Bees exposed to climate change are more sensitive to pesticides.

Osmia cornuta body size climate change global warming longevity nutritional stress pesticide exposure sulfoxaflor synergistic effects toxicity

Journal

Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746

Informations de publication

Date de publication:
Nov 2023
Historique:
received: 04 05 2023
accepted: 13 08 2023
pubmed: 1 9 2023
medline: 1 9 2023
entrez: 1 9 2023
Statut: ppublish

Résumé

Bee populations are exposed to multiple stressors, including land-use change, biological invasions, climate change, and pesticide exposure, that may interact synergistically. We analyze the combined effects of climate warming and sublethal insecticide exposure in the solitary bee Osmia cornuta. Previous Osmia studies show that warm wintering temperatures cause body weight loss, lipid consumption, and fat body depletion. Because the fat body plays a key role in xenobiotic detoxification, we expected that bees exposed to climate warming scenarios would be more sensitive to pesticides. We exposed O. cornuta females to three wintering treatments: current scenario (2007-2012 temperatures), near-future (2021-2050 projected temperatures), and distant-future (2051-2080). Upon emergence in spring, bees were orally exposed to three sublethal doses of an insecticide (Closer, a.i. sulfoxaflor; 0, 4.55 and 11.64 ng a.i./bee). We measured the combined effects of wintering and insecticide exposure on phototactic response, syrup consumption, and longevity. Wintering treatment by itself did not affect winter mortality, but body weight loss increased with increasing wintering temperatures. Similarly, wintering treatment by itself hardly influenced phototactic response or syrup consumption. However, bees wintered at the warmest temperatures had shorter longevity, a strong fecundity predictor in Osmia. Insecticide exposure, especially at the high dose, impaired the ability of bees to respond to light, and resulted in reduced syrup consumption and longevity. The combination of the warmest winter and the high insecticide dose resulted in a 70% longevity decrease. Smaller bees, resulting from smaller pollen-nectar provisions, had shorter longevity suggesting nutritional stress may further compromise fecundity in O. cornuta. Our results show a synergistic interaction between two major drivers of bee declines, and indicate that bees will become more sensitive to pesticides under the current global warming scenario. Our findings have important implications for pesticide regulation and underscore the need to consider multiple stressors to understand bee declines.

Identifiants

pubmed: 37656005
doi: 10.1111/gcb.16928
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

6248-6260

Subventions

Organisme : Spanish Ministry of Science and Innovation
ID : PRE2019-090375
Organisme : Spanish Ministry of Science and Innovation
ID : PRE2019-088817
Organisme : Spanish Ministry of Science and Innovation
ID : PID2021-128938OB-I00
Organisme : Spanish Ministry of Science and Innovation
ID : RTI2018-098399-B-I00
Organisme : Spanish Ministry of Universities
ID : Margarita-Salas-scholarship

Informations de copyright

© 2023 The Authors. Global Change Biology published by John Wiley & Sons Ltd.

