., Cutler, G. C. (2012). Susceptibility of Megachile rotundata to insecticides used in wild blueberry production in Atlantic Canada. J. Pest. Sci., 85(1), 133-140. https://doi.org/10.1007/s10340-011-0391-0 CrossRefGoogle Scholar
- Guirguis, G. N., & Brindley, W. A. (1974). Insecticide susceptibility and response to selected pollens of larval alfalfa leafcutting bees, Megachile pacifica (Panzer) (Hymenoptera: Megachilidae). Environ. Entomol., 3(4), 691–694. https://doi.org/10.1093/ee/3.4.691 CrossRefGoogle Scholar
- Heard, M. S., Baas, J., Dorne, J.- Lou, Lahive, E., Robinson, A. G., Rortais, A., … Hesketh, H. (2017). 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 CrossRefGoogle Scholar
- Hendriksma, H. P., Härtel, P., & Steffan-dewenter, I. (2011) Honey bee risk assessment: new approaches for in vitro larvae rearing and data analyses. Methods Ecol. Evol., 2, 509–517. https://doi.org/10.1111/j.2041-210X.2011.00099.x CrossRefGoogle Scholar
- Hodgson, E. W., Pitts-singer, T. L., & Barbour, J. D. (2011). Effects of the insect growth regulator, novaluron on immature alfalfa leafcutting bees, Megachile rotundata. J. Insect Sci., 11(43), 1–10. https://doi.org/10.1673/031.011.0143 CrossRefGoogle Scholar
- Huntzinger, I. C., James, R. R., Bosch, J., & Kemp, W. P. (2008). Fungicide tests on adult alfalfa leafcutting bees (Hymenoptera: Megachilidae). J. Econ. Entomol., 101(4), 1088–1094. https://doi.org/10.1603/0022-0493(2008)101 CrossRefPubMedGoogle Scholar
- Jin, N., Klein, S., Leimig, F., Bischoff, G., & Menzel, R. (2015). The neonicotinoid clothianidin interferes with navigation of the solitary bee Osmia cornuta in a laboratory test. J. Exp. Biol., 218(18), 2821–2825. https://doi.org/10.1242/jeb.123612 CrossRefPubMedGoogle Scholar
- Johansen, C. A., Rincker, C. M., George, D. A., Mayer, D. F., & Kious, A. W. (1984). Effects of aldicarb and its biologically active metabolites on bees. Environ. Entomol., 13(5), 1386–1398. https://doi.org/10.1093/ee/13.5.1386 CrossRefGoogle Scholar
- Kemp, W. P., Bosch, J., & Dennis, D. (2004). Oxygen consumption during the life cycles of the prepupa-wintering bee Megachile rotundata and the adult-wintering bee Osmia lignaria (Hymenoptera: Megachilidae), Ann. Entomol. Soc. Am., 97(1), 161–170. https://doi.org/10.1603/0013-8746(2004)097[0161:OCDTLC]2.0.CO;2 CrossRefGoogle Scholar
- Konrad, R., Ferry, N., Gatehouse, A. M. R., & Babendreier, D. (2008). Potential effects of oilseed rape expressing oryzacystatin-1 (OC-1) and of purified insecticidal proteins on larvae of the solitary bee Osmia bicornis. PLoS ONE, 3(7), e2664. https://doi.org/10.1371/journal.pone.0002664 CrossRefPubMedPubMedCentralGoogle Scholar
- Kopit, A. M., & Pitts-singer, T. L. (2018). Routes of pesticide exposure in solitary, cavity-nesting bees. Environ. Entomol., 47(3), 499–510. https://doi.org/10.1093/ee/nvy034 CrossRefGoogle Scholar
- Krunić, M.D., Stanisavljević, L.Z., (2006). The biology of European orchard Bee Osmia cornuta (Latr.) (Hymenoptera: Megachilidae). Belgrade: University of Belgrade.Google Scholar
- Ladurner, E., Bosch, J., Kemp, W. P., & Maini, S. (2005). Original article asessing delayed and acute toxicity of five formulated fungicides to Osmia lignaria Say and Apis mellifera. Apidologie, 36(3), 449–460. https://doi.org/10.1051/apido CrossRefGoogle Scholar
