Anthophila; Heavy metal; Metalloid; Trace Elements; Xenobiotics
Abstract :
[en] The pervasiveness of human imprint on Earth is alarming and most animal species, including bees (Hymenoptera: Apoidea: Anthophila), must cope with several stressors. Recently, exposure to trace metals and metalloids (TMM) has drawn attention and has been suggested as a threat for bee populations. In this review, we aimed at bringing together all the studies (n = 59), both in laboratories and in natura, that assessed the effects of TMM on bees. After a brief comment on semantics, we listed the potential routes of exposure to soluble and insoluble (i.e. nanoparticle) TMM, and the threat posed by metallophyte plants. Then, we reviewed the studies that addressed whether bees could detect and avoid TMM in their environment, as well as the ways bee detoxify these xenobiotics. Afterwards, we listed the impacts TMM have on bees at the community, individual, physiological, histological and microbial levels. We discussed around the interspecific variations among bees, as well as around the simultaneous exposure to TMM. Finally, we highlighted that bees are likely exposed to TMM in combination or with other stressors, such as pesticides and parasites. Overall, we showed that most studies focussed on the domesticated western honey bee and mainly addressed lethal effects. Because TMM are widespread in the environment and have been shown to result in detrimental consequences, evaluating their lethal and sublethal effects on bees, including non-Apis species, warrants further investigations.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Gekiere, Antoine ; Université de Mons - UMONS > Faculté des Sciences > Service de Zoologie
Vanderplanck, Maryse ; Université de Mons - UMONS > Facult?des Sciences > Service de Zoologie ; CEFE, Univ Montpellier, CNRS, EPHE, IRD, 1919 Route de Mende, 34090 Montpellier, France. Electronic address: maryse.vanderplanck@cefe.cnrs.fr
Michez, Denis ; Université de Mons - UMONS > Faculté des Sciences > Service de Zoologie
Language :
English
Title :
Trace metals with heavy consequences on bees: A comprehensive review
A.G. is supported by a F.R.S.-FNRS PhD grant ‘Aspirant’. D.M. has received funding from the European Union 's Horizon 2020 Research and Innovation Programme under grant agreement No 773921 for the POSHBEE project. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Abdalla, F.C., Domingues, C.E. da C., Hepato-nephrocitic system: a novel model of biomarkers for analysis of the ecology of stress in environmental biomonitoring. PLoS One, 10(7), 2015, e0132349, 10.1371/journal.pone.0132349.
Adachi, K., Tainosho, Y., Characterization of heavy metal particles embedded in tire dust. Environ. Int. 30:8 (2004), 1009–1017, 10.1016/j.envint.2004.04.004.
Aguilera, A., Bautista, F., Gutiérrez-Ruiz, M., Ceniceros-Gómez, A.E., Cejudo, R., Goguitchaichvili, A., Heavy metal pollution of street dust in the largest city of Mexico, sources and health risk assessment. Environ. Monit. Assess., 193(4), 2021, 193, 10.1007/s10661-021-08993-4.
Aizen, M.A., Aguiar, S., Biesmeijer, J.C., Garibaldi, L.A., Inouye, D.W., Jung, C., Martins, D.J., Medel, R., Morales, C.L., Ngo, H., Pauw, A., Paxton, R.J., Sáez, A., Seymour, C.L., Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification. Glob. Chang. Biol. 25:10 (2019), 3516–3527, 10.1111/gcb.14736.
Al Naggar, Y., Dabour, K., Masry, S., Sadek, A., Naiem, E., Giesy, J.P., Sublethal effects of chronic exposure to CdO or PbO nanoparticles or their binary mixture on the honey bee (Apis mellifera L.). Environ. Sci. Pollut. Res. 27:16 (2020), 19004–19015, 10.1007/s11356-018-3314-2.
Al Naggar, Y., Brinkmann, M., Sayes, C.M., AL-Kahtani, S.N., Dar, S.A., El-Seedi, H.R., Grünewald, B., Giesy, J.P., Are honey bees at risk from microplastics?. Toxics, 9(5), 2021, 109, 10.3390/toxics9050109.
Al Naggar, Y., Singavarapu, B., Paxton, R.J., Wubet, T., Bees under interactive stressors: the novel insecticides flupyradifurone and sulfoxaflor along with the fungicide azoxystrobin disrupt the gut microbiota of honey bees and increase opportunistic bacterial pathogens. Sci. Total Environ., 849, 2022, 157941.
Alaerjani, W.M.A., Abu-Melha, S., Alshareef, R.M.H., Al-Farhan, B.S., Ghramh, H.A., Al-Shehri, B.M.A., Bajaber, M.A., Khan, K.A., Alrooqi, M.M., Modawe, G.A., Mohammed, M.E.A., Biochemical reactions and their biological contributions in honey. Molecules, 27(15), 2022, 4719, 10.3390/molecules27154719.
Alford, D.V., Bumblebees. 1975, Davis-Poynter.
Ali, H., Khan, E., Sajad, M.A., Phytoremediation of heavy metals - concepts and applications. Chemosphere 91:7 (2013), 869–881, 10.1016/j.chemosphere.2013.01.075.
Alloway, B.J., Heavy Metals in Soils-Trace Metals and Metalloids in Soils and their Bioavailability. Third Edit, 2013, Springer.
Anderson, K.E., Ricigliano, V.A., Honey bee gut dysbiosis: a novel context of disease ecology. Curr. Opin. Insect. Sci. 22 (2017), 125–132, 10.1016/j.cois.2017.05.020.
Arena, M., Sgolastra, F., A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23:3 (2014), 324–334, 10.1007/s10646-014-1190-1.
Astolfi, M.L., Conti, M.E., Messi, M., Marconi, E., Probiotics as a promising prophylactic tool to reduce levels of toxic or potentially toxic elements in bees. Chemosphere, 308(P1), 2022, 136261, 10.1016/j.chemosphere.2022.136261.
Atkins, P., Jones, L., Chemistry—Molecules, Matter and Change. Third Edit, 1997, W.H. Freeman & Co.
Badiou-Bénéteau, A., Benneveau, A., Géret, F., Delatte, H., Becker, N., Brunet, J.L., Reynaud, B., Belzunces, L.P., Honeybee biomarkers as promising tools to monitor environmental quality. Environ. Int. 60 (2013), 31–41, 10.1016/j.envint.2013.07.002.
Baracchi, D., Brown, M.J.F., Chittka, L., Behavioural evidence for self-medication in bumblebees?. F1000Res., 4(0), 2015, 73, 10.12688/f1000research.6262.3.