Références

Agencia Estatal de Meteorología (AEMET). (2021). 2020, the warmest year in Spain, in Europe and in the world. https://www.aemet.es/es/noticias/2022/10/septiembre_2022_resumen_clima
Albacete, S., Sancho, G., Azpiazu, C., Rodrigo, A., Molowny-Horas, R., Sgolastra, F., & Bosch, J. (2023). Bees exposed to climate change are more sensitive to pesticides. Dryad Dataset. https://doi.org/10.5061/dryad.dz08kps3f
Arrese, E. L., & Soulages, J. L. (2010). Insect fat body: Energy, metabolism, and regulation. Annual Review of Entomology, 55, 207-225. https://doi.org/10.1146/annurev-ento-112408-085356
Aufauvre, J., Biron, D. G., Vidau, C., Fontbonne, R., Roudel, M., Diogon, M., Viguès, B., Belzunces, L. P., Delbac, F., & Blot, N. (2012). Parasite-insecticide interactions: A case study of Nosema ceranae and fipronil synergy on honeybee. Scientific Reports, 2(1), 326. https://doi.org/10.1038/srep00326
Azpiazu, C., Bosch, J., Bortolotti, L., Medrzycki, P., Teper, D., Molowny-Horas, R., & Sgolastra, F. (2021). Toxicity of the insecticide sulfoxaflor alone and in combination with the fungicide fluxapyroxad in three bee species. Scientific Reports, 11(1), 6821. https://doi.org/10.1038/s41598-021-86036-1
Azpiazu, C., Bosch, J., Martins, C., & Sgolastra, F. (2022). Effects of chronic exposure to the new insecticide sulfoxaflor in combination with a SDHI fungicide in a solitary bee. Science of the Total Environment, 850, 157822. https://doi.org/10.1016/j.scitotenv.2022.157822
Azpiazu, C., Bosch, J., Viñuela, E., Medrzycki, P., Teper, D., & Sgolastra, F. (2019). Chronic oral exposure to field-realistic pesticide combinations via pollen and nectar: Effects on feeding and thermal performance in a solitary bee. Scientific Reports, 9(1), 13770. https://doi.org/10.1038/s41598-019-50255-4
Azpiazu, C., Hinarejos, S., Sancho, G., Albacete, S., Sgolastra, F., Martins, C. A. H., Domene, X., Benrezkallah, J., Rodrigo, A., Arnan, X., & Bosch, J. (2023). Description and validation of an improved method to feed solitary bees (Osmia spp.) known amounts of pesticides. Ecotoxicology and Environmental Safety, 264, 115398.
Bird, G., Wilson, A. E., Williams, G. R., & Hardy, N. B. (2021). Parasites and pesticides act antagonistically on honey bee health. Journal of Applied Ecology, 58(5), 997-1005. https://doi.org/10.1111/1365-2664.13811
Blanckenhorn, W. U., & Henseler, C. (2005). Temperature-dependent ovariole and testis maturation in the yellow dung fly. Entomologia Experimentalis et Applicata, 116(3), 159-165. https://doi.org/10.1111/j.1570-7458.2005.00316.x
Blanken, L. J., van Langevelde, F., & van Dooremalen, C. (2015). Interaction between Varroa destructor and imidacloprid reduces flight capacity of honeybees. Proceedings of the Royal Society B: Biological Sciences, 282(1820), 20151738. https://doi.org/10.1098/rspb.2015.1738
Bloch, G., & Meshi, A. (2007). Influences of octopamine and juvenile hormone on locomotor behavior and period gene expression in the honeybee, Apis mellifera. Journal of Comparative Physiology A, 193, 181-199. https://doi.org/10.1007/s00359-006-0179-5/tables/6
Bosch, J. (1994). The nesting behaviour of the mason bee Osmia cornuta (Latr) with special reference to its pollinating potential (hymenoptera, Megachilidae). Apidologie, 25(1), 84-93. https://doi.org/10.1051/apido:19940109
Bosch, J., & Blas, M. (1994a). Foraging behaviour and pollinating efficiency of Osmia cornuta and Apis mellifera on almond (Hymenoptera, Megachilidae and Apidae). Applied Entomology and Zoology, 29(1), 1-9. https://doi.org/10.1303/aez.29.1
Bosch, J., & Blas, M. (1994b). 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
Bosch, J., & Kemp, W. P. (2000). Development and emergence of the orchard pollinator Osmia lignaria (Hymenoptera: Megachilidae). Environmental Entomology, 29(1), 8-13. https://doi.org/10.1603/0046-225x-29.1.8
Bosch, J., & Kemp, W. P. (2001). How to manage the blue orchard bee as an orchard pollinator. Handbook series book 5. Sustainable Agriculture Network.
Bosch, J., & Kemp, W. P. (2002). Developing and establishing bee, species as crop pollinators: The example of Osmia spp. (Hymenoptera: Megachilidae) and fruit trees. Bulletin of Entomological Research, 92(1), 3-16. https://doi.org/10.1079/ber2001139
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). Environmental Entomology, 32(4), 711-716. https://doi.org/10.1603/0046-225x-32.4.711
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:2004035