- Lens, L., Dongen, S. Van, Kark, S. & Matthysen, E. (2002) Fluctuating asymmetry as an indicator of fitness: Can we bridge the gap between studies? Biol. Rev., 77, 27–38. https://doi.org/10.1017/S1464793101005796 CrossRefPubMedGoogle Scholar
- Michener, C. D., (2007). The nees of the world. Baltimore: The Johns Hopkins University Press.Google Scholar
- Nicholls, E., Fowler, R., Niven, J. E., Gilbert, J. D., & Goulson, D. (2017). Larval exposure to field-realistic concentrations of clothianidin has no effect on development rate, over-winter survival or adult metabolic rate in a solitary bee, Osmia bicornis. PeerJ, e3417. https://doi.org/10.7717/peerj.3417 CrossRefGoogle Scholar
- Norden, B. B. (1984). Nesting biology of Anthophora abrupta (Hymenoptera: Anthophoridae). J. Kansas Entomol. Soc., 57(2), 243–262.Google Scholar
- OECD (2017a), Test No. 246: Bumblebee, acute contact toxicity test, OECD guidelines for the testing of chemicals, Section 2, OECD Publishing, Paris, https://doi.org/10.1787/9789264284104-en CrossRefGoogle Scholar
- OECD (2017b), Test No. 247: Bumblebee, acute oral toxicity test, OECD guidelines for the testing of chemicals, Section 2, OECD Publishing, Paris, https://doi.org/10.1787/9789264284128-en CrossRefGoogle Scholar
- Ohl, M., & Thiele, K. (2007). Estimating body size in apoid wasps: the significance of linear variables in a morphologically diverse taxon (Hymenoptera, Apoidea). Zoosystemat. Evol., 83(2), 110–124. https://doi.org/10.1002/mmnz.200700003 CrossRefGoogle Scholar
- Ollerton, J., Winfree, R., Tarrant, S., (2011). How many flowering plants are pollinated by animals? Oikos 120, 321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x CrossRefGoogle Scholar
- Ondo, N. A. Z., Alibert, P., Dousset, S., Savadogo, P. W., Savadogo, M., & Sedogo, M. (2011). Chemosphere insecticide residues in cotton soils of Burkina Faso and effects of insecticides on fluctuating asymmetry in honey bees (Apis mellifera Linnaeus). Chemosphere, 83(4), 585–592. https://doi.org/10.1016/j.chemosphere.2010.12.021 CrossRefGoogle Scholar
- Peach, M. L., Alston, D. G., Tepedino, V. J. (1994). Bees and bran bait: is carbaryl bran bait lethal to alfalfa leafcutting Bbee (Hymenoptera: Megachilidae) adults or larvae? J. Econ. Entomol., 87(2), 311-317. https://doi.org/10.1093/jee/87.2.311 CrossRefGoogle Scholar
- Pitts-Singer, T.L. & Bosch, J. (2010) Nest establishment, pollination efficiency, and reproductive success of Megachile rotundata (Hymenoptera: Megachilidae) in relation to resource availability in field enclosures. Environ. Entomol., 39, 149–158. https://doi.org/10.1603/en09077 CrossRefPubMedGoogle Scholar
- Powney, G.D., Carvell, C., Edwards, M., Morris, R.K.A., Roy, H.E., Woodcock, B.A., Isaac, N.J.B., (2019). Widespread losses of pollinating insects in Britain. Nat. Commun. 10, 1018. https://doi.org/10.1038/s41467-019-08974-9 CrossRefPubMedPubMedCentralGoogle Scholar
- Radmacher, S., & Strohm, E. (2010). Factors affecting offspring body size in the solitary bee Osmia bicornis (Hymenoptera, Megachilidae). Apidologie, 41(2), 169–177. https://doi.org/10.1051/apido/2009064 CrossRefGoogle Scholar
- Raw, A. (1972) The biology of the solitary bee Osmia rufa (L.) (Megachilidae). Trans. R. Entomol. Soc. Lond., 124, 213–229. https://doi.org/10.1111/j.1365-2311.1972.tb00364.x CrossRefGoogle Scholar