Ben-Shahar, Y., Dudek, N.L., Robinson, G.E., Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor. J. Exp. Biol. 207:19 (2004), 3281–3288, 10.1242/jeb.01151.
Bernardes, R.C., Fernandes, K.M., Bastos, D.S.S., Freire, A.F.P.A., Lopes, M.P., de Oliveira, L.L., Tavares, M.G., dos Santos Araújo, R., Martins, G.F., Impact of copper sulfate on survival, behavior, midgut morphology, and antioxidant activity of Partamona helleri (Apidae: Meliponini). Environ. Sci. Pollut. Res. 29:4 (2021), 6294–6305, 10.1007/s11356-021-16109-1.
Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J., Kunin, W.E., Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:5785 (2006), 351–354, 10.1126/science.1127863.
Bonilla-Rosso, G., Engel, P., Functional roles and metabolic niches in the honey bee gut microbiota. Curr. Opin. Microbiol. 43 (2018), 69–76, 10.1016/j.mib.2017.12.009.
Borsuk, G., Sulborska, A., Stawiarz, E., Olszewski, K., Wiącek, D., Ramzi, N., Nawrocka, A., Jędryczka, M., Capacity of honeybees to remove heavy metals from nectar and excrete the contaminants from their bodies. Apidologie 52:6 (2021), 1098–1111, 10.1007/s13592-021-00890-6.
Botina, L.L., Vélez, M., Barbosa, W.F., Mendonça, A.C., Pylro, V.S., Tótola, M.R., Martins, G.F., Behavior and gut bacteria of Partamona helleri under sublethal exposure to a bioinsecticide and a leaf fertilizer. Chemosphere 234 (2019), 187–195, 10.1016/j.chemosphere.2019.06.048.
Bounias, M., Kruk, I., Nectoux, M., Popeskovic, D., Toxicology of cupric salts on honeybees. V. Gluconate and sulfate action on gut alkaline and acid phosphatases. Ecotoxicol. Environ. Saf. 35:1 (1996), 67–76, 10.1006/eesa.1996.0082.
Bower, J.J., Leonard, S.S., Shi, X., Molecular mechanisms of metal toxicity and carcinogenesis. Mol. Cell. Biochem. 279:1–2 (2005), 3–15, 10.1007/s11010-005-8210-7.
Bromenshenk, J.J., Gudatis, J.L., Carlson, S.R., Thomas, J.M., Simmons, M.A., Population dynamics of honey bee nucleus colonies exposed to industrial pollutants. Apidologie 22:4 (1991), 359–369, 10.1051/apido:19910401.
Brown, M.J.F., Complex networks of parasites and pollinators: moving towards a healthy balance. Philos. Trans. R. Soc. B: Biol. Sci., 377(1853), 2022, 10.1098/rstb.2021.0161.
Brown, M.J.F., Dicks, L.V., Paxton, R.J., Baldock, K.C.R., Barron, A.B., Chauzat, M.-P., Freitas, B.M., Goulson, D., Jepsen, S., Kremen, C., Li, J., Neumann, P., Pattemore, D.E., Potts, S.G., Schweiger, O., Seymour, C.L., Stout, J.C., A horizon scan of future threats and opportunities for pollinators and pollination. PeerJ, 4(9), 2016, e2249, 10.7717/peerj.2249.
Bugin, G., Lenzi, L., Ranzani, G., Barisan, L., Porrini, C., Zanella, A., Bolzonella, C., Agriculture and pollinating insects, no longer a choice but a need: EU agriculture's dependence on pollinators in the 2007–2019 period. Sustainability, 14(6), 2022, 3644, 10.3390/su14063644.
Caliani, I., Campani, T., Conti, B., Cosci, F., Bedini, S., D'Agostino, A., Ammendola, A., Di Noi, A., Gori, A., Casini, S., Multi-biomarker approach and IBR index to evaluate the effects of different contaminants on the ecotoxicological status of Apis mellifera. Ecotoxicol. Environ. Saf., 208, 2021, 111486, 10.1016/j.ecoenv.2020.111486.
Ceschi-Bertoli, L., Vidal, F.A.P., Balsamo, P.J., Abdalla, F.C., Comet assay protocol for Bombus atratus fat body and pericardial cells (hymenoptera, bombini) at a safe concentration of mercury. Chemosphere, 261, 2020, 127752, 10.1016/j.chemosphere.2020.127752.
Chaplin-Kramer, R., Sharp, R.P., Weil, C., Bennett, E.M., Pascual, U., Arkema, K.K., Brauman, K.A., Bryant, B.P., Guerry, A.D., Haddad, N.M., Hamann, M., Hamel, P., Johnson, J.A., Mandle, L., Pereira, H.M., Polasky, S., Ruckelshaus, M., Shaw, M.R., Silver, J.M., Vogl, A.L., Daily, G.C., Global modeling of nature's contributions to people. Science 366:6462 (2019), 255–258, 10.1126/science.aaw3372.
Chapman, P.M., Holzmann, M., Heavy metal—music, not science. Environ. Sci. Technol., 41(12), 2007, 6, 10.1021/es072552o.
Costa, A., Veca, M., Barberis, M., Tosti, A., Notaro, G., Nava, S., Lazzari, M., Agazzi, A., Tangorra, F.M., Heavy metals on honeybees indicate their concentration in the atmosphere. A proof of concept. Ital. J. Anim. Sci. 18:1 (2019), 309–315, 10.1080/1828051X.2018.1520052.
Crichton, R.R., An overview of the role of metals in biology. Practical Approaches to Biological Inorganic Chemistry, 2020, Elsevier, 1–16, 10.1016/B978-0-444-64225-7.00001-8.
Cronn, R.C., Determination of cadmium toxicity and the relationship between dose and metallothionein le dose and metallothionein levels in the honey bee, Apis mellifera. [University of Montana] https://scholarworks.umt.edu/etd/2032, 1991.
Dabour, K., Al Naggar, Y., Masry, S., Naiem, E., Giesy, J.P., Cellular alterations in midgut cells of honey bee workers (Apis mellifera L.) exposed to sublethal concentrations of CdO or PbO nanoparticles or their binary mixture. Sci. Total Environ. 651 (2019), 1356–1367, 10.1016/j.scitotenv.2018.09.311.
Dağlıoğlu, Y., Kabakcı, D., Akdeniz, G., Toxicity of nano and non-nano boron particles on Apis mellifera (honey bee). Res. J. Environ. Sci. 3:3 (2015), 6–13.