Bosch, J., Kemp, W. P., & Peterson, S. S. (2000). Management of Osmia lignaria (Hymenoptera: Megachilidae) populations for almond pollination: Methods to advance bee emergence. Environmental Entomology, 29(5), 874-883. https://doi.org/10.1603/0046-225x-29.5.874
Bosch, J., Sgolastra, F., & Kemp, W. P. (2010). Timing of eclosion affects diapause development, fat body consumption and longevity in Osmia lignaria, a univoltine, adult-wintering solitary bee. Journal of Insect Physiology, 56(12), 1949-1957. https://doi.org/10.1016/j.jinsphys.2010.08.017
Bosch, J., & Vicens, N. (2002). Body size as an estimator of production costs in a solitary bee. Ecological Entomology, 27(2), 129-137. https://doi.org/10.1046/j.1365-2311.2002.00406.x
Bosch, J., & Vicens, N. (2006). Relationship between body size, provisioning rate, longevity and reproductive success in females of the solitary bee Osmia cornuta. Behavioral Ecology and Sociobiology, 60, 26-33. https://doi.org/10.1007/s00265-005-0134-4
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., & West, G. B. (2004). Toward a metabolic theory of ecology. Ecology, 85(7), 1771-1789. https://doi.org/10.1890/03-9000
Bruckner, S., Straub, L., Neumann, P., & Williams, G. R. (2023). Negative but antagonistic effects of neonicotinoid insecticides and ectoparasitic mites Varroa destructor on Apis mellifera honey bee food glands. Chemosphere, 313, 137535. https://doi.org/10.1016/j.chemosphere.2022.137535
CaraDonna, P. J., Cunningham, J. L., & Iler, A. M. (2018). Experimental warming in the field delays phenology and reduces body mass, fat content and survival: Implications for the persistence of a pollinator under climate change. Functional Ecology, 32(10), 2345-2356. https://doi.org/10.1111/1365-2435.13151
Castelli, L., Branchiccela, B., Garrido, M., Invernizzi, C., Porrini, M., Romero, H., Santos, E., Zunino, P., & Antúnez, K. (2020). Impact of nutritional stress on honeybee gut microbiota, immunity, and Nosema ceranae infection. Microbial Ecology, 80, 908-919. https://doi.org/10.1007/s00248-020-01538-1
Castle, D., Alkassab, A. T., Bischoff, G., Steffan-Dewenter, I., & Pistorius, J. (2022). High nutritional status promotes vitality of honey bees and mitigates negative effects of pesticides. Science of the Total Environment, 806, 151280. https://doi.org/10.1016/j.scitotenv.2021.151280
Chole, H., Woodard, S. H., & Bloch, G. (2019). Body size variation in bees: Regulation, mechanisms, and relationship to social organization. Current Opinion in Insect Science, 35, 77-87. https://doi.org/10.1016/j.cois.2019.07.006
Copernicus Climate Change Service (Copernicus). (2020). The boreal winter season 19/20 was by far the warmest winter season ever recorded in Europe. https://climate.copernicus.eu/boreal-winter-season-1920-was-far-warmest-winter-season-ever-recorded-europe-0
Costa, C. P., Duennes, M. A., Fisher, K., Der, J. P., Watrous, K. M., Okamoto, N., Yamanaka, N., & Woodard, S. H. (2020). Transcriptome analysis reveals nutrition- and age-related patterns of gene expression in the fat body of pre-overwintering bumble bee queens. Molecular Ecology, 29(4), 720-737. https://doi.org/10.1111/mec.15361
Cribari-Neto, F., & Zeileis, A. (2010). Beta regression in R. Journal of Statistical Software, 34, 1-24. https://doi.org/10.18637/jss.v034.i02
David, A., Botías, C., Abdul-Sada, A., Nicholls, E., Rotheray, E. L., Hill, E. M., & Goulson, D. (2016). Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environment International, 88, 169-178. https://doi.org/10.1016/j.envint.2015.12.011
David, J. P., Boyer, S., Mesneau, A., Ball, A., Ranson, H., & Dauphin-Villemant, C. (2006). Involvement of cytochrome P450 monooxygenases in the response of mosquito larvae to dietary plant xenobiotics. Insect Biochemistry and Molecular Biology, 36(5), 410-420. https://doi.org/10.1016/J.IBMB.2006.02.004
Demidenko, E., & Miller, T. W. (2019). Statistical determination of synergy based on bliss definition of drugs independence. PLoS One, 14(11), e0224137. https://doi.org/10.1371/journal.pone.0224137
Deutsch, C. A., Tewksbury, J. J., Huey, R. B., Sheldon, K. S., Ghalambor, C. K., Haak, D. C., & Martin, P. R. (2008). Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences of the United States of America, 105(18), 6668-6672. https://doi.org/10.1073/pnas.070947210
Dively, G. P., & Kamel, A. (2012). Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. Journal of Agricultural and Food Chemistry, 60(18), 4449-4456. https://doi.org/10.1021/jf205393x