- Rust, R., Torchio, P., & Trostle, R. (1989). Late embryogenesis and immature development of Osmia rufa cornigera (Rossi) (Hymenoptera: Megachilidae). Apidologie, 20(4), 359–367. https://doi.org/10.1051/apido:19890408 CrossRefGoogle Scholar
- Sandrock, C., Tanadini, L.G., Pettis, J.S., Biesmeijer, J.C., Potts, S.G. & Neumann, P. (2014) Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agric. For. Entomol., 16, 119–128. https://doi.org/10.1111/afe.12041 CrossRefGoogle Scholar
- Schenk, M., Krauss, J., & Holzschuh, A. (2018a). Desynchronizations in bee-plant interactions cause severe fitness losses in solitary bees. J. Anim. Ecol., 87(1), 139–149. https://doi.org/10.1111/1365-2656.12694 CrossRefPubMedGoogle Scholar
- Schenk, M., Mitesser, O., Hovestadt, T., & Holzschuh, A. (2018b). Overwintering temperature and body condition shift emergence dates of spring-emerging solitary bees. PeerJ, 6, e4721. https://doi.org/10.7717/peerj.4721 CrossRefPubMedPubMedCentralGoogle Scholar
- Scott-dupree, C. D., Conroy, L., & Harris, C. R. (2009). Impact of currently used or potentially useful insecticides for canola agroecosystems on Bombus impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymentoptera: Megachilidae), and Osmia lignaria (Hymenoptera: Megachilidae). J. Econ. Entomol., 102(1), 177–182. https://doi.org/10.1603/029.102.0125 CrossRefPubMedGoogle Scholar
- Sgolastra, F., Kemp, W.P., Buckner, J.S., Pitts-Singer, T.L., Maini, S. & Bosch, J. (2011) The long summer: pre-wintering temperatures affect metabolic expenditure and winter survival in a solitary bee. J. Insect Physiol., 57, 1651–1659. https://doi.org/10.1016/j.jinsphys.2011.08.017 CrossRefPubMedGoogle Scholar
- Sgolastra, F., Tosi, S., Medrzycki, P., Porrini, C., & Burgio, G. (2015). Toxicity of spirotetramat on solitary bee larvae, Osmia cornuta (Hymenoptera: Megachilidae), in laboratory conditions. J. Apicult. Sci., 59(2), 73–83. https://doi.org/10.1515/JAS-2015-0024 CrossRefGoogle Scholar
- Sgolastra, F., Medrzycki, P., Bortolotti, L., Renzi, T., Tosi, S., Bogo, G., … Bosch, J. (2017). Synergistic mortality between a neonicotinoid insecticide and an ergosterol-biosynthesis-inhibiting fungicide in three bee species. Pest Manag. Sci., 73(6), 1236–1243. https://doi.org/10.1002/ps.4449 CrossRefPubMedGoogle Scholar
- Sgolastra, F., Hinarejos, S., Pitts-singer, T. L., Boyle, N. K., Joseph, T., Johannes, L., … Bosch, J. (2018a). Pesticide exposure assessment paradigm for solitary bees. Environ. Entomol., nvy105, 1–14. https://doi.org/10.1093/ee/nvy105 CrossRefGoogle Scholar
- Sgolastra, F., Arnan, X., Cabbri, R., Isani, G., Medrzycki, P., Teper, D., & Bosch, J. (2018b). Combined exposure to sublethal concentrations of an insecticide and a fungicide affect feeding, ovary development and longevity in a solitary bee. Proc. R. Soc. B Biol. Sci., 285, 20180887. https://doi.org/10.1098/rspb.2018.0887 CrossRefGoogle Scholar
- Staab, M., Pufal, G., Tscharntke, T. & Klein, A.M. (2018) Trap nests for bees and wasps to analyse trophic interactions in changing environments - A systematic overview and user guide. Methods Ecol. Evol., 9, 2226–2239. https://doi.org/10.1111/2041-210X.13070 CrossRefGoogle Scholar
- Stoner, K. A. (2016). Current pesticide risk assessment protocols do not adequately address differences between honey bees (Apis mellifera) and bumble bees (Bombus spp.). Front. Environ. Sci., 4(December), 1–8. https://doi.org/10.3389/fenvs.2016.00079 CrossRefGoogle Scholar
