Long-term field-realistic exposure to a next-generation pesticide, flupyradifurone, impairs honey bee behaviour and survival.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
28 06 2021
28 06 2021
Historique:
received:
02
01
2021
accepted:
11
05
2021
entrez:
29
6
2021
pubmed:
30
6
2021
medline:
17
8
2021
Statut:
epublish
Résumé
The assessment of pesticide risks to insect pollinators have typically focused on short-term, lethal impacts. The environmental ramifications of many of the world's most commonly employed pesticides, such as those exhibiting systemic properties that can result in long-lasting exposure to insects, may thus be severely underestimated. Here, seven laboratories from Europe and North America performed a standardised experiment (a ring-test) to study the long-term lethal and sublethal impacts of the relatively recently approved 'bee safe' butenolide pesticide flupyradifurone (FPF, active ingredient in Sivanto
Identifiants
pubmed: 34183763
doi: 10.1038/s42003-021-02336-2
pii: 10.1038/s42003-021-02336-2
pmc: PMC8238954
doi:
Substances chimiques
Pesticides
0
Pyridines
0
flupyradifurone
8H7JT159D0
4-Butyrolactone
OL659KIY4X
Banques de données
figshare
['10.6084/m9.figshare.14269706']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
805Références
Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One 12, (2017).
IPBES. The assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on Pollinators, Pollination and Food Production (eds Potts, S.G., Imperatriz-Fonseca, V.L. & Ngo, H.T. 2017).
Goulson, D. The insect apocalypse, and why it matters. Curr. Biol. 29, R967–R971 (2019).
pubmed: 31593678
doi: 10.1016/j.cub.2019.06.069
Crall, J. D. et al. Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science 362, 683–686 (2018).
pubmed: 30409882
doi: 10.1126/science.aat1598
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
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
Limay-Rios, V. et al. Neonicotinoid insecticide residues in soil dust and associated parent soil in fields with a history of seed treatment use on crops in southwestern Ontario. Environ. Toxicol. Chem. 35, 303–310 (2016).
pubmed: 26395849
doi: 10.1002/etc.3257
Tosi, S., Costa, C., Vesco, U., Quaglia, G. & Guido, G. A 3-year survey of Italian honey bee-collected pollen reveals widespread contamination by agricultural pesticides. Sci. Total Environ. 615, 208–218 (2018).
pubmed: 28968582
doi: 10.1016/j.scitotenv.2017.09.226
Mitchell, E. A. D., Mulhauser, B., Mulot, M. & Aebi, A. A worldwide survey of neonicotinoids in honey. Science 111, 109–111 (2017).
doi: 10.1126/science.aan3684
Long, E. Y. & Krupke, C. H. Non-cultivated plants present a season-long route of pesticide exposure for honey bees. Nat. Commun. 7, 1–12 (2016).
doi: 10.1038/ncomms11629
Simon-Delso, N. et al. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ. Sci. Pollut. Res. 22, 5–34 (2014).
doi: 10.1007/s11356-014-3470-y
Sgolastra, F. et al. Bees and pesticide regulation: lessons from the neonicotinoid experience. Biol. Conserv. 241, 108356 (2020).
doi: 10.1016/j.biocon.2019.108356
Palmer, M. J. et al. Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nat. Commun. 4, 1634–1638 (2013).
pubmed: 23535655
doi: 10.1038/ncomms2648
Giorio, C. et al. An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 1: new molecules, metabolism, fate, and transport. Environ. Sci. Pollut. Res. 1–33 https://doi.org/10.1007/s11356-017-0394-3 (2017).
Jeschke, P. et al. Flupyradifurone (Sivanto
pubmed: 26047109
doi: 10.1016/j.pestbp.2014.10.011
Bayer CropScience A.G. Sivanto worldwide. Available at: https://www.sivanto.bayer.com/sivanto-worldwide.html (Accessed: 23 Mar 2018).
Nauen, R. et al. Flupyradifurone: a brief profile of a new butenolide insecticide. Pest Manag. Sci. 71, 850–862 (2014).
Prosser, R. S. et al. Sensitivity of the early-life stages of freshwater mollusks to neonicotinoid and butenolide insecticides. Environ. Pollut. https://doi.org/10.1016/j.envpol.2016.07.022 (2016).
Bayer CropScience A.G. Flupyradifurone Technical Information (Bayer CropScience A.G., 2013).
O’Mullane, M., Liying, Z. & Boobis, A. Flupyradifurone, Pesticide residues in food—2015: toxicological evaluations. In Joint Meeting of the FAO Panel of Experts on Pesticide Residues in Food and the Environment and the WHO Core Assessment Group on Pesticide Residues, Geneva, 15–24 September 2015 (2016).
Ford, K. A. & Casida, J. E. Chloropyridinyl neonicotinoid insecticides: Diverse molecular substituents contribute to facile metabolism in mice. Chem. Res. Toxicol. 19, 944–951 (2006).
pubmed: 16841963
doi: 10.1021/tx0600696
Suchail, S., Guez, D. & Belzunces, L. P. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ. Toxicol. Chem. 20, 2482–2486 (2001).
pubmed: 11699773
doi: 10.1002/etc.5620201113
US EPA. Environmental Fate and Ecological Risk Assessment for Foliar, Soil Drench, and Seed Treatment Uses Of The New Insecticide Flupyradifurone (BYI 02960) (2014).
Tosi, S. & Nieh, J. C. Lethal and sublethal synergistic effects of a new systemic pesticide, flupyradifurone (Sivanto®) on honey bees. Proc. R. Soc. B Biol. Sci. 286, 20190433 (2019).
doi: 10.1098/rspb.2019.0433
Tong, L., James, C. N. & Tosi, S. Combined nutritional stress and a new systemic pesticide (flupyradifurone, Sivanto®) reduce bee survival, food consumption, flight success, and thermoregulation. Chemosphere 237, 124408 (2019).
pubmed: 31356997
doi: 10.1016/j.chemosphere.2019.124408
Tan, K. et al. A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Sci. Rep. 5, 2–10 (2015).
Hesselbach, H. & Scheiner, R. Supplementary information of Effects of the novel pesticide flupyradifurone (Sivanto) on honeybee taste and cognition. Sci. Rep. 8, 4954 (2018).
pubmed: 29563522
pmcid: 5862975
doi: 10.1038/s41598-018-23200-0
Hesselbach, H. & Scheiner, R. The novel pesticide flupyradifurone (Sivanto) affects honeybee motor abilities. Ecotoxicology 1–6 https://doi.org/10.1007/s10646-019-02028-y (2019).
Hesselbach, H., Seeger, J., Schilcher, F., Ankenbrand, M. & Scheiner, R. Chronic exposure to the pesticide flupyradifurone can lead to premature onset of foraging in honeybees Apis mellifera. J. Appl. Ecol. 609–618 https://doi.org/10.1111/1365-2664.13555 (2019).
Chakrabarti, P., Carlson, E. A., Lucas, H. M., Melathopoulos, A. P. & Sagili, R. R. Field rates of Sivanto
pubmed: 32437365
pmcid: 7241780
doi: 10.1371/journal.pone.0233033
Al Naggar, Y. & Baer, B. Consequences of a short time exposure to a sublethal dose of Flupyradifurone (Sivanto) pesticide early in life on survival and immunity in the honeybee (Apis mellifera). Sci. Rep. 9, 1–11 (2019).
doi: 10.1038/s41598-019-56224-1
Campbell, J. W., Cabrera, A. R., Stanley-Stahr, C. & Ellis, J. D. An evaluation of the honey bee (Hymenoptera: Apidae) safety profile of a new systemic insecticide, flupyradifurone, under field conditions in Florida. J. Econ. Entomol. 96, 875–878 (2016).
EFSA. EFSA Guidance Document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees) - version 2014. EFSA J. 11, 268 (2013).
Rortais, A. et al. Risk assessment of pesticides and other stressors in bees: principles, data gaps and perspectives from the European Food Safety Authority. Sci. Total Environ. 587–588, 524–537 (2017).
pubmed: 28279532
doi: 10.1016/j.scitotenv.2016.09.127
European Commission. COMMISSION REGULATION (EU) No 283/2013 of 1 March 2013 setting out the data requirements for active substances, in accordance with Regulation (EC) No 1107/2009 of the European Parliament and of the Council concerning the placing of plant protection produc. Official Journal of the European Union (2013).
OECD/OCDE. OECD Guideline 245 for the Testing of Chemicals. Honey bee (Apis mellifera L.), Chronic Oral Toxicity Test (10-Day Feeding). OECD/OCDE (OECD Publishing, 2017). https://doi.org/10.1787/9789264284081-en
EFSA. Conclusion on the peer review of the pesticide risk assessment of the active substance flupyradifurone. EFSA J. 13, 1–106 (2015).
Baines, D., Wilton, E., Pawluk, A., De Gorter, M. & Chomistek, N. Neonicotinoids act like endocrine disrupting chemicals in newly-emerged bees and winter bees. Sci. Rep. 7, 10979 (2017).
pubmed: 28887455
pmcid: 5591280
doi: 10.1038/s41598-017-10489-6
Simon-Delso, N., San Martin, G., Bruneau, E. & Hautier, L. Time-to-death approach to reveal chronic and cumulative toxicity of a fungicide for honeybees not revealed with the standard ten-day test. Sci. Rep. 8, 1–11 (2018).
doi: 10.1038/s41598-018-24746-9
Hesketh, H. et al. Extending standard testing period in honeybees to predict lifespan impacts of pesticides and heavy metals using dynamic energy budget modelling. Nat. Publ. Gr. 1–12 https://doi.org/10.1038/srep37655 (2016).
Sánchez‐bayo, F. & Tennekes, H. A. Time‐cumulative toxicity of neonicotinoids: experimental evidence and implications for environmental risk assessments. Int. J. Environ. Res Public Health 17, 1629 (2020).
Tennekes, H. A. & Sánchez-Bayo, F. The molecular basis of simple relationships between exposure concentration and toxic effects with time. Toxicology 309, 39–51 (2013).
pubmed: 23603429
doi: 10.1016/j.tox.2013.04.007
European Commission. Flupyradifurone Ecotoxicology 6 (European Commision, 2014).
Gladbach, D., Theis, M., Przygoda, D. & Nikolakis, A. Assessment of chronic effects of BYI02960 tech. to the honey bee, Apis mellifera L., in a 10 days continuous laboratory feeding test; Bayer CropScience AG, Monheim, Germany; Report No E318 4561-8, Document No: M-462475-01-1 (2013).
Tosi, S., Burgio, G. & Nieh, J. C. J. C. A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Sci. Rep. 7, 1201 (2017).
pubmed: 28446783
pmcid: 5430654
doi: 10.1038/s41598-017-01361-8
Tosi, S. & Nieh, J. C. A common neonicotinoid pesticide, thiamethoxam, alters honey bee activity, motor functions, and movement to light. Sci. Rep. 7, 15132 (2017).
pubmed: 29123189
pmcid: 5680225
doi: 10.1038/s41598-017-15308-6
Henry, M. et al. Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees. Proc. R. Soc. B Biol. Sci. 282, 20152110 (2015).
doi: 10.1098/rspb.2015.2110
Fischer, J. et al. Neonicotinoids interfere with specific components of navigation in honeybees. PLoS ONE 9, e91364 (2014).
pubmed: 24646521
pmcid: 3960126
doi: 10.1371/journal.pone.0091364
Rondeau, G. et al. Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci. Rep. 4, 1–8 (2014).
doi: 10.1038/srep05566
Mulvey, J. & Cresswell, J. E. Time‐dependent effects on bumble bees of dietary exposures to farmland insecticides (imidacloprid, thiamethoxam and fipronil). Pest Manag. Sci. https://doi.org/10.1002/ps.5838 (2020).
Tennekes, H. A. Time-dependent toxicity of neonicotinoids and other toxicants: implications for a new approach to risk assessment. J. Environ. Anal. Toxicol. 01, (2011).
Holder, P. J., Jones, A., Tyler, C. R. & Cresswell, J. E. Fipronil pesticide as a suspect in historical mass mortalities of honey bees. Proc. Natl Acad. Sci. U. S. A. 115, 13033–13038 (2018).
pubmed: 30509996
pmcid: 6304995
doi: 10.1073/pnas.1804934115
Manjon, C. et al. Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Curr. Biol. 28, 1137–1143.e5 (2018).
pubmed: 29576476
pmcid: 5887109
doi: 10.1016/j.cub.2018.02.045
Topping, C. J., Aldrich, A. & Berny, P. Overhaul environmental risk assessment for pesticides. Science 367, 360–363 (2020).
pubmed: 31974232
doi: 10.1126/science.aay1144
Decourtye, A., Henry, M. & Desneux, N. Overhaul pesticide testing on bees. Nature 497, 188 (2013).
pubmed: 23657341
doi: 10.1038/497188a
Spurgeon, D. et al. Chronic Oral Lethal and Sub-lethal Toxicities of Different Binary Mixtures of Pesticides and Contaminants in Bees (Apis mellifera, Osmia bicornis and Bombus terrestris) EN-1076 (EFSA Supporting Publications, 2016).
Tang, Q., Ma, K., Chi, H., Hou, Y. & Id, X. G. Transgenerational hormetic effects of sublethal dose of flupyradifurone on the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). PLoS ONE 14, e0208058 (2019).
Calabrese, E. J. Hormesis: a revolution in toxicology, risk assessment and medicine. EMBO Rep. 5, 37–40 (2004).
doi: 10.1038/sj.embor.7400222
Christopher Cutler, G. & Guedes, R. N. C. in Pesticide Dose: Effects on the Environment and Target and Non-Target Organisms (eds Duke, S. O., Kudsk, P. & Solomon, K.) (ACS Publications, 2010).
Tosi, S. et al. Effects of a neonicotinoid pesticide on thermoregulation of African honey bees (Apis mellifera scutellata). J. Insect Physiol. 93–94, 56–63 (2016).
FAO. Things to Know About the Ring Test (FAO, 2015).
Dietemann, V. et al. Standard methods for varroa research. J. Apic. Res. 52, 1–54 (2013).
Fries, I. et al. Standard methods for nosema research. J. Apic. Res. 52, 1–28 (2013).
doi: 10.3896/IBRA.1.52.1.14
OECD/OCDE. OECD Guideline 213 for the testing of chemicals on honeybee, acute oral toxicity test (1998). https://doi.org/10.1787/9789264070165-en
Pisa, L. W. et al. Effects of neonicotinoids and fipronil on non-target invertebrates. Environ. Sci. Pollut. Res. Int. 22, 68–102 (2014).
pubmed: 25223353
pmcid: 4284392
doi: 10.1007/s11356-014-3471-x
EFSA. Scientific Opinion on the science behind the development of a risk assessment of Plant Protection Products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J. 10, 1–275 (2012).
Medrzycki, P. et al. Standard methods for toxicology research in Apis mellifera. J. Apic. Res. 52, 1–60 (2013).
doi: 10.3896/IBRA.1.52.4.14
Williams, G. R. et al. Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. J. Apic. Res. 52, 1–36 (2013).
doi: 10.3896/IBRA.1.52.1.04
Cox, D. R. & Oakes, D. Analysis of Survival Data (CRC Press, 1984).
Kaplan, E. L. & Meier, P. Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 53, 457–481 (1958).
doi: 10.1080/01621459.1958.10501452
Madsen, H. & Thyregod, P. Introduction to General and Generalized LInear Models (Chapman & Hall/CRC, 2011).
Warton, D. & Hui, F. K. The arcsine is asinine: the analysis of proportions in ecology. Ecology 92, 3–10 (2011).
pubmed: 21560670
doi: 10.1890/10-0340.1
Ritz, C., Baty, F., Streibig, J. C. & Gerhard, D. Dose-response analysis using R. PLoS ONE 10, 1–13 (2015).
doi: 10.1371/journal.pone.0146021
Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Ministry of Agriculture Livestock and Supply. Proficiency Test Final Report—Determination of ochratoxin A in Green Coffee by Immunoaffinity Column Clean-up and LC/TLC. (2006).
R Core Team. R: a Language and Environment for Statistical Computing (R Core Team, 2016).
Sokal, R. R. & Rohlf, F. J. Biometry: the Principles and Practice of Statistics in Biological Research (WH Freman and Company: New York, 1995).