Dorian, N. N., McCarthy, M. W., & Crone, E. E. (2022). Ecological traits explain long-term phenological trends in solitary bees. Journal of Animal Ecology, 92(2), 285-296. https://doi.org/10.1111/1365-2656.13778
Doublet, V., Labarussias, M., de Miranda, J. R., Moritz, R. F. A., & Paxton, R. J. (2015). Bees under stress: Sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environmental Microbiology, 17(4), 969-983. https://doi.org/10.1111/1462-2920.12426
European Food Safety Authority (EFSA). (2013). Guidance document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA Journal, 11(7), 3295. https://doi.org/10.2903/j.efsa.2013.3295
Fischer, K., Klockmann, M., & Reim, E. (2014). Strong negative effects of simulated heat waves in a tropical butterfly. Journal of Experimental Biology, 217(16), 2892-2898. https://doi.org/10.1242/jeb.106245
Fliszkiewicz, M., Giejdasz, K., Wasielewski, O., & Krishnan, N. (2012). Influence of winter temperature and simulated climate change on body mass and fat body depletion during diapause in adults of the solitary bee, Osmia rufa (Hymenoptera: Megachilidae). Environmental Entomology, 41(6), 1621-1630. https://doi.org/10.1603/EN12004
González-Tokman, D., Córdoba-Aguilar, A., Dáttilo, W., Lira-Noriega, A., Sánchez-Guillén, R. A., & Villalobos, F. (2020). Insect responses to heat: Physiological mechanisms, evolution and ecological implications in a warming world. Biological Reviews, 95(3), 802-821. https://doi.org/10.1111/BRV.12588
Goulson, D., Nicholls, E., Botias, C., & Rotheray, E. L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229), 1255957. https://doi.org/10.1126/science.1255957
Grab, H., Brokaw, J., Anderson, E., Gedlinske, L., Gibbs, J., Wilson, J., Loeb, G., Isaacs, R., & Poveda, K. (2019). Habitat enhancements rescue bee body size from the negative effects of landscape simplification. Journal of Applied Ecology, 56(9), 2144-2154. https://doi.org/10.1111/1365-2664.13456
Grassl, J., Holt, S., Cremen, N., Peso, M., Hahne, D., & Baer, B. (2018). Synergistic effects of pathogen and pesticide exposure on honey bee (Apis mellifera) survival and immunity. Journal of Invertebrate Pathology, 159, 78-86. https://doi.org/10.1016/j.jip.2018.10.005
Hahn, D. A., & Denlinger, D. L. (2007). Meeting the energetic demands of insect diapause: Nutrient storage and utilization. Journal of Insect Physiology, 53(8), 760-773. https://doi.org/10.1016/j.jinsphys.2007.03.018
Heller, S., Joshi, N. K., Chen, J., Rajotte, E. G., Mullin, C., & Biddinger, D. J. (2020). Pollinator exposure to systemic insecticides and fungicides applied in the previous fall and pre-bloom period in apple orchards. Environmental Pollution, 265, 114589. https://doi.org/10.1016/j.envpol.2020.114589
Herrera, C. M., Núñez, A., Valverde, J., & Alonso, C. (2023). Body mass decline in a Mediterranean community of solitary bees supports the size shrinking effect of climatic warming. Ecology, e4128. https://doi.org/10.1002/ecy.4128
Hladik, M. L., Vandever, M., & Smalling, K. L. (2016). Exposure of native bees foraging in an agricultural landscape to current-use pesticides. Science of the Total Environment, 542, 469-477. https://doi.org/10.1016/j.scitotenv.2015.10.077
IPBES. (2021). Scoping report for a thematic assessment of the underlying causes of biodiversity loss and the determinants of transformative change and options for achieving the 2050 vision for biodiversity (transformative change assessment). Annex II to decision IPBES-8/1. IPBES Secretariat.
Jaumejoan, X., Arnan, X., Hagenbucher, S., Rodrigo, A., Sédivy, C., & Bosch, J. (2023). Different effects of local and landscape context on pollen foraging decisions by two managed orchard pollinators, Osmia cornuta and Bombus terrestris. Agriculture, Ecosystems & Environment, 353, 108528. https://doi.org/10.1016/j.agee.2023.108528
Jean, C., Coderre, D., & Tourneur, J. C. (1990). Effects of temperature and substrate on survival and lipid consumption of hibernating Coleomegilla maculata lengi (Coleoptera: Coccinellidae). Environmental Entomology, 19(6), 1657-1662. https://doi.org/10.1093/EE/19.6.1657
Kassambara, A., Kosinski, M., Biecek, P., & Fabian, S. (2020). Survminer: Drawing Survival Curves using “ggplot2”. R package version 0.4, 8, 556. https://CRAN.R-project.org/package=survminer
Keeley, L. L. (1985). Physiology and biochemistry of the fat body. In G. A. Kerkut & L. I. Gilbert (Eds.), Comprehensive insect physiology, biochemistry and pharmacology (Vol. 3, pp. 211-248). Pergamon Press.