- Straub, L., Williams, G. R., Pettis, J., Fries, I., & Neumann, P. (2015). Superorganism resilience: eusociality and susceptibility of ecosystem service providing insects to stressors. Curr. Opin. Insect Sci. 12, 109–112. https://doi.org/10.1016/j.cois.2015.10.010 CrossRefGoogle Scholar
- Szentgyörgyi, H., Moron, D., Nawrocka, A., Tofilski, A., & Woyciechowski, M. (2017). Forewing structure of the solitary bee Osmia bicornis developing on heavy metal pollution gradient. Ecotoxicology, 26(8), 1031–1040. https://doi.org/10.1007/s10646-017-1831-2 CrossRefPubMedPubMedCentralGoogle Scholar
- Tesoriero, D., Maccagnani, B., Santi, F., & Celli, G. (2003). Toxicity of three pesticides on larval instars of Osmia cornuta: preliminary results. Bull. Insectol., 56(1), 169–171.Google Scholar
- Thompson, H. (2016). Extrapolation of acute toxicity across bee species. Integr. Environ. Assess. Manag., 12(4), 622–626. https://doi.org/10.1002/ieam.1737 CrossRefPubMedGoogle Scholar
- Thompson, H., Pamminger, T. (2019). Perspective: Are honeybees suitable surrogates for use in pesticide risk assessment for non-Apis bees? Pest Manag. Sci., accepted online. https://doi.org/10.1002/ps.5494 CrossRefGoogle Scholar
- Torchio, P. F. (1989). In-nest biologies and development of immature stages of three Osmia species (Hymenoptera: Megachilidae). Ann. Entomol. Soc. Am., 82(5), 599–615. https://doi.org/10.1093/aesa/82.5.599 CrossRefGoogle Scholar
- Uhl, P., Franke, L. A., Re, C., Wollmann, C., Peter, S., Jeker, L., & Brühl, C. A. (2016). Interspecific sensitivity of bees towards dimethoate and implications for environmental risk assessment. Sci. Rep., 6(34439), 1–7. https://doi.org/10.1038/srep34439 CrossRefGoogle Scholar
- Vázquez, D.E., Ilina, N., Pagano, E.A., Zavala, J.A., Farina, W.M., 2018. Glyphosate affects the larval development of honey bees depending on the susceptibility of colonies. PLoS One 13, e0205074. https://doi.org/10.1371/journal.pone.0205074 CrossRefPubMedPubMedCentralGoogle Scholar
- Weissel, N., Mitesser, O., Poethke, H.J. & Strohm, E. (2012) Availability and depletion of fat reserves in Halictid foundress queens with a focus on solitary nest founding. Insect. Soc., 59, 67–74. https://doi.org/10.1007/s00040-011-0189-3 CrossRefGoogle Scholar
- Wood, T. J., & Goulson, D. (2017). The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ. Sci. Pollut. Res., 24(21), 17285–17325. https://doi.org/10.1007/s11356-017-9240-x CrossRefGoogle Scholar
- Woodcock, B. A., Bullock, J. M., Shore, R. F., Heard, M. S., Pereira, M. G., Redhead, J., … Pywell, R. F. (2017). Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science, 356(6345), 1393–1395. https://doi.org/10.1126/science.aaa1190 CrossRefPubMedGoogle Scholar
- Wu, J.Y., Anelli, C.M., Sheppard, W.S., (2011). Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS One 6, e14720. https://doi.org/10.1371/journal.pone.0014720 CrossRefPubMedPubMedCentralGoogle Scholar
- Youn, Y. N., Seo, M. J., Shin, J. G., Jang, C., & Yu, Y. M. (2003). Toxicity of greenhouse pesticides to multicolored Asian lady beetles, Harmonia axyridis (Coleoptera: Coccinellidae). Biol. Control, 28(2), 164–170. https://doi.org/10.1016/S1049-9644(03)00098-7 CrossRefGoogle Scholar