[en] Neonicotinoids (neonics) are the most widely used insecticides worldwide and are considered to be of low risk to non-target organisms such as vertebrates. Further, they are reported to be rapidly excreted and metabolized, reducing their potential toxicity. Nevertheless, growing evidence of adverse effects of neonics on farmland bird species raise questions about the purported harmless nature of these pesticides. We attempted to search for pesticide residues in species of different trophic levels and at different life stages, by using multiple bird monitoring programs on a Long-Term Socio-Ecological Research (LTSER) platform. Three passerine birds-the blackbird (Turdus merula), cirl bunting (Emberiza cirlus), and common nightingale (Luscinia megarhynchos)-that feed on seeds and invertebrates were monitored during their reproductive period, and the grey partridge (Perdix perdix) that feeds on seeds was monitored during its wintering period. We also monitored chicks of an apex predator-the Montagu's harrier (Circus pygargus)-that preys mostly upon common voles but also upon insects. We found that the birds' blood samples showed presence of residues of five neonics: three banned since 2018 in France-clothianidin, thiacloprid, and thiamethoxam-and two-dinotefuran and nitenpyram-used for veterinary purposes only. While none of these neonics was detected in blackbirds, all were present in grey partridges. Clothianidin was detected in all species, except blackbirds. Concentrations of the three banned neonics were similar or higher than concentrations found in birds monitored elsewhere before the ban. These findings raise questions about the persistence of neonics within the environment and the mode of exposure to wild fauna. Future investigations on the sublethal effects of these neonics on life-history traits of these farmland birds may help in providing a better understanding of the effects of exposure of bird populations to these insecticides, and also to the consequent effect on human health.
Disciplines :
Chemistry
Author, co-author :
Fuentes, Elva ✱; UMR 7372, Centre d'Études Biologiques de Chizé, La Rochelle Université & CNRS, 79360 Villiers en Bois, France
Gaffard, Agathe ✱; UMR 7372, Centre d'Études Biologiques de Chizé, La Rochelle Université & CNRS, 79360 Villiers en Bois, France
Rodrigues, Anaïs ; Université de Liège - ULiège > Molecular Systems (MolSys) ; Université de Strasbourg, CNRS-UMR 7515, ICPEES, 67087 Strasbourg cedex 2, France
Millet, Maurice; Université de Strasbourg, CNRS-UMR 7515, ICPEES, 67087 Strasbourg cedex 2, France
Bretagnolle, Vincent; UMR 7372, Centre d'Études Biologiques de Chizé, La Rochelle Université & CNRS, 79360 Villiers en Bois, France, LTSER "Zone Atelier Plaine & Val de Sèvre", CNRS, 79360 Villiers-en-Bois, France
Moreau, Jérôme; UMR CNRS 6282 Biogéosciences, Équipe Écologie Évolutive, Université de Bourgogne-Franche-Comté, 21000 Dijon, France
Monceau, Karine ; UMR 7372, Centre d'Études Biologiques de Chizé, La Rochelle Université & CNRS, 79360 Villiers en Bois, France. Electronic address: karine.monceau@univ-lr.fr
✱ These authors have contributed equally to this work.
Language :
English
Title :
Neonicotinoids: Still present in farmland birds despite their ban.
CNRS - Centre National de la Recherche Scientifique
Funding text :
This work was supported by the French National Research Agency (ANR JCJC PestiStress, grant # 19-CE34-0003-01 ), the French National Centre of Scientific Research ( CNRS ), the French National Research Institute for Agriculture, Food and the Environment ( INRAE ), and the University of La Rochelle . This study was partly funded by the BioBird project (regional government of Nouvelle-Aquitaine) , by the ACI (University of La Rochelle) , BIRDPEST project (RECOTOX 2019) , AgriBioBird project (OSU Theta ISITE-BFC) , the Contrat de Plan État-Région (CPER) Econat and the French National program EC2CO (Ecosphère Continentale et Côtière) .
Abu Zeid, E.H., Alam, R.T., Ali, S.A., Hendawi, M.Y., Dose-related impacts of imidacloprid oral intoxication on brain and liver of rock pigeon (Columba livia domestica), residues analysis in different organs. Ecotoxicol. Environ. Saf. 167 (2019), 60–68, 10.1016/j.ecoenv.2018.09.121.
Addy-Orduna, L., Cazenave, J., Mateo, R., Avoidance of neonicotinoid-treated seeds and cotyledons by captive eared doves (Zenaida auriculata, Columbidae). Environ. Pollut., 304, 2022, 119237, 10.1016/j.envpol.2022.119237.
Anastassiades, M., Lehotay, S.J., Štajnbaher, D., Schenck, F.J., Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. J. AOAC Int. 86 (2003), 412–431, 10.1093/jaoac/86.2.412.
Arnold, K.E., Herborn, K.A., Adam, A., Alexander, L., Individual variation in the oxidative costs of personality traits. Funct. Ecol. 29 (2015), 522–530, 10.1111/1365-2435.12375.
Arroyo, B., Leroux, A., Bretagnolle, V., Patterns of egg and clutch size variation in the Montagu's Harrier. J. Raptor Res. 32 (1998), 136–142.
Arroyo, B.E., García, J.T., Bretagnolle, V., Montagu's harrier. – BWP update. J. Birds Western Palearctic 6:1/2 (2004), 41–55 Oxford University Press, Oxford.
Arroyo, B.E., Bretagnolle, V., Leroux, A., Interactive effects of food and age on breeding in the Montagu's Harrier Circus pygargus. Ibis 149 (2007), 806–813, 10.1111/j.1474-919X.2007.00716.x.
Badry, A., Krone, O., Jaspers, V.L., Mateo, R., García-Fernández, A., Leivits, M., Shore, R.F., Towards harmonisation of chemical monitoring using avian apex predators: identification of key species for pan-European biomonitoring. Sci. Total Environ., 731, 2020, 139198, 10.1016/j.scitotenv.2020.139198.
Bean, T.G., Gross, M.S., Karouna-Renier, N.K., Henry, P.F., Schultz, S.L., Hladik, M.L., Kuivila, K.M., Rattner, B.A., Toxicokinetics of imidacloprid-coated wheat seeds in Japanese quail (Coturnix japonica) and an evaluation of hazard. Environ. Sci. Technol. 53 (2019), 3888–3897, 10.1021/acs.est.8b07062.
Bishop, C.A., Moran, A.J., Toshack, M.C., Elle, E., Maisonneuve, F., Elliott, J.E., Hummingbirds and bumble bees exposed to neonicotinoid and organophosphate insecticides in the Fraser Valley, British Columbia, Canada. Environ. Toxicol. Chem. 37 (2018), 2143–2152, 10.1002/etc.4174.
Bishop, C.A., Woundneh, M.B., Maisonneuve, F., Common, J., Elliott, J.E., Moran, A.J., Determination of neonicotinoids and butenolide residues in avian and insect pollinators and their ambient environment in Western Canada (2017, 2018). Sci. Total Environ., 737, 2020, 139386, 10.1016/j.scitotenv.2020.139386.
Bonneris, E., Gao, Z., Prosser, A., Barfknecht, R., Selecting appropriate focal species for assessing the risk to birds from newly drilled pesticide‐treated winter cereal fields in France. Integr. Environ. Asses. 15 (2019), 422–436, 10.1002/ieam.4112.
Bretagnolle, V., Berthet, E., Gross, N., Gauffre, B., Plumejeaud, C., Houte, S., Badenhausser, I., Monceau, K., Allier, F., Monestiez, P., Gaba, S., Towards sustainable and multifunctional agriculture in farmland landscapes: lessons from the integrative approach of a French LTSER platform. Sci. Total Environ. 627 (2018), 822–834, 10.1016/j.scitotenv.2018.01.142.
Bro, E., Devillers, J., Millot, F., Decors, A., Residues of plant protection products in grey partridge eggs in French cereal ecosystems. Environ. Sci. Pollut. R. 23 (2016), 9559–9573, 10.1007/s11356-016-6093-7.
Burns, F., Eaton, M.A., Burfield, I.J., Klvaňová, A., Šilarová, E., Staneva, A., Gregory, R.D., Abundance decline in the avifauna of the European Union reveals cross‐continental similarities in biodiversity change. Ecol. Evol. 11 (2021), 16647–16660, 10.1002/ece3.8282.
Butet, A., Leroux, A.B., Effects of agriculture development on vole dynamics and conservation of Montagu's harrier in western French wetlands. Biol. Conserv. 100 (2001), 289–295, 10.1016/S0006-3207(01)00033-7.
Byholm, P., Mäkeläinen, S., Santangeli, A., Goulson, D., First evidence of neonicotinoid residues in a long-distance migratory raptor, the European honey buzzard (Pernis apivorus). Sci. Total Environ. 639 (2018), 929–933, 10.1016/j.scitotenv.2018.05.185.
Campbell, L.H., Avery, M.I., Donald, P., Evans, A.D., Green, R.E., Wilson, J.D., A Review of the Indirect Effects of Pesticides on Birds. JNCC Report No. 227., 1997, Joint Nature Conservation Committee, Peterborough.
Casida, J.E., Neonicotinoids and other insect nicotinic receptor competitive modulators: progress and prospects. Annu. Rev. Entomol. 63 (2018), 125–144, 10.1146/annurev-ento-020117-043042.
Chiron, F., Chargé, R., Julliard, R., Jiguet, F., Muratet, A., Pesticide doses, landscape structure and their relative effects on farmland birds. Agric. Ecosyst. Environ. 185 (2014), 153–160, 10.1016/j.agee.2013.12.013.
Cimino, A.M., Boyles, A.L., Thayer, K.A., Perry, M.J., Effects of neonicotinoid pesticide exposure on human health: a systematic review. Environ. Health Perspect. 125 (2017), 155–162, 10.1289/EHP515.
Comolet-Tirman, J., Siblet, J.P., Witté, I., Cadiou, B., Czajkowski, M.A., Deceuninck, B., Jiguet, F., Landry, P., Quaintenne, G., Roché, J.E., Sarasa, M., Touroult, J., Statuts et tendances des populations d'oiseaux nicheurs de France. Bilan simplifié du premier rapportage national au titre de la Directive Oiseaux. Alauda 83 (2015), 35–76.
CVMP, V.I.C.H., Guideline on Environmental Impact Assessment (EIAs) for Veterinary Medicinal Products (VMPs) – Phase I, VICH GL 6 (CVMP/VICH/592/1998). 2000 [Online]. Available at: https://www.ema.europa.eu/en/vich-gl6-environmental-impact-assessment-eias-veterinary-medicinal-products-phase-i accessed date:. (Accessed 12 October 2022)
DEFRA. Wild Bird Populations in the UK, 1970 to 2019 – Updated for Wintering and Waterbirds. 2021, Department for Environment, Food Rural Affairs [Online]. Available at: https://www.gov.uk/government/statistics/wild-bird-populations-in-the-uk accessed date:. (Accessed 12 October 2022)
Diepens, N.J., Belgers, D., Buijse, L., Roessink, I., Pet dogs transfer veterinary medicines to the environment. Sci. Total Environ., 858, 2023, 159550, 10.1016/j.scitotenv.2022.159550.
EFSA (European Food Safety Authority). Evaluation of the emergency authorisations granted by Member State France for plant protection products containing imidacloprid or thiamethoxam. EFSA supporting publication 2021, 2021, 10.2903/sp.efsa.2021.EN-6968 EN-6968. 13pp.
Eng, M.L., Stutchbury, B.J., Morrissey, C.A., Imidacloprid and chlorpyrifos insecticides impair migratory ability in a seed-eating songbird. Sci. Rep-UK 7 (2017), 1–9, 10.1038/s41598-017-15446-x.
Ertl, H.M., Mora, M.A., Brightsmith, D.J., Navarro-Alberto, J.A., Potential impact of neonicotinoid use on Northern bobwhite (Colinus virginianus) in Texas: a historical analysis. PLoS One, 13, 2018, e0191100, 10.1371/journal.pone.0191100.
Espín, S., García-Fernández, A.J., Herzke, D., Shore, R.F., van Hattum, B., Martínez-López, E., Coeurdassier, M., Eulaers, I., Fritsch, C., Gómez-Ramírez, P., Jaspers, V.L.B., Krone, O., Duke, G., Helander, B., Mateo, R., Movalli, P., Sonne, C., van den Brink, N.W., Tracking pan-continental trends in environmental contamination using sentinel raptors—what types of samples should we use?. Ecotoxicology 25 (2016), 777–801, 10.1007/s10646-016-1636-8.
Fritsch, C., Appenzeller, B., Burkart, L., Coeurdassier, M., Scheifler, R., Raoul, F., Driget, V., Powolny, T., Gagnaison, C., Rieffel, D., Afonso, E., Goydadin, A.-C., Hardy, E.M., Palazzi, P., Schaeffer, C., Gaba, S., Bretagnolle, V., Bertrand, C., Pelosi, C., Pervasive exposure of wild small mammals to legacy and currently used pesticide mixtures in arable landscapes. Sci. Rep-UK 12 (2022), 1–22, 10.1038/s41598-022-19959-y.
Geiger, F., Bengtsson, J., Berendse, F., Weisser, W.W., Emmerson, M., Morales, M.B., Ceryngier, P., Liira, J., Tscharntke, T., Winqvist, C., Eggers, S., Bommarco, R., Pärt, T., Bretagnolle, V., Plantegenest, M., Clement, L.W., Dennis, C., Palmer, C., Oñate, J.J., Guerrero, I., Hawro, V., Aavik, T., Thies, C., Flohre, A., Hänke, S., Fischer, C., Goedhart, P.W., Inchausti, P., Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl. Ecol. 11 (2010), 97–105, 10.1016/j.baae.2009.12.001.
Gibbons, D., Morrissey, C., Mineau, P., A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ. Sci. Pollut. R. 22 (2015), 103–118, 10.1007/s11356-014-3180-5.
Graves, E.E., Jelks, K.A., Foley, J.E., Filigenzi, M.S., Poppenga, R.H., Ernest, H.B., Melnicoe, R., Tell, L.A., Analysis of insecticide exposure in California hummingbirds using liquid chromatography-mass spectrometry. Environ. Sci. Pollut. R. 26 (2019), 15458–15466, 10.1007/s11356-019-04903-x.
Grue, C.E., Gibert, P.L., Seeley, M.E., Neurophysiological and behavioral changes in non-target wildlife exposed to organophosphate and carbamate pesticides: thermoregulation, food consumption, and reproduction. Am. Zool. 37 (1997), 369–388 https://www.jstor.org/stable/3884019.
Hallmann, C.A., Foppen, R.P., Van Turnhout, C.A., De Kroon, H., Jongejans, E., Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511 (2014), 341–343, 10.1038/nature13531.
Han, W., Tian, Y., Shen, X., Human exposure to neonicotinoid insecticides and the evaluation of their potential toxicity: an overview. Chemosphere 192 (2018), 59–65, 10.1016/j.chemosphere.2017.10.149.
Hao, C., Eng, M.L., Sun, F., Morrissey, C.A., Part-per-trillion LC-MS/MS determination of neonicotinoids in small volumes of songbird plasma. Sci. Total Environ. 644 (2018), 1080–1087, 10.1016/j.scitotenv.2018.06.317.
Henry, M., Cerrutti, N., Aupinel, P., Decourtye, A., Gayrard, M., Odoux, J.F., Pissard, A., Rüger, C., Bretagnolle, V., Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees. Proc. Biol. Sci., 282, 2015, 20152110, 10.1098/rspb.2015.2110.
Hoshi, N., Hirano, T., Omotehara, T., Tokumoto, J., Umemura, Y., Mantani, Y., Tanida, T., Warita, K., Tabuchi, Y., Yokoyama, T., Kitagawa, H., Insight into the mechanism of reproductive dysfunction caused by neonicotinoid pesticides. Biol. Pharm. Bull. 37 (2014), 1439–1443, 10.1248/bpb.b14-00359.
Humann-Guilleminot, S., de Montaigu, C.T., Sire, J., Grünig, S., Gning, O., Glauser, G., Vallat, A., Helfenstein, F., A sublethal dose of the neonicotinoid insecticide acetamiprid reduces sperm density in a songbird. Environ. Res., 177, 2019, 108589, 10.1016/j.envres.2019.108589.
Humann-Guilleminot, S., Laurent, S., Bize, P., Roulin, A., Glauser, G., Helfenstein, F., Contamination by neonicotinoid insecticides in barn owls (Tyto alba) and Alpine swifts (Tachymarptis melba). Sci. Total Environ., 785, 2021, 147403, 10.1016/j.scitotenv.2021.147403.
Humann-Guilleminot, S., Andreo, L., Blatti, E., Glauser, G., Helfenstein, F., Desprat, J., Experimental evidence for clothianidin deposition in feathers of house sparrows after ingestion of sublethal doses treated seeds. Chemosphere, 315, 2022, 137724, 10.1016/j.chemosphere.2022.137724.
Ihara, M., D Buckingham, S., Matsuda, K., B Sattelle, D., Modes of action, resistance and toxicity of insecticides targeting nicotinic acetylcholine receptors. Curr. Med. Chem. 24 (2017), 2925–2934, 10.2174/0929867324666170206142019.
Klingelhöfer, D., Braun, M., Brüggmann, D., Groneberg, D.A., Neonicotinoids: a critical assessment of the global research landscape of the most extensively used insecticide. Environ. Res., 213, 2022, 113727, 10.1016/j.envres.2022.113727.
Köhler, H.R., Triebskorn, R., Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond?. Science 341 (2013), 759–765, 10.1126/science.1237591.
Lennon, R.J., Peach, W.J., Dunn, J.C., Shore, R.F., Pereira, M.G., Sleep, D., Dodd, S., Wheatley, C.J., Arnold, K.E., Brown, C.D., From seeds to plasma: confirmed exposure of multiple farmland bird species to clothianidin during sowing of winter cereals. Sci. Total Environ., 723, 2020, 138056, 10.1016/j.scitotenv.2020.138056.
Lennon, R.J., Shore, R.F., Pereira, M.G., Peach, W.J., Dunn, J.C., Arnold, K.E., Brown, C.D., High prevalence of the neonicotinoid clothianidin in liver and plasma samples collected from gamebirds during autumn sowing. Sci. Total Environ., 742, 2020, 140493, 10.1016/j.scitotenv.2020.140493.
Li, Y., Miao, R., Khanna, M., Neonicotinoids and decline in bird biodiversity in the United States. Nat. Sustain. 3 (2020), 1027–1035, 10.1038/s41893-020-0582-x.
Lopez-Antia, A., Ortiz-Santaliestra, M.E., Mougeot, F., Mateo, R., Experimental exposure of red-legged partridges (Alectoris rufa) to seeds coated with imidacloprid, thiram and difenoconazole. Ecotoxicology 22 (2013), 125–138, 10.1007/s10646-012-1009-x.
Lopez-Antia, A., Ortiz-Santaliestra, M.E., Camarero, P.R., Mougeot, F., Mateo, R., Assessing the risk of fipronil-treated seed ingestion and associated adverse effects in the red-legged partridge. Environ. Sci. Technol. 49 (2015), 13649–13657, 10.1021/acs.est.5b03822.
Lopez-Antia, A., Ortiz-Santaliestra, M.E., Mougeot, F., Mateo, R., Imidacloprid-treated seed ingestion has lethal effect on adult partridges and reduces both breeding investment and offspring immunity. Environ. Res. 136 (2015), 97–107, 10.1016/j.envres.2014.10.023.
Lv, Y., Bing, Q., Lv, Z., Xue, J., Li, S., Han, B., Yang, Q., Wang, X., Zhang, Z., Imidacloprid-induced liver fibrosis in quails via activation of the TGF-β1/Smad pathway. Sci. Total Environ., 705, 2020, 135915, 10.1016/j.scitotenv.2019.135915.
McKay, H.V., Prosser, P.J., Hart, A.D.M., Langton, S.D., Jones, A., McCoy, C., Chandler-Morris, S.A., Pascual, J.A., Do wood‐pigeons avoid pesticide‐treated cereal seed?. J. Appl. Ecol. 36 (1999), 283–296, 10.1046/j.1365-2664.1999.00398.x.
Millon, A., Arroyo, B.E., Bretagnolle, V., Variable but predictable prey availability affects predator breeding success: natural versus experimental evidence. J. Zool. 275 (2008), 349–358, 10.1111/j.1469-7998.2008.00447.x.
Millot, F., Decors, A., Mastain, O., Quintaine, T., Berny, P., Vey, D., Lasseur, R., Bro, E., Field evidence of bird poisonings by imidacloprid-treated seeds: a review of incidents reported by the French SAGIR network from 1995 to 2014. Environ. Sci. Pollut. Res. 24 (2017), 5469–5485, 10.1007/s11356-016-8272-y.
Mineau, P., Whiteside, M., Pesticide acute toxicity is a better correlate of US grassland bird declines than agricultural intensification. PLoS One, 8, 2013, e57457, 10.1371/journal.pone.0057457.
Mitra, A., Chatterjee, C., Mandal, F.B., Synthetic chemical pesticides and their effects on birds. Res. J. Environ. Toxicol. 5 (2011), 81–96, 10.3923/rjet.2011.81.96.
Mohanty, B., Pandey, S.P., Tsutsui, K., Thyroid disrupting pesticides impair the hypothalamic-pituitary-testicular axis of a wildlife bird, Amandava amandava. Reprod. Toxicol. 71 (2017), 32–41, 10.1016/j.reprotox.2017.04.006.
Moreau, J., Monceau, K., Crépin, M., Tochon, F.D., Mondet, C., Fraikin, M., Teixeira, M., Bretagnolle, V., Feeding partridges with organic or conventional grain triggers cascading effects in life-history traits. Environ. Pollut., 278, 2021, 116851, 10.1016/j.envpol.2021.116851.
Moreau, J., Rabdeau, J., Badenhausser, I., Giraudeau, M., Sepp, T., Crépin, M., Gaffard, A., Bretagnolle, V., Monceau, K., Pesticide impacts on avian species with special reference to farmland birds: a review. Environ. Monit. Assess. 194 (2022), 1–48, 10.1007/s10661-022-10394-0.
Moreau, J., Monceau, K., Gonnet, G., Pfister, M., Bretagnolle, V., Organic farming positively affects the vitality of passerine birds in agricultural landscapes. Agric. Ecosyst. Environ., 336, 2022, 108034, 10.1016/j.agee.2022.108034.
Nauen, R., Ebbinghaus-Kintscher, U., Salgado, V.L., Kaussmann, M., Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pestic. Biochem. Physiol. 76 (2003), 55–69, 10.1016/S0048-3575(03)00065-8.
Pacyna-Kuchta, A.D., What should we know when choosing feather, blood, egg or preen oil as biological samples for contaminants detection? A non-lethal approach to bird sampling for PCBs, OCPs, PBDEs and PFASs. Crit. Rev. Environ. Sci. Technol. 53 (2023), 625–649, 10.1080/10643389.2022.2077077.
Pan, Y., Chang, J., Xu, P., Xie, Y., Yang, L., Hao, W., Li, J., Wan, B., Twenty-four hours of Thiamethoxam: in vivo and molecular dynamics simulation study on the toxicokinetic and underlying mechanisms in quails (Coturnix japonica). J. Hazard Mater., 427, 2022, 128159, 10.1016/j.jhazmat.2021.128159.
Pelosi, C., Bertrand, C., Daniele, G., Coeurdassier, M., Benoit, P., Nélieu, S., Lafay, F., Bretagnolle, V., Gaba, S., Vulliet, E., Fritsch, C., Residues of currently used pesticides in soils and earthworms: a silent threat?. Agric. Ecosyst. Environ., 305, 2021, 107167, 10.1016/j.agee.2020.107167.
Pelosi, C., Bertrand, C., Bretagnolle, V., Coeurdassier, M., Delhomme, O., Deschamps, M., Gaba, S., Millet, M., Nélieu, S., Fritsch, C., Glyphosate, AMPA and glufosinate in soils and earthworms in a French arable landscape. Chemosphere, 301, 2022, 134672, 10.1016/j.chemosphere.2022.134672.
Perkins, R., Whitehead, M., Civil, W., Goulson, D., Potential role of veterinary flea products in widespread pesticide contamination of English rivers. Sci. Total Environ., 755, 2021, 143560, 10.1016/j.scitotenv.2020.143560.
Rawi, S.M., Al-Logmani, A.S., Hamza, R.Z., Neurological alterations induced by formulated imidacloprid toxicity in Japanese quails. Metab. Brain Dis. 34 (2019), 443–450, 10.1007/s11011-018-0377-1.
Rodrigues, A., Gaffard, A., Moreau, J., Monceau, K., Delhomme, O., Millet, M., Analytical development for the assessment of pesticide contaminations in blood and plasma of wild birds: the case of grey partridges (Perdix Perdix). J. Chromatogr. A, 1687, 2023, 463681, 10.1016/j.chroma.2022.463681.
Rosenberg, K.V., Dokter, A.M., Blancher, P.J., Sauer, J.R., Smith, A.C., Smith, P.A., Stanton, J.C., Panjabi, A., Helft, L., Parr, M., Marra, P.P., Decline of the North American avifauna. Science 366 (2019), 120–124, 10.1126/science.aaw1313.
Rust, M.K., The biology and ecology of cat fleas and advancements in their pest management: a review. Insects, 8, 2017, 118, 10.3390/insects8040118.
Ruuskanen, S., Rainio, M.J., Kuosmanen, V., Laihonen, M., Saikkonen, K., Saloniemi, I., Helander, M., Female preference and adverse developmental effects of glyphosate-based herbicides on ecologically relevant traits in Japanese quails. Environ. Sci. Technol. 54 (2020), 1128–1135, 10.1021/acs.est.9b07331.
Salamolard, M., Butet, A., Leroux, A., Bretagnolle, V., Responses of an avian predator to variations in prey density at a temperate latitude. Ecology 81 (2000), 2428–2441, 10.1890/0012-9658(2000)081[2428 ROAAPT]2.0.CO;2.
Simon-Delso, N., Amaral-Rogers, V., Belzunces, L.P., Bonmatin, J.M., Chagnon, M., Downs, C., Furlan, L., Gibbons, D.W., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D.P., Krupke, C.H., Liess, M., Long, E., McField, M., Mineau, P., Mitchell, E.A.D., Morrissey, C.A., Noome, D.A., Pisa, L., Settele, J., Stark, J.D., Tapparo, A., Van Dyck, H., Van Praagh, J., Van der Sluijs, J.P., Whitehorn, P.R., Wiemers, M., Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ. Sci. Pollut. R. 22 (2015), 5–34, 10.1007/s11356-014-3470-y.
Stanton, R.L., Morrissey, C.A., Clark, R.G., Analysis of trends and agricultural drivers of farmland bird declines in North America: a review. Agric. Ecosyst. Environ. 254 (2018), 244–254, 10.1016/j.agee.2017.11.028.
Story, P., Cox, M., Review of the effects of organophosphorus and carbamate insecticides on vertebrates. Are there implications for locust management in Australia?. Wildl. Res. 28 (2001), 179–193, 10.1071/WR99060.
Taliansky-Chamudis, A., Gómez-Ramírez, P., León-Ortega, M., García-Fernández, A.J., Validation of a QuECheRS method for analysis of neonicotinoids in small volumes of blood and assessment of exposure in Eurasian eagle owl (Bubo bubo) nestlings. Sci. Total Environ. 595 (2017), 93–100, 10.1016/j.scitotenv.2017.03.246.
Tassin de Montaigu, C., Goulson, D., Identifying agricultural pesticides that may pose a risk for birds. PeerJ, 8, 2020, e9526, 10.7717/peerj.9526.
Teerlink, J., Hernandez, J., Budd, R., Fipronil washoff to municipal wastewater from dogs treated with spot-on products. Sci. Total Environ. 599 (2017), 960–966, 10.1016/j.scitotenv.2017.04.219.
Thompson, D.A., Lehmler, H.J., Kolpin, D.W., Hladik, M.L., Vargo, J.D., Schilling, K.E., LeFevre, G.H., Peeples, T.L., Poch, M.C., LaDuca, L.E., Cwiertny, D.M., Field, R.W., A critical review on the potential impacts of neonicotinoid insecticide use: current knowledge of environmental fate, toxicity, and implications for human health. Environ. Sci.-Proc. Imp. 22 (2020), 1315–1346, 10.1039/C9EM00586B.
Tokumoto, J., Danjo, M., Kobayashi, Y., Kinoