The impact of landscape structure on pesticide exposure to honey bees.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
22 Oct 2024
22 Oct 2024
Historique:
received:
30
11
2023
accepted:
05
09
2024
medline:
23
10
2024
pubmed:
23
10
2024
entrez:
22
10
2024
Statut:
epublish
Résumé
Pesticides may have serious negative impacts on bee populations. The pesticide exposure of bees could depend on the surrounding landscapes in which they forage. In this study, we assess pesticide exposure across various land-use categories, while targeting the Japanese honey bee, Apis cerana japonica, a native subspecies of the eastern honey bee. In a project involving public participation, we measured the concentrations of major pesticides in honey and beeswax collected from 175 Japanese honey bee colonies across Japan and quantitatively analyzed the relationships between pesticide presence/absence or pesticide concentration and land-use categories around the colonies. Our findings revealed that the surrounding environment in which bees live strongly influences pesticide residues in beehive materials, whether the pesticides are systemic or not, with a clear trend for each land-use category. Agricultural lands, particularly paddy fields and orchards, and urban areas resulted in higher pesticide exposure, whereas forests presented a lower risk of exposure. To effectively control pesticide exposure levels in bees, it is essential to understand pesticide usage patterns and to develop appropriate regulatory systems in non-agricultural lands, similar to those in agricultural lands.
Identifiants
pubmed: 39438449
doi: 10.1038/s41467-024-52421-3
pii: 10.1038/s41467-024-52421-3
doi:
Substances chimiques
Pesticides
0
beeswax
2ZA36H0S2V
Waxes
0
Pesticide Residues
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8999Subventions
Organisme : MEXT | Japan Society for the Promotion of Science (JSPS)
ID : JP20H00425
Informations de copyright
© 2024. The Author(s).
Références
Potts, S. G. et al. Safeguarding pollinators and their values to human well-being. Nature 540, 220–229 (2016).
pubmed: 27894123
doi: 10.1038/nature20588
Friedman, J. & Barrett, S. C. Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Ann. Bot. 103, 1515–1527 (2009).
pubmed: 19218583
pmcid: 2701749
doi: 10.1093/aob/mcp035
Ollerton, J., Winfree, R. & Tarrant, S. How many flowering plants are pollinated by animals? Oikos 120, 321–326 (2011).
doi: 10.1111/j.1600-0706.2010.18644.x
Klein, A. M. et al. Importance of pollinators in changing landscapes for world crops. Proc. Biol. Sci. 274, 303–313 (2007).
pubmed: 17164193
Rollin, O. et al. Differences of floral resource use between honey bees and wild bees in an intensive farming system. Agriculture Ecosyst. Environ. 179, 78–86 (2013).
doi: 10.1016/j.agee.2013.07.007
Potts, S. G. et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353 (2010).
pubmed: 20188434
doi: 10.1016/j.tree.2010.01.007
Biesmeijer, J. C. et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354 (2006).
pubmed: 16857940
doi: 10.1126/science.1127863
Woodcock, B. A. et al. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356, 1393–1395 (2017).
pubmed: 28663502
doi: 10.1126/science.aaa1190
Woodcock, B. A. et al. Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nat. Commun. 7, 12459 (2016).
pubmed: 27529661
pmcid: 4990702
doi: 10.1038/ncomms12459
Sánchez-Bayo, F. & Wyckhuys, K. A. G. Worldwide decline of the entomofauna: a review of its drivers. Biol. Conserv. 232, 8–27 (2019).
doi: 10.1016/j.biocon.2019.01.020
El Hassani, A. K., Dacher, M., Gauthier, M. & Armengaud, C. Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera). Pharmacol. Biochem. Behav. 82, 30–39 (2005).
pubmed: 16102801
doi: 10.1016/j.pbb.2005.07.008
Thompson, H. M. Behavioural effects of pesticides in bees - Their potential for use in risk assessment. Ecotoxicology 12, 317–330 (2003).
pubmed: 12739878
doi: 10.1023/A:1022575315413
Wu, T. et al. Chlorothalonil alters the gut microbiota and reduces the survival of immature honey bees reared in vitro. Pest Manag Sci. 78, 1976–1981 (2022).
pubmed: 35088523
doi: 10.1002/ps.6816
Lu, C., Hung, Y.-T. & Cheng, Q. A review of sub-lethal neonicotinoid insecticides exposure and effects on pollinators. Curr. Pollut. Rep. 6, 137–151 (2020).
doi: 10.1007/s40726-020-00142-8
Blacquière, T., Smagghe, G., van Gestel, C. A. M. & Mommaerts, V. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21, 973–992 (2012).
pubmed: 22350105
pmcid: 3338325
doi: 10.1007/s10646-012-0863-x
Chauzat, M. P. et al. A survey of pesticide residues in pollen loads collected by honey bees in France. J. Econ. Entomol. 99, 253–262 (2006).
pubmed: 16686121
doi: 10.1093/jee/99.2.253
Chauzat, M. P. & Faucon, J. P. Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in France. Pest Manag Sci. 63, 1100–1106 (2007).
pubmed: 17879980
doi: 10.1002/ps.1451
Bernal, J. et al. Overview of pesticide residues in stored pollen and their potential effect on bee colony (Apis mellifera) losses in Spain. J. Econ. Entomol. 103, 1964–1971 (2010).
pubmed: 21309214
doi: 10.1603/EC10235
Mullin, C. A. et al. High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5, e9754 (2010).
pubmed: 20333298
pmcid: 2841636
doi: 10.1371/journal.pone.0009754
Xiao, J. et al. Analysis of honey bee exposure to multiple pesticide residues in the hive environment. Sci. Total Environ. 805, 150292 (2022).
pubmed: 34536857
doi: 10.1016/j.scitotenv.2021.150292
Beekman, M. & Ratnieks, F. L. W. Long-range foraging by the honey-bee, Apis mellifera L. Funct. Ecol. 14, 490–496 (2000).
doi: 10.1046/j.1365-2435.2000.00443.x
Wood, T. J., Kaplan, I., Zhang, Y. & Szendrei, Z. Honeybee dietary neonicotinoid exposure is associated with pollen collection from agricultural weeds. Proc. Biol. Sci. 286, 20190989 (2019).
pubmed: 31213190
pmcid: 6599974
Tsvetkov, N. et al. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science 356, 1395–1397 (2017).
pubmed: 28663503
doi: 10.1126/science.aam7470
Bednarska, A. J. et al. Effects of agricultural landscape structure, insecticide residues, and pollen diversity on the life-history traits of the red mason bee Osmia bicornis. Sci. Total Environ. 809, 151142 (2022).
pubmed: 34688758
doi: 10.1016/j.scitotenv.2021.151142
Nicholson, C. C. et al. Pesticide use negatively affects bumble bees across European landscapes. Nature 628, 355–358 (2024).
pubmed: 38030722
doi: 10.1038/s41586-023-06773-3
Kavanagh, S., Henry, M., Stout, J. C. & White, B. Neonicotinoid residues in honey from urban and rural environments. Environ. Sci. Pollut. Res. Int. 28, 28179–28190 (2021).
pubmed: 33528772
doi: 10.1007/s11356-021-12564-y
Thompson, D. G. Ecological impacts of major forest-use pesticides. In: Ecological Impacts of Toxic Chemicals (eds Sánchez-Bayo F., Brink P. J., van den Mann R. M.). Bentham Science Publishers Ltd. (2012).
Wang, L. et al. Current and future control of the wood-boring pest Anoplophora glabripennis. Insect Sci. 30, 1534–1551 (2023).
pubmed: 36944595
doi: 10.1111/1744-7917.13187
Eatough Jones, M. et al. Evaluations of insecticides and fungicides for reducing attack rates of a new invasive ambrosia beetle (Euwallacea sp., Coleoptera: Curculionidae: Scolytinae.) in infested landscape trees in California. J. Econ. Entomol. 110, 1611–1618 (2017).
European Food Safety Authority. Guidance on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J. 11, 3295 (2013).
doi: 10.2903/j.efsa.2013.3295
Thompson, T. S., van den Heever, J. P. & Limanowka, R. E. Determination of glyphosate, AMPA, and glufosinate in honey by online solid-phase extraction-liquid chromatography-tandem mass spectrometry. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 36, 434–446 (2019).
pubmed: 30806173
doi: 10.1080/19440049.2019.1577993
Suzuki, T., Ikegami, M., Goka, K. & Sakamoto, Y. Insecticide residues associated with apple orchard treatments in the mason bee, Osmia cornifrons, and their nests. Environ. Toxicol. Chem. 42, 1564–1574 (2023).
pubmed: 37083249
doi: 10.1002/etc.5635
Botías, C. et al. Neonicotinoid residues in wildflowers, a potential route of chronic exposure for bees. Environ. Sci. Technol. 49, 12731–12740 (2015).
pubmed: 26439915
doi: 10.1021/acs.est.5b03459
Stewart, S. D. et al. Potential exposure of pollinators to neonicotinoid insecticides from the use of insecticide seed treatments in the mid-southern United States. Environ. Sci. Technol. 48, 9762–9769 (2014).
pubmed: 25010122
doi: 10.1021/es501657w
Favaro, R. et al. Botanical origin of pesticide residues in pollen loads collected by honeybees during and after apple bloom. Front. Physiol. 10, 1069 (2019).
pubmed: 31620006
pmcid: 6759928
doi: 10.3389/fphys.2019.01069
Stopes, C., Measures, M., Smith, C. & Foster, L. Hedgerow management in organic farming. In: Biodiversity and Land Use, The Role of Organic Farming Multitext, Barcelona, Spain (eds Isart J., Llerena J. J.) (1995).
Tscharntke, T., Steffan-Dewenter, I., Kruess, A. & Thies, C. Contribution of small habitat fragments to conservation of insect communities of grassland–cropland landscapes. Ecol. Appl. 12, 354–363 (2002).
Smodis Skerl, M. I., Velikonja Bolta, S., Basa Cesnik, H. & Gregorc, A. Residues of pesticides in honeybee (Apis mellifera carnica) bee bread and in pollen loads from treated apple orchards. Bull. Environ. Contam. Toxicol. 83, 374–377 (2009).
pubmed: 19434347
doi: 10.1007/s00128-009-9762-0
David, A. et al. Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ. Int. 88, 169–178 (2016).
pubmed: 26760714
doi: 10.1016/j.envint.2015.12.011
Okada, E., Allinson, M., Barral, M. P., Clarke, B. & Allinson, G. Glyphosate and aminomethylphosphonic acid (AMPA) are commonly found in urban streams and wetlands of Melbourne, Australia. Water Res. 168, 115139 (2020).
pubmed: 31605832
doi: 10.1016/j.watres.2019.115139
Lentola, A. et al. Ornamental plants on sale to the public are a significant source of pesticide residues with implications for the health of pollinating insects. Environ. Pollut. 228, 297–304 (2017).
pubmed: 28551560
doi: 10.1016/j.envpol.2017.03.084
Taki, H., Yamaura, Y., Okabe, K. & Maeto, K. Plantation vs. natural forest: Matrix quality determines pollinator abundance in crop fields. Sci. Rep. 1, 132 (2011).
pubmed: 22355649
pmcid: 3216613
doi: 10.1038/srep00132
Taki, H. et al. Succession influences wild bees in a temperate forest landscape: the value of early successional stages in naturally regenerated and planted forests. PLoS ONE 8, e56678 (2013).
pubmed: 23457602
pmcid: 3574003
doi: 10.1371/journal.pone.0056678
Mitchell, E. A. D. et al. A worldwide survey of neonicotinoids in honey. Science 358, 109–111 (2017).
pubmed: 28983052
doi: 10.1126/science.aan3684
Nagamitsu, T. & Inoue, T. Differences in pollen sources of Apis cerana and Apis mellifera at a primary beech forest in central Japan. J. Apic. Res. 38, 71–78 (1999).
doi: 10.1080/00218839.1999.11100997
Kimura, K., Yoshiyama, M., Saito, K., Nirasawa, K. & Ishizaka, M. Examination of mass honey bee death at the entrance to hives in a paddy rice production district in Japan: the influence of insecticides sprayed on nearby rice fields. J. Apic. Res. 53, 599–606 (2015).
doi: 10.3896/IBRA.1.53.5.12
Yasuda, M., Sakamoto, Y., Goka, K., Nagamitsu, T. & Taki, H. Insecticide susceptibility in Asian honey bees (Apis cerana (Hymenoptera: Apidae)) and implications for wild honey bees in Asia. J. Econ. Entomol. 110, 447–452 (2017).
pubmed: 28334064
doi: 10.1093/jee/tox032
de Souza, A. P. F., Rodrigues, N. R. & Reyes, F. G. R. Glyphosate and aminomethylphosphonic acid (AMPA) residues in Brazilian honey. Food Addit. Contam Part B Surveill. 14, 40–47 (2021).
pubmed: 33327891
doi: 10.1080/19393210.2020.1855676
Zoller, O., Rhyn, P., Rupp, H., Zarn, J. A. & Geiser, C. Glyphosate residues in Swiss market foods: monitoring and risk evaluation. Food Addit. Contam Part B Surveill. 11, 83–91 (2018).
pubmed: 29284371
doi: 10.1080/19393210.2017.1419509
Dively, G. P., Embrey, M. S., Kamel, A., Hawthorne, D. J. & Pettis, J. S. Assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLoS One 10, e0118748 (2015).
pubmed: 25786127
pmcid: 4364903
doi: 10.1371/journal.pone.0118748
Sasaki, M., Takahashi, H. & Sato, Y. Comparison of the dance dialect and foraging range between Apis mellifera and northern most subspecies of A. cerana in Japan. Honeybee Sci. 14, 49–54 (1993). (in Japanese).