Kerr, J. T., Pindar, A., Galpern, P., Packer, L., Potts, S. G., Roberts, S. M., Rasmont, P., Schweiger, O., Colla, S. R., Richardson, L. L., Wagner, D. L., Gall, L. F., Sikes, D., & Pantoja, A. (2015). Climate change impacts on bumblebees converge across continents. Science, 349(6244), 177-180. https://doi.org/10.1126/science.aaa7031
Kierat, J., Szentgyörgyi, H., Czarnoleski, M., & Woyciechowski, M. (2017). The thermal environment of the nest affects body and cell size in the solitary red mason bee (Osmia bicornis L.). Journal of Thermal Biology, 68, 39-44. https://doi.org/10.1016/j.jtherbio.2016.11.008
Klein, A. M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274(1608), 303-313. https://doi.org/10.1098/rspb.2006.3721
Klein, S., Cabirol, A., Devaud, J. M., Barron, A. B., & Lihoreau, M. (2017). Why bees are so vulnerable to environmental stressors. Trends in Ecology & Evolution, 32(4), 268-278. https://doi.org/10.1016/j.tree.2016.12.009
Klepsatel, P., Gáliková, M., Xu, Y., & Kühnlein, R. P. (2016). Thermal stress depletes energy reserves in drosophila. Scientific Reports, 6(1), 1-12. https://doi.org/10.1038/srep33667
Knapp, J. L., Nicholson, C. C., Jonsson, O., de Miranda, J. R., & Rundlöf, M. (2023). Ecological traits interact with landscape context to determine bees' pesticide risk. Nature Ecology & Evolution, 7(4), 547-556. https://doi.org/10.1038/s41559-023-01990-5
Lenth, R., Singmann, H., Love, J., Buerkner, P., & Herve, M. (2019). Emmeans: Estimated marginal means, aka least-squares means. R package version, 1(3.4). https://CRAN.R-project.org/package=emmeans
Li, J., Zhao, L., Qi, S., Zhao, W., Xue, X., Wu, L., & Huang, S. (2021). Sublethal effects of IsoclastTM active (50% sulfoxaflor water dispersible granules) on larval and adult worker honey bees (Apis mellifera L.). Ecotoxicology and Environmental Safety, 220, 112379. https://doi.org/10.1016/j.ecoenv.2021.112379
Linguadoca, A., Jürison, M., Hellström, S., Straw, E. A., Šima, P., Karise, R., Costa, C., Serra, G., Colombo, R., Paxton, R. J., Mänd, M., & Brown, M. J. F. (2022). Intra-specific variation in sensitivity of Bombus terrestris and Osmia bicornis to three pesticides. Scientific Reports, 12(1), 17311. https://doi.org/10.1038/s41598-022-22239-4
Linguadoca, A., Rizzi, C., Villa, S., & Brown, M. J. F. (2021). Sulfoxaflor and nutritional deficiency synergistically reduce survival and fecundity in bumblebees. Science of the Total Environment, 795, 148680. https://doi.org/10.1016/j.scitotenv.2021.148680
Lycett, G. J., McLaughlin, L. A., Ranson, H., Hemingway, J., Kafatos, F. C., Loukeris, T. G., & Paine, M. J. I. (2006). Anopheles gambiae P450 reductase is highly expressed in oenocytes and in vivo knockdown increases permethrin susceptibility. Insect Molecular Biology, 15(3), 321-327. https://doi.org/10.1111/j.1365-2583.2006.00647.x
Martelli, F., Zhongyuan, Z., Wang, J., Wong, C. O., Karagas, N. E., Roessner, U., Rupasinghe, T., Venkatachalam, K., Perry, T., Bellen, H. J., & Batterham, P. (2020). Low doses of the neonicotinoid insecticide imidacloprid induce ROS triggering neurological and metabolic impairments in drosophila. Proceedings of the National Academy of Sciences of the United States of America, 117(41), 25840-25850. https://doi.org/10.1073/pnas.2011828117/suppl_file/pnas.2011828117.sapp.pdf
Moss, R. H., Edmonds, J. A., Hibbard, K. A., Manning, M. R., Rose, S. K., Van Vuuren, D. P., Carter, T. R., Emori, S., Kainuma, M., Kram, T., Meehl, G. A., Mitchell, J. F. B., Nakicenovic, N., Riahi, K., Smith, S. J., Stouffer, R. J., Thomson, A. M., Weyant, J. P., & Wilbanks, T. J. (2010). The next generation of scenarios for climate change research and assessment. Nature, 463(7282), 747-756. https://doi.org/10.1038/nature08823
Müller, A. (2022). Palaearctic osmiine bees. ETH Zürich. http://blogs.ethz.ch/osmiini
Nestel, D., Papadopoulos, N. T., Pascacio-Villafán, C., Righini, N., Altuzar-Molina, A. R., & Aluja, M. (2016). Resource allocation and compensation during development in holometabolous insects. Journal of Insect Physiology, 95, 78-88. https://doi.org/10.1016/J.JINSPHYS.2016.09.010
Neven, L. G. (2000). Physiological responses of insects to heat. Postharvest Biology and Technology, 21(1), 103-111. https://doi.org/10.1016/S0925-5214(00)00169-1
Oliveira, M. O., Freitas, B. M., Scheper, J., & Kleijn, D. (2016). Size and sex-dependent shrinkage of dutch bees during one and a half centuries of land-use change. PLoS One, 11(2), e0148983. https://doi.org/10.1371/journal.pone.0148983
Oller, R., & Langohr, K. (2017). FHtest: An R package for the comparison of survival curves with censored data. Journal of Statistical Software, 81, 1-25. https://doi.org/10.18637/jss.v081.i15
Ollerton, J., Winfree, R., & Tarrant, S. (2011). How many flowering plants are pollinated by animals? Oikos, 120(3), 321-326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Ostap-Chec, M., Kierat, J., Kuszewska, K., & Woyciechowski, M. (2021). Red mason bee (Osmia bicornis) thermal preferences for nest sites and their effects on offspring survival. Apidologie, 52(3), 707-719. https://doi.org/10.1007/s13592-021-00858-6
Petersen, R. A., Zangerl, A. R., Berenbaum, M. R., & Schuler, M. A. (2001). Expression of CYP6B1 and CYP6B3 cytochrome P450 monooxygenases and furanocoumarin metabolism in different tissues of Papilio polyxenes (Lepidoptera: Papilionidae). Insect Biochemistry and Molecular Biology, 31(6-7), 679-690. https://doi.org/10.1016/S0965-1748(00)00174-0
Pettis, J. S., Vanengelsdorp, D., Johnson, J., & Dively, G. (2012). Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften, 99, 153-158. https://doi.org/10.1007/S00114-011-0881-1/tables/1
Portner, H. O. (2002). Climate variations and the physiological basis of temperature dependent biogeography: Systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 132(4), 739-761. https://doi.org/10.1016/S1095-6433(02)00045-4
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., & Kunin, W. E. (2010). Global pollinator declines: Trends, impacts and drivers. Trends in Ecology & Evolution, 25(6), 345-353. https://doi.org/10.1016/j.tree.2010.01.007
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-project.org/
Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., Lim, D., Joklik, J., Cicero, J. M., Ellis, J. D., Hawthorne, D., & Van Engelsdorp, D. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences of the United States of America, 116(5), 1792-1801. https://doi.org/10.1073/pnas.1818371116
Sanchez-Bayo, F., & Goka, K. (2014). Pesticide residues and bees-A risk assessment. PLoS One, 9(4), e94482. https://doi.org/10.1371/journal.pone.0094482
Sánchez-Bayo, F., & Wyckhuys, K. A. G. (2019). Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation, 232, 8-27. https://doi.org/10.1016/j.biocon.2019.01.020
Scheiner, R., Toteva, A., Reim, T., Søvik, E., & Barron, A. B. (2014). Differences in the phototaxis of pollen and nectar foraging honey bees are related to their octopamine brain titers. Frontiers in Physiology, 5, 116. https://doi.org/10.3389/fphys.2014.00116/bibtex
Schwartz, K. R., Minor, H., Magro, C., McConnell, J., Capani, J., Griffin, J., & Doebel, H. (2021). The neonicotinoid imidacloprid alone alters the cognitive behavior in Apis mellifera L. and the combined exposure of imidacloprid and Varroa destructor mites synergistically contributes to trial attrition. Journal of Apicultural Research, 60(3), 431-438. https://doi.org/10.1080/00218839.2020.1866233
Sgolastra, F., Arnan, X., Cabbri, R., Isani, G., Medrzycki, P., Teper, D., & Bosch, J. (2018). Combined exposure to sublethal concentrations of an insecticide and a fungicide affect feeding, ovary development and longevity in a solitary bee. Proceedings of the Royal Society B, 285(1885), 20180887. https://doi.org/10.1098/rspb.2018.0887
Sgolastra, F., Arnan, X., Pitts-Singer, T. L., Maini, S., Kemp, W. P., & Bosch, J. (2016). Pre-wintering conditions and post-winter performance in a solitary bee: Does diapause impose an energetic cost on reproductive success? Ecological Entomology, 41(2), 201-210. https://doi.org/10.1111/een.12292
Sgolastra, F., Bosch, J., Molowny-Horas, R., Maini, S., & Kemp, W. P. (2010). Effect of temperature regime on diapause intensity in an adult-wintering hymenopteran with obligate diapause. Journal of Insect Physiology, 56(2), 185-194. https://doi.org/10.1016/j.jinsphys.2009.10.001
Sgolastra, F., Hinarejos, S., Pitts-Singer, T. L., Boyle, N. K., Joseph, T., Lūckmann, J., Raine, N. E., Singh, R., Williams, N. M., & Bosch, J. (2019). Pesticide exposure assessment paradigm for solitary bees. Environmental Entomology, 48(1), 22-35. https://doi.org/10.1093/ee/nvy105
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. Journal of Insect Physiology, 57(12), 1651-1659. https://doi.org/10.1016/j.jinsphys.2011.08.017
Sgolastra, F., Kemp, W. P., Maini, S., & Bosch, J. (2012). Duration of prepupal summer dormancy regulates synchronization of adult diapause with winter temperatures in bees of the genus Osmia. Journal of Insect Physiology, 58(7), 924-933. https://doi.org/10.1016/j.jinsphys.2012.04.008
Siviter, H., Bailes, E. J., Martin, C. D., Oliver, T. R., Koricheva, J., Leadbeater, E., & Brown, M. J. F. (2021). Agrochemicals interact synergistically to increase bee mortality. Nature, 596(7872), 389-392. https://doi.org/10.1038/s41586-021-03787-7
Siviter, H., Horner, J., Brown, M. J. F., & Leadbeater, E. (2020). Sulfoxaflor exposure reduces egg laying in bumblebees Bombus terrestris. Journal of Applied Ecology, 57(1), 160-169. https://doi.org/10.1111/1365-2664.13519
Siviter, H., Linguadoca, A., Ippolito, A., & Muth, F. (2023). Pesticide licensing in the EU and protecting pollinators. Current Biology, 33(2), R44-R48. https://doi.org/10.1016/j.cub.2022.12.002
Skowronek, P., Wójcik, Ł., Strachecka, A., & Brivio, F. (2021). Fat body-multifunctional insect tissue. Insects, 12(6), 547. https://doi.org/10.3390/insects12060547
Sparks, T. C., Watson, G. B., Loso, M. R., Geng, C., Babcock, J. M., & Thomas, J. D. (2013). Sulfoxaflor and the sulfoximine insecticides: Chemistry, mode of action and basis for efficacy on resistant insects. Pesticide Biochemistry and Physiology, 107(1), 1-7. https://doi.org/10.1016/j.pestbp.2013.05.014
Sponsler, D. B., Grozinger, C. M., Hitaj, C., Rundlöf, M., Botías, C., Code, A., Lonsdorf, E. V., Melathopoulos, A. P., Smith, D. J., Suryanarayanan, S., Thogmartin, W. G., Williams, N. M., Zhang, M., & Douglas, M. R. (2019). Pesticides and pollinators: A socioecological synthesis. Science of the Total Environment, 662, 1012-1027. https://doi.org/10.1016/j.scitotenv.2019.01.016
Storey, K. B., & Storey, J. M. (2004). Metabolic rate depression in animals: Transcriptional and translational controls. Biological Reviews, 79(1), 207-233. https://doi.org/10.1017/S1464793103006195
Therneau, T., Crowson, C., & Atkinson, E. (2020). Multi-state models and competing risks. https://cran.r-project.org/web/packages/survival/vignettes/compete.pdf
Thompson, H. (2016). Extrapolation of acute toxicity across bee species. Integrated Environmental Assessment and Management, 12(4), 622-626. https://doi.org/10.1002/ieam.1737
Tong, L., Nieh, J. C., & Tosi, S. (2019). Combined nutritional stress and a new systemic pesticide (flupyradifurone, Sivanto®) reduce bee survival, food consumption, flight success, and thermoregulation. Chemosphere, 237, 124408. https://doi.org/10.1016/j.chemosphere.2019.124408
Tosi, S., Nieh, J. C., Sgolastra, F., Cabbri, R., & Medrzycki, P. (2017). Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees. Proceedings of the Royal Society B: Biological Sciences, 284(1869), 20171711. https://doi.org/10.1098/RSPB.2017.1711
United States Environmental Protection Agency (USEPA). (2019). Ecological risk assessment for the registration review of sulfoxaflor. United States Environmental Protection Agency.
Vanbergen, A. J. (2021). A cocktail of pesticides, parasites and hunger leaves bees down and out. Nature, 596, 351-352. https://doi.org/10.1038/d41586-021-02079-4
Vesterlund, S. R., Lilley, T. M., van Ooik, T., & Sorvari, J. (2014). The effect of overwintering temperature on the body energy reserves and phenoloxidase activity of bumblebee Bombus lucorum queens. Insectes Sociaux, 61, 265-272. https://doi.org/10.1007/S00040-014-0351-9/figures/6
Vidau, C., Diogon, M., Aufauvre, J., Gis Fontbonne, R., Viguè, B., Brunet, J.-L., Texier, C., Biron, D. G., Blot, N., El Alaoui, H., Belzunces, L. P., & Delbac, F. (2011). Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS One, 6, e21550. https://doi.org/10.1371/journal.pone.0021550
Williams, C. M., Marshall, K. E., MacMillan, H. A., Dzurisin, J. D. K., Hellmann, J. J., & Sinclair, B. J. (2012). Thermal variability increases the impact of autumnal warming and drives metabolic depression in an overwintering butterfly. PLoS One, 7(3), e34470. https://doi.org/10.1371/journal.pone.0034470
Zaragoza-Trello, C., Vilà, M., Botías, C., & Bartomeus, I. (2021). Interactions among global change pressures act in a non-additive way on bumblebee individuals and colonies. Functional Ecology, 35(2), 420-434. https://doi.org/10.1111/1365-2435.13703
Zhang, W., Chang, X. Q., Hoffmann, A. A., Zhang, S., & Ma, C. S. (2015). Impact of hot events at different developmental stages of a moth: The closer to adult stage, the less reproductive output. Scientific Reports, 5(1), 1-9. https://doi.org/10.1038/srep10436
Zhu, Y. C., Yao, J., & Wang, Y. (2022). Varroa mite and deformed wing virus infestations interactively make honey bees (Apis mellifera) more susceptible to insecticides. Environmental Pollution, 292, 118212. https://doi.org/10.1016/j.envpol.2021.118212

Auteurs

Sergio Albacete (S)

Universitat Autònoma de Barcelona, Bellaterra, Spain.
Centre for Ecological Research and Forestry Applications (CREAF), Bellaterra, Spain.

Gonzalo Sancho (G)

Universitat Autònoma de Barcelona, Bellaterra, Spain.
Centre for Ecological Research and Forestry Applications (CREAF), Bellaterra, Spain.

Celeste Azpiazu (C)

Universitat Autònoma de Barcelona, Bellaterra, Spain.
Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Barcelona, Spain.

Anselm Rodrigo (A)

Universitat Autònoma de Barcelona, Bellaterra, Spain.
Centre for Ecological Research and Forestry Applications (CREAF), Bellaterra, Spain.

Roberto Molowny-Horas (R)

Universitat Autònoma de Barcelona, Bellaterra, Spain.
Centre for Ecological Research and Forestry Applications (CREAF), Bellaterra, Spain.

Fabio Sgolastra (F)

Dipartimento di Scienze e Tecnologie Agro-Alimentari, Alma Mater Studiorum Università di Bologna, Bologna, Italy.

Jordi Bosch (J)

Universitat Autònoma de Barcelona, Bellaterra, Spain.
Centre for Ecological Research and Forestry Applications (CREAF), Bellaterra, Spain.

Classifications MeSH