Dallinger, R., Chapter 14. Strategies of metal detoxification in terrestrial invertebrates. Dalling, R., (eds.) Ecotoxicology of Metals in Invertebrates, Issue December 2016, 1993, Lewis, Boca Raton, 245–289.
Dalvi, A.A., Bhalerao, S.A., Response of plants towards heavy metal toxicity: an overview of avoidance, tolerance and uptake mechanism. Ann. Plant Sci. 2:09 (2013), 362–368.
de Brito Sanchez, M.G., Taste perception in honey bees. Chem. Senses 36:8 (2011), 675–692, 10.1093/chemse/bjr040.
De Temmerman, L., Vanongeval, L., Boon, W., Hoenig, M., Geypens, M., Heavy metal content of arable soils in northern Belgium. Water Air Soil Pollut. 148:1–4 (2003), 61–76, 10.1023/A:1025498629671.
Defarge, N., Spiroux de Vendômois, J., Séralini, G.E., Toxicity of formulants and heavy metals in glyphosate-based herbicides and other pesticides. Toxicol. Rep. 5 (2018), 156–163, 10.1016/j.toxrep.2017.12.025.
Di, N., Hladun, K.R., Zhang, K., Liu, T.-X., Trumble, J.T., Laboratory bioassays on the impact of cadmium, copper and lead on the development and survival of honeybee (Apis mellifera L.) larvae and foragers. Chemosphere 152 (2016), 530–538, 10.1016/j.chemosphere.2016.03.033.
Di, N., Zhang, K., Hladun, K.R., Rust, M., Chen, Y.-F., Zhu, Z.-Y., Liu, T.-X., Trumble, J.T., Joint effects of cadmium and copper on Apis mellifera foragers and larvae. Comp. Biochem. Physiol. Part - C: Toxicol. Pharmacol, 237, 2020, 108839, 10.1016/j.cbpc.2020.108839.
Díaz, S., Pascual, U., Stenseke, M., Martín-López, B., Watson, R.T., Molnár, Z., Hill, R., Chan, K.M.A., Baste, I.A., Brauman, K.A., Polasky, S., Church, A., Lonsdale, M., Larigauderie, A., Leadley, P.W., van Oudenhoven, A.P.E., van der Plaat, F., Schröter, M., Lavorel, S., Aumeeruddy-Thomas, Y., Bukvareva, E., Davies, K., Demissew, S., Erpul, G., Failler, P., Guerra, C.A., Hewitt, C.L., Keune, H., Lindley, S., Shirayama, Y., Assessing nature's contributions to people. Science 359:6373 (2018), 270–272, 10.1126/science.aap8826.
Dicks, L.V., Breeze, T.D., Ngo, H.T., Senapathi, D., An, J., Aizen, M.A., Basu, P., Buchori, D., Galetto, L., Garibaldi, L.A., Gemmill-Herren, B., Howlett, B.G., Imperatriz-Fonseca, V.L., Johnson, S.D., Kovács-Hostyánszki, A., Kwon, Y.J., Lattorff, H.M.G., Lungharwo, T., Seymour, C.L., Vanbergen, A.J., Potts, S.G., A global-scale expert assessment of drivers and risks associated with pollinator decline. Nat. Ecol. Evol 5:10 (2021), 1453–1461, 10.1038/s41559-021-01534-9.
Duffus, J.H., “Heavy metals” a meaningless term? (IUPAC technical report). Pure Appl. Chem. 74:5 (2002), 793–807, 10.1351/pac200274050793.
Edelstein, M., Ben-Hur, M., Heavy metals and metalloids: sources, risks and strategies to reduce their accumulation in horticultural crops. Sci. Hortic. 234 (2018), 431–444, 10.1016/j.scienta.2017.12.039.
El Kholy, S., Al Naggar, Y., Exposure to a sublethal concentration of CdO nanoparticles impairs the vision of the fruit fly (Drosophila melanogaster) by disrupting histamine synthesis and recycling mechanisms. Environ. Sci. Pollut. Res. 30 (2023), 27936–27947, 10.1007/s11356-022-24034-0.
El Kholy, S., Giesy, J.P., Al Naggar, Y., Consequences of a short-term exposure to a sub lethal concentration of CdO nanoparticles on key life history traits in the fruit fly (Drosophila melanogaster). J. Hazard. Mater., 410, 2021, 124671, 10.1016/j.jhazmat.2020.124671.
Eskov, E.K., Eskova, M.D., Dubovik, V.A., Vyrodov, I.V., Content of heavy metals in melliferous vegetation, bee bodies, and beekeeping production. Russ. Agric. Sci. 41:5 (2015), 396–398, 10.3103/S1068367415050079.
Evans, J.D., Aronstein, K., Chen, Y.P., Hetru, C., Imler, J.L., Jiang, H., Kanost, M., Thompson, G.J., Zou, Z., Hultmark, D., Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15:5 (2006), 645–656, 10.1111/j.1365-2583.2006.00682.x.
Feldhaar, H., Otti, O., Pollutants and their interaction with diseases of social hymenoptera. Insects 11:153 (2020), 1–20, 10.3390/insects11030153.
Filipiak, M., Woyciechowski, M., Czarnoleski, M., Stoichiometric niche, nutrient partitioning and resource allocation in a solitary bee are sex-specific and phosphorous is allocated mainly to the cocoon. Sci. Rep. 11:1 (2021), 1–12, 10.1038/s41598-020-79647-7.
Filipiak, Z.M., Denisow, B., Stawiarz, E., Filipiak, M., Unravelling the dependence of a wild bee on floral diversity and composition using a feeding experiment. Sci. Total Environ., 820, 2022, 153326, 10.1016/j.scitotenv.2022.153326.
Gauthier, M., Aras, P., Jumarie, C., Boily, M., Low dietary levels of Al, Pb and cd may affect the non-enzymatic antioxidant capacity in caged honey bees (Apis mellifera). Chemosphere 144 (2016), 848–854, 10.1016/j.chemosphere.2015.09.057.
Ghosh, S., Namin, S.M., Jung, C., Differential bacterial community of bee bread and bee pollen revealed by 16s rRNA high-throughput sequencing. Insects, 13(10), 2022, 863, 10.3390/insects13100863.
Gizaw, G., Kim, Y., Moon, K., Choi, J.B., Kim, Y.H., Park, J.K., Effect of environmental heavy metals on the expression of detoxification-related genes in honey bee Apis mellifera. Apidologie 51:4 (2020), 664–674, 10.1007/s13592-020-00751-8.
Glavan, G., Milivojević, T., Božič, J., Sepčić, K., Drobne, D., Feeding preference and sub-chronic effects of ZnO nanomaterials in honey bees (Apis mellifera carnica). Arch. Environ. Contam. Toxicol. 72:3 (2017), 471–480, 10.1007/s00244-017-0385-x.
Gradish, A.E., Van Der Steen, J., Scott-Dupree, C.D., Cabrera, A.R., Cutler, G.C., Goulson, D., Klein, O., Lehmann, D.M., Lückmann, J., O'Neill, B., Raine, N.E., Sharma, B., Thompson, H., Comparison of pesticide exposure in honey bees (hymenoptera: Apidae) and bumble bees (hymenoptera: Apidae): implications for risk assessments. Environ. Entomol. 48:1 (2019), 12–21, 10.1093/ee/nvy168.
Gustin, M.S., Hou, D., Tack, F.M.G., The term “heavy metal(s)”: history, current debate, and future use. Sci. Total Environ., 789, 2021, 147951, 10.1016/j.scitotenv.2021.147951.
Hallmann, C.A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., Stenmans, W., Müller, A., Sumser, H., Hörren, T., Goulson, D., De Kroon, H., More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One, 12(10), 2017, 10.1371/journal.pone.0185809.
Haynes, W.M., Abundance of elements in the earth's crust and in the sea. CRC Handbook of Chemistry and Physics, 97th Editi, 2017, CRC Press, 14–17.
He, Z.L., Yang, X.E., Stoffella, P.J., Trace elements in agroecosystems and impacts on the environment. J. Trace Elem. Med. Biol. 19:2–3 (2005), 125–140, 10.1016/j.jtemb.2005.02.010.
He, W., Guo, W., Qian, Y., Zhang, S., Ren, D., Liu, S., Synergistic hepatotoxicity by cadmium and chlorpyrifos: disordered hepatic lipid homeostasis. Mol. Med. Rep. 12:1 (2015), 303–308, 10.3892/mmr.2015.3381.
Heard, M.S., Baas, J., Dorne, J. Lou, Lahive, E., Robinson, A.G., Rortais, A., Spurgeon, D.J., Svendsen, C., Hesketh, H., Comparative toxicity of pesticides and environmental contaminants in bees: are honey bees a useful proxy for wild bee species?. Sci. Total Environ. 578 (2017), 357–365, 10.1016/j.scitotenv.2016.10.180.
Hladun, K.R., Parker, D.R., Trumble, J.T., Cadmium, copper, and lead accumulation and bioconcentration in the vegetative and reproductive organs of Raphanus sativus: implications for plant performance and pollination. J. Chem. Ecol. 41:4 (2015), 386–395, 10.1007/s10886-015-0569-7.
Hesketh, H., Lahive, E., Horton, A.A., Robinson, A.G., Svendsen, C., Rortais, A., Dorne, J.-L., Baas, J., Spurgeon, D.J., Heard, M.S., Extending standard testing period in honeybees to predict lifespan impacts of pesticides and heavy metals using dynamic energy budget modelling. Sci. Rep., 6, 2016, 37655, 10.1038/srep37655.
Hladun, K.R., Di, N., Liu, T., Trumble, J.T., Metal contaminant accumulation in the hive: consequences for whole-colony health and brood production in the honey bee (Apis mellifera L.). Environ. Toxicol. Chem. 35:2 (2016), 322–329, 10.1002/etc.3273.
Hrdina, A., Iatsenko, I., The roles of metals in insect–microbe interactions and immunity. Curr. Opin. Insect. Sci. 49 (2022), 71–77, 10.1016/j.cois.2021.12.004.
Hübner, R., Astin, K.B., Herbert, R.J.H., “Heavy metal” - time to move on from semantics to pragmatics?. J. Environ. Monit. 12:8 (2010), 1511–1514, 10.1039/c0em00056f.
Hurst, V., Stevenson, P.C., Wright, G.A., Toxins induce ‘malaise’ behaviour in the honeybee (Apis mellifera). J. Comp. Physiol. A. 200:10 (2014), 881–890, 10.1007/s00359-014-0932-0.
Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B.B., Beeregowda, K.N., Toxicity, mechanism and health effects of some heavy metals. Interdiscip. Toxicol. 7:2 (2014), 60–72, 10.2478/intox-2014-0009.
Jayakumar, M., Surendran, U., Raja, P., Kumar, A., Senapathi, V., A review of heavy metals accumulation pathways, sources and management in soils. Arab. J. Geosci., 14(20), 2021, 2156, 10.1007/s12517-021-08543-9.
Jumarie, C., Aras, P., Boily, M., Mixtures of herbicides and metals affect the redox system of honey bees. Chemosphere 168 (2017), 163–170, 10.1016/j.chemosphere.2016.10.056.
Kägi, J.H.R., Overview of metallothionein. Methods in Enzymology, Vol. 205, Issue 1981, 1991, 613–626, 10.1016/0076-6879(91)05145-L.
Kalbande, D.M., Dhadse, S.N., Chaudhari, P.R., Wate, S.R., Biomonitoring of heavy metals by pollen in urban environment. Environ. Monit. Assess. 138:1–3 (2008), 233–238, 10.1007/s10661-007-9793-0.
Kelly, F.J., Fussell, J.C., Size, source and chemical composition as determinants of toxicity attributable to ambient particulate matter. Atmos. Environ. 60 (2012), 504–526, 10.1016/j.atmosenv.2012.06.039.
Khalifa, S.A.M., Elshafiey, E.H., Shetaia, A.A., Abd El-Wahed, A.A., Algethami, A.F., Musharraf, S.G., AlAjmi, M.F., Zhao, C., Masry, S.H.D., Abdel-Daim, M.M., Halabi, M.F., Kai, G., Al Naggar, Y., Bishr, M., Diab, M.A.M., El-Seedi, H.R., Overview of bee pollination and its economic value for crop production. Insects, 12, 2021, 688, 10.3390/insects12080688.
Khodadadi, N., Amini, A., Dehbandi, R., Contamination, probabilistic health risk assessment and quantitative source apportionment of potentially toxic metals (PTMs) in street dust of a highly developed city in north of Iran. Environ. Res., 210, 2022, 112962, 10.1016/j.envres.2022.112962.
Klaus, F., Tscharntke, T., Bischoff, G., Grass, I., Floral resource diversification promotes solitary bee reproduction and may offset insecticide effects – evidence from a semi-field experiment. Ecol. Lett. 24:4 (2021), 668–675, 10.1111/ele.13683.
Koh, I., Lonsdorf, E.V., Williams, N.M., Brittain, C., Isaacs, R., Gibbs, J., Ricketts, T.H., Modeling the status, trends, and impacts of wild bee abundance in the United States. Proc. Natl. Acad. Sci. U. S. A. 113:1 (2016), 140–145, 10.1073/pnas.1517685113.
Kopit, A.M., Pitts-Singer, T.L., Routes of pesticide exposure in solitary, cavity-nesting bees. Environ. Entomol. 47:3 (2018), 499–510, 10.1093/ee/nvy034.
Kos, M., Jemec Kokalj, A., Glavan, G., Marolt, G., Zidar, P., Božič, J., Novak, S., Drobne, D., Cerium(IV) oxide nanoparticles induce sublethal changes in honeybees after chronic exposure. Environ. Sci. Nano 4:12 (2017), 2297–2310, 10.1039/C7EN00596B.
Kosior, A., Celary, W., Olejniczak, P., Fijał, J., Król, W., Solarz, W., Płonka, P., The decline of the bumble bees and cuckoo bees (hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41:1 (2007), 79–88, 10.1017/S0030605307001597.
Lado, L.R., Hengl, T., Reuter, H.I., Heavy metals in European soils: a geostatistical analysis of the FOREGS geochemical database. Geoderma 148:2 (2008), 189–199, 10.1016/j.geoderma.2008.09.020.
Li, Z., Qiu, Y., Li, J., Wan, K., Nie, H., Su, S., Chronic cadmium exposure induces impaired olfactory learning and altered brain gene expression in honey bees (Apis mellifera). Insects, 13(11), 2022, 988, 10.3390/insects13110988.
Lucchetti, M.A., Kilchenmann, V., Glauser, G., Praz, C., Kast, C., Nursing protects honeybee larvae from secondary metabolites of pollen. Proc. R. Soc. B Biol. Sci., 285(1875), 2018, 20172849, 10.1098/rspb.2017.2849.
Maret, W., The metals in the biological periodic system of the elements: concepts and conjectures. Int. J. Mol. Sci., 17(1), 2016, 66, 10.3390/ijms17010066.
Meindl, G.A., Ashman, T.L., The effects of aluminum and nickel in nectar on the foraging behavior of bumblebees. Environ. Pollut. 177 (2013), 78–81, 10.1016/j.envpol.2013.02.017.
Meindl, G.A., Ashman, T., Effects of floral metal accumulation on floral visitor communities: introducing the elemental filter hypothesis. Am. J. Bot. 102:3 (2015), 379–389, 10.3732/ajb.1400468.
Melchor-Martínez, E.M., Macias-Garbett, R., Malacara-Becerra, A., Iqbal, H.M.N., Sosa-Hernández, J.E., Parra-Saldívar, R., Environmental impact of emerging contaminants from battery waste: a mini review. Case Stud. Chem. Environ. Eng., 3, 2021, 100104, 10.1016/j.cscee.2021.100104.
Michez, D., Rasmont, P., Terzo, M., Vereecken, N.J., Bees of Europe (Hymenoptera of Europe Volume 1). 2019 (N.A.P. Edi).
Milchreit, K., Ruhnke, H., Wegener, J., Bienefeld, K., Effects of an insect growth regulator and a solvent on honeybee (Apis mellifera L.) brood development and queen viability. Ecotoxicology 25:3 (2016), 530–537, 10.1007/s10646-016-1611-4.
Milivojević, T., Glavan, G., Božič, J., Sepčić, K., Mesarič, T., Drobne, D., Neurotoxic potential of ingested ZnO nanomaterials on bees. Chemosphere 120 (2015), 547–554, 10.1016/j.chemosphere.2014.07.054.
Mockler, B.K., Kwong, W.K., Moran, N.A., Koch, H., Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Appl. Environ. Microbiol. 84:7 (2018), 1–11, 10.1128/AEM.02335-17.
Monchanin, C., Devaud, J.-M., Barron, A.B., Lihoreau, M., Current permissible levels of metal pollutants harm terrestrial invertebrates. Sci. Total Environ., 779, 2021, 146398, 10.1016/j.scitotenv.2021.146398.
Monchanin, C., Drujont, E., Devaud, J.-M., Lihoreau, M., Barron, A.B., Metal pollutants have additive negative effects on honey bee cognition. J. Exp. Biol., 224(12), 2021, 10.1242/jeb.241869.
Monchanin, C., Blanc-Brude, A., Drujont, E., Negahi, M.M., Pasquaretta, C., Silvestre, J., Baqué, D., Elger, A., Barron, A.B., Devaud, J.-M., Lihoreau, M., Chronic exposure to trace lead impairs honey bee learning. Ecotoxicol. Environ. Saf., 212, 2021, 112008, 10.1016/j.ecoenv.2021.112008.
Monchanin, C., de Brito, Gabriela, Sanchez, M., Lecouvreur, L., Boidard, O., Méry, G., Silvestre, J., Le Roux, G., Baqué, D., Elger, A., Barron, A.B., Lihoreau, M., Devaud, J.-M., Honey bees cannot sense harmful concentrations of metal pollutants in food. Chemosphere, 297, 2022, 134089, 10.1016/j.chemosphere.2022.134089.
Monchanin, C., Burden, C., Barron, A.B., Smith, B.H., Heavy metal pollutants: the hidden pervasive threat to honey bees and other pollinators. Environmental Threats to Pollinator Health and Fitness, 1st ed, 2023, Elsevier Ltd., 1–34, 10.1016/bs.aiip.2023.01.005.
Moroń, D., Szentgyörgyi, H., Grześ, I., Wantuch, M., Rożej, E., Settele, J., Potts, S.G., Laskowski, R., Woyciechowski, M., The effect of heavy metal pollution on the development of wild bees. Atlas of Biodiversity Risks - from Europe to the Globe, from Stories to Maps, 2010, Pensoft, 224–225.
Moroń, D., Grześ, I.M., Skórka, P., Szentgyörgyi, H., Laskowski, R., Potts, S.G., Woyciechowski, M., Abundance and diversity of wild bees along gradients of heavy metal pollution. J. Appl. Ecol. 49:1 (2012), 118–125, 10.1111/j.1365-2664.2011.02079.x.
Moroń, D., Szentgyörgyi, H., Skórka, P., Potts, S.G., Woyciechowski, M., Survival, reproduction and population growth of the bee pollinator, Osmia rufa (hymenoptera: Megachilidae), along gradients of heavy metal pollution. Insect Conserv. Divers. 7:2 (2014), 113–121, 10.1111/icad.12040.
Motta, E.V.S., Moran, N.A., The effects of glyphosate, pure or in herbicide formulation, on bumble bees and their gut microbial communities. Sci. Total Environ., 872(October 2022), 2023, 162102, 10.1016/j.scitotenv.2023.162102.
Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V.M., Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8:3 (2010), 199–216, 10.1007/s10311-010-0297-8.
Negri, I., Mavris, C., Di Prisco, G., Caprio, E., Pellecchia, M., Honey bees (Apis mellifera, L.) as active samplers of airborne particulate matter. PLoS One, 10(7), 2015, e0132491, 10.1371/journal.pone.0132491.
Nicholls, E., Hempel de Ibarra, N., Assessment of pollen rewards by foraging bees. Funct. Ecol. 31:1 (2017), 76–87, 10.1111/1365-2435.12778.
Nikolić, T.V., Purać, J., Orčić, S., Kojić, D., Environmental effects on superoxide dismutase and catalase activity and expression in honey bee. Arch. Insect Biochem. Physiol. 90:4 (2015), 181–194, 10.1002/arch.21253.
Nikolić, T.V., Kojić, D., Orčić, S., Batinić, D., Vukašinović, E., Blagojević, D.P., Purać, J., The impact of sublethal concentrations of Cu, Pb and Cd on honey bee redox status, superoxide dismutase and catalase in laboratory conditions. Chemosphere 164 (2016), 98–105, 10.1016/j.chemosphere.2016.08.077.
Nikolić, T.V., Kojić, D., Orčić, S., Vukašinović, E.L., Blagojević, D.P., Purać, J., Laboratory bioassays on the response of honey bee (Apis mellifera L.) glutathione S-transferase and acetylcholinesterase to the oral exposure to copper, cadmium, and lead. Environ. Sci. Pollut. Res. 26:7 (2019), 6890–6897, 10.1007/s11356-018-3950-6.
Nisbet, C., Güler, A., Ormanci, N., Cenesiz, S., Preventive action of zinc against heavy metals toxicity in honeybee. Afr. J. Biochem. Res. 12:1 (2018), 1–6, 10.5897/AJBR2016.0921.
Nogueira, F.L. de A., Bálsamo, P.J., Costa, M.J., Abdalla, F.C., Exposure to mercury at trace concentrations leads to collapse of the hepato-nephrocitic system in two neotropical species of bumblebee. Am. J. Agric. Biol. Sci. 14 (2019), 1–10, 10.3844/ajabssp.2019.1.10.
Nriagu, J.O., Pacyna, J.M., Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 333:6169 (1988), 134–139, 10.1038/333134a0.
OECD, Test No. 213: Honeybees, Acute Oral Toxicity Test. OECD Guidelines for the Testing of Chemicals, Section 2. 1998, OECD Publishing, Paris, 10.1787/9789264070165-en.
Osterman, J., Aizen, M.A., Biesmeijer, J.C., Bosch, J., Howlett, B.G., Inouye, D.W., Jung, C., Martins, D.J., Medel, R., Pauw, A., Seymour, C.L., Paxton, R.J., Global trends in the number and diversity of managed pollinator species. Agric. Ecosyst. Environ., 322, 2021, 107653, 10.1016/j.agee.2021.107653.
Özkan, Y., Irende, İ., Akdeniz, G., Kabakçi, D., Sökmen, M., Evaluation of the comparative acute toxic effects of TiO2, Ag-TiO2 and ZnO-TiO2 composite nanoparticles on honey bee (Apis mellifera). J. Int. Environ. Appl. Sci. 10:1 (2014), 26–36.
Paris, L., Peghaire, E., Moné, A., Diogon, M., Debroas, D., Delbac, F., El Alaoui, H., Honeybee gut microbiota dysbiosis in pesticide/parasite co-exposures is mainly induced by Nosema ceranae. J. Invertebr. Pathol., 172, 2020, 107348, 10.1016/j.jip.2020.107348.
Perugini, M., Manera, M., Grotta, L., Abete, M.C., Tarasco, R., Amorena, M., Heavy metal (Hg, Cr, Cd, and Pb) contamination in urban areas and wildlife reserves: honeybees as bioindicators. Biol. Trace Elem. Res. 140:2 (2011), 170–176, 10.1007/s12011-010-8688-z.
Phillips, B.B., Bullock, J.M., Gaston, K.J., Hudson-Edwards, K.A., Bamford, M., Cruse, D., Dicks, L.V., Falagan, C., Wallace, C., Osborne, J.L., Impacts of multiple pollutants on pollinator activity in road verges. J. Appl. Ecol. 58:5 (2021), 1017–1029, 10.1111/1365-2664.13844.
Pietrelli, L., Menegoni, P., Papetti, P., Bioaccumulation of heavy metals by herbaceous species grown in urban and rural sites. Water Air Soil Pollut., 233(4), 2022, 141, 10.1007/s11270-022-05577-x.
Pitts-Singer, T.L., Barbour, J.D., Effects of residual novaluron on reproduction in alfalfa leafcutting bees, Megachile rotundata F. (Megachilidae). Pest Manag. Sci. 73:1 (2017), 153–159, 10.1002/ps.4356.
Polykretis, P., Delfino, G., Petrocelli, I., Cervo, R., Tanteri, G., Montori, G., Perito, B., Branca, J.J.V., Morucci, G., Gulisano, M., Evidence of immunocompetence reduction induced by cadmium exposure in honey bees (Apis mellifera). Environ. Pollut. 218 (2016), 826–834, 10.1016/j.envpol.2016.08.006.
Poquet, Y., Bodin, L., Tchamitchian, M., Fusellier, M., Giroud, B., Lafay, F., Buleté, A., Tchamitchian, S., Cousin, M., Pélissier, M., Brunet, J.-L., Belzunces, L.P., A pragmatic approach to assess the exposure of the honey bee (Apis mellifera) when subjected to pesticide spray. PLoS One, 9(11), 2014, e113728, 10.1371/journal.pone.0113728.
Pourret, O., On the necessity of banning the term “heavy metal” from the scientific literature. Sustainability, 10(8), 2018, 2879, 10.3390/su10082879.
Pourret, O., Bollinger, J.-C., “Heavy metal” - what to do now: to use or not to use?. Sci. Total Environ. 610–611 (2018), 419–420, 10.1016/j.scitotenv.2017.08.043.
Pourret, O., Bollinger, J.-C., Hursthouse, A., Heavy metal: a misused term?. Acta Geochim. 40:3 (2021), 466–471, 10.1007/s11631-021-00468-0.
Powney, G.D., Carvell, C., Edwards, M., Morris, R.K.A., Roy, H.E., Woodcock, B.A., Isaac, N.J.B., Widespread losses of pollinating insects in Britain. Nat. Commun. 10:1 (2019), 1–6, 10.1038/s41467-019-08974-9.
Purać, J., Nikolić, T.V., Kojić, D., Ćelić, A.S., Plavša, J.J., Blagojević, D.P., Petri, E.T., Identification of a metallothionein gene in honey bee Apis mellifera and its expression profile in response to Cd, Cu and Pb exposure. Mol. Ecol. 28:4 (2019), 731–745, 10.1111/mec.14984.
Rader, R., Cunningham, S.A., Howlett, B.G., Inouye, D.W., Non-bee insects as visitors and pollinators of crops: biology, ecology, and management. Annu. Rev. Entomol. 65 (2020), 391–407, 10.1146/annurev-ento-011019-025055.
Raes, H., Cornelis, R., Rzeznik, U., Distribution, accumulation and depuration of administered lead in adult honeybees. Sci. Total Environ. 113:3 (1992), 269–279, 10.1016/0048-9697(92)90005-D.
Robinson, A., Hesketh, H., Lahive, E., Horton, A.A., Svendsen, C., Rortais, A., Dorne, J. Lou, Baas, J., Heard, M.S., Spurgeon, D.J., Comparing bee species responses to chemical mixtures: common response patterns?. PLoS One, 12(6), 2017, e0176289, 10.1371/journal.pone.0176289.
Rodrigues, C.G., Krüger, A.P., Barbosa, W.F., Guedes, R.N.C., Leaf fertilizers affect survival and behavior of the neotropical stingless bee Friesella schrottkyi (Meliponini: Apidae: hymenoptera). J. Econ. Entomol. 109:3 (2016), 1001–1008, 10.1093/jee/tow044.
Rosales, C., Cellular and molecular mechanisms of insect immunity. Insect Physiology and Ecology, Vol. 10, Issue 3, 2017, InTech, 182–190, 10.5772/67107.
Rothman, J.A., Leger, L., Kirkwood, J.S., McFrederick, Q.S., Cadmium and selenate exposure affects the honey bee microbiome and metabolome, and bee-associated bacteria show potential for bioaccumulation. Appl. Environ. Microbiol. 85:21 (2019), 1–18, 10.1128/AEM.01411-19.
Rothman, J.A., Russell, K.A., Leger, L., McFrederick, Q.S., Graystock, P., The direct and indirect effects of environmental toxicants on the health of bumblebees and their microbiomes. Proc. R. Soc. B Biol. Sci., 287, 2020, 20200980, 10.1098/rspb.2020.0980rspb20200980.
Salt, D.E., Smith, R.D., Raskin, I., Phytoremediation: a review. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 (1998), 643–668 http://www.annualreviews.org/doi/abs/10.1146/annurev.arplant.49.1.643.
Salvaggio, A., Pecoraro, R., Scalisi, E.M., Tibullo, D., Lombardo, B.M., Messina, G., Loreto, F., Copat, C., Ferrante, M., Avola, R., D'amante, G., Genovese, C., Raccuia, S.A., Brundo, M.V., Morphostructural and immunohistochemical study on the role of metallothionein in the detoxification of heavy metals in Apis mellifera L., 1758. Microsc. Res. Tech. 80:11 (2017), 1215–1220, 10.1002/jemt.22919.
Sampson, H., Ketley, J., Mallon, E., Morrissey, J., Impact of air pollution on buff-tailed bumblebees (Bombus terrestris) and their gut microbiome. Access. Microbiology, 2(7A), 2020, 10.1099/acmi.ac2020.po0626.
Sánchez-Bayo, F., Wyckhuys, K.A.G., Worldwide decline of the entomofauna: a review of its drivers. Biol. Conserv. 232 (2019), 8–27, 10.1016/j.biocon.2019.01.020.
Scott, S.B., Sivakoff, F.S., Gardiner, M.M., Exposure to urban heavy metal contamination diminishes bumble bee colony growth. Urban Ecosyst. 25:3 (2022), 989–997, 10.1007/s11252-022-01206-x.
Scott, S.B., Sivakoff, F.S., Meuti, M.E., Gardiner, M.M., Metals could challenge pollinator conservation in legacy cities. J. Insect Conserv., 1–15, 2023, 10.1007/s10841-023-00474-y.
Sgolastra, F., Blasioli, S., Renzi, T., Tosi, S., Medrzycki, P., Molowny-Horas, R., Porrini, C., Braschi, I., Lethal effects of Cr(III) alone and in combination with propiconazole and clothianidin in honey bees. Chemosphere 191 (2017), 365–372, 10.1016/j.chemosphere.2017.10.068.
Sharma, A., Pant, K., Brar, D.S., Thakur, A., Nanda, V., A review on Api-products: current scenario of potential contaminants and their food safety concerns. Food Control, 145, 2023, 109499, 10.1016/j.foodcont.2022.109499.
Silberberg, M., Amateis, P., Chemistry: The Molecular Nature of Matter and Change (Ninth Edit). 2021, McGraw Hill.
Singh, N., Gupta, V.K., Kumar, A., Sharma, B., Synergistic effects of heavy metals and pesticides in living systems. Front. Chem. 5 (2017), 1–9, 10.3389/fchem.2017.00070.
Singh, S., Diksha, Mahajan, E., Sohal, S.K., Effect of heavy metals on insects. Appraisal of Metal(Loids) in the Ecosystem, 2022, Elsevier, 361–390, 10.1016/B978-0-323-85621-8.00014-5.
Sivakoff, F.S., Gardiner, M.M., Soil lead contamination decreases bee visit duration at sunflowers. Urban Ecosyst. 20:6 (2017), 1221–1228, 10.1007/s11252-017-0674-1.
Sivakoff, F.S., Prajzner, S.P., Gardiner, M.M., Urban heavy metal contamination limits bumblebee colony growth. J. Appl. Ecol. 57:8 (2020), 1561–1569, 10.1111/1365-2664.13651.
Smith, L.A., Means, J.L., Chen, A., Remedial Options for Metals-Contaminated Sites. 1995, Lewis Publishers.
Søvik, E., Perry, C.J., LaMora, A., Barron, A.B., Ben-Shahar, Y., Negative impact of manganese on honeybee foraging. Biol. Lett., 11(3), 2015, 20140989, 10.1098/rsbl.2014.0989.
Stefanatou, A., Dimitrakopoulos, P.G., Aloupi, M., Adamidis, G.C., Nakas, G., Petanidou, T., From bioaccumulation to biodecumulation: nickel movement from Odontarrhena lesbiaca (Brassicaceae) individuals into consumers. Sci. Total Environ., 747, 2020, 141197, 10.1016/j.scitotenv.2020.141197.
Straub, L., Williams, G.R., Pettis, J., Fries, I., Neumann, P., Superorganism resilience: Eusociality and susceptibility of ecosystem service providing insects to stressors. Curr. Opin. Insect. Sci. 12 (2015), 109–112, 10.1016/j.cois.2015.10.010.
Straw, E.A., Thompson, L.J., Leadbeater, E., Brown, M.J.F., ‘Inert’ ingredients are understudied, potentially dangerous to bees and deserve more research attention. Proc. R. Soc. B Biol. Sci. 289:1970 (2022), 35–60, 10.1098/rspb.2021.2353.
Suman, J., Uhlik, O., Viktorova, J., Macek, T., Phytoextraction of heavy metals: a promising tool for clean-up of polluted environment?. Front. Plant Sci., 9, 2018, 10.3389/fpls.2018.01476.
Szentgyörgyi, H., Blinov, A., Eremeeva, N., Luzyanin, S., Grześ, I.M., Woyciechowski, M., Bumblebees (Bombidae) along pollution gradient - heavy metal accumulation, species diversity, and Nosema bombi infection level. Pol. J. Ecol. 59:3 (2011), 599–610.
Szentgyörgyi, H., Moroń, D., Nawrocka, A., Tofilski, A., Woyciechowski, M., Forewing structure of the solitary bee Osmia bicornis developing on heavy metal pollution gradient. Ecotoxicology 26:8 (2017), 1031–1040, 10.1007/s10646-017-1831-2.
Tchounwou, P.B., Yedjou, C.G., Patlolla, A.K., Sutton, D.J., Heavy metal toxicity and the environment. Molecular, Clinical and Environmental Toxicology, Vol. 101, 2012, 10.1007/978-3-7643-8340-4.
Thompson, H., Extrapolation of acute toxicity across bee species. Integr. Environ. Assess. Manag. 12:4 (2016), 622–626, 10.1002/ieam.1737.
Vamerali, T., Bandiera, M., Mosca, G., Field crops for phytoremediation of metal-contaminated land. A review. Environ. Chem. Lett. 8:1 (2010), 1–17, 10.1007/s10311-009-0268-0.
Van Aken, B., Transgenic plants for phytoremediation: helping nature to clean up environmental pollution. Trends Biotechnol. 26:5 (2008), 225–227, 10.1016/j.tibtech.2008.02.001.
Vanderplanck, M., Gilles, H., Nonclercq, D., Duez, P., Gerbaux, P., Asteraceae paradox: chemical and mechanical protection of Taraxacum pollen. Insects, 11(5), 2020, 304, 10.3390/insects11050304.
Wagner, D.L., Grames, E.M., Forister, M.L., Berenbaum, M.R., Stopak, D., Insect decline in the Anthropocene: death by a thousand cuts. PNAS 118:2 (2021), 1–10, 10.1073/pnas.2023989118.
Wang, K., Li, J., Zhao, L., Mu, X., Wang, C., Wang, M., Xue, X., Qi, S., Wu, L., Gut microbiota protects honey bees (Apis mellifera L.) against polystyrene microplastics exposure risks. J. Hazard. Mater., 402(August 2020), 2021, 123828, 10.1016/j.jhazmat.2020.123828.
Willcox, B. K., Potts, S. G., Brown, M. J. F., Alix, A., Al Naggar, Y., Chauzat, M.-P., Costa, C., Gekière, A., Hartfield, C., Hatjina, F., Knapp, J. L., Martínez-López, V., Maus, C., Metodiev, T., Nazzi, F., Osterman, J., Raimets, R., Rortais, A., Strobl, V., Van Oystaeyen, A., Wintermantel, D., Yovcheva, N., Senapathi, D. Emerging threats and opportunities to managed bee species in European agricultural systems - A Horizon Scan. Submitted in People and Nature.
Wood, T.J., Michez, D., Paxton, R.J., Drossart, M., Neumann, P., Gérard, M., Vanderplanck, M., Barraud, A., Martinet, B., Leclercq, N., Vereecken, N.J., Managed honey bees as a radar for wild bee decline?. Apidologie 51:6 (2020), 1100–1116, 10.1007/s13592-020-00788-9.
Wu, Y., Zheng, Y., Chen, Y., Wang, S., Chen, Y., Hu, F., Zheng, H., Honey bee (Apis mellifera) gut microbiota promotes host endogenous detoxification capability via regulation of P450 gene expression in the digestive tract. Microb. Biotechnol. 13:4 (2020), 1201–1212, 10.1111/1751-7915.13579.
Wuana, R.A., Okieimen, F.E., Heavy metals in contaminated soils: A review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol. 2011 (2011), 1–20, 10.5402/2011/402647.
Xu, M.-Y., Wang, P., Sun, Y.-J., Wu, Y.-J., Metabolomic analysis for combined hepatotoxicity of chlorpyrifos and cadmium in rats. Toxicology 384 (2017), 50–58, 10.1016/j.tox.2017.04.008.
Xun, E., Zhang, Y., Zhao, J., Guo, J., Translocation of heavy metals from soils into floral organs and rewards of Cucurbita pepo: implications for plant reproductive fitness. Ecotoxicol. Environ. Saf. 145 (2017), 235–243, 10.1016/j.ecoenv.2017.07.045.
Xun, E., Zhang, Y., Zhao, J., Guo, J., Heavy metals in nectar modify behaviors of pollinators and nectar robbers: consequences for plant fitness. Environ. Pollut. 242 (2018), 1166–1175, 10.1016/j.envpol.2018.07.128.
Yu, X., Sun, R., Yan, H., Guo, X., Xu, B., Characterization of a sigma class glutathione S-transferase gene in the larvae of the honeybee (Apis cerana cerana) on exposure to mercury. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 161:4 (2012), 356–364, 10.1016/j.cbpb.2011.12.009.
Zattara, E.E., Aizen, M.A., Worldwide occurrence records suggest a global decline in bee species richness. One Earth 4:1 (2021), 114–123, 10.1016/j.oneear.2020.12.005.
Zhang, W., Chen, W., Li, Z., Ma, L., Yu, J., Wang, H., Liu, Z., Xu, B., Identification and characterization of three new cytochrome P450 genes and the use of RNA interference to evaluate their roles in antioxidant defense in Apis cerana cerana Fabricius. Front. Physiol. 9 (2018), 1–16, 10.3389/fphys.2018.01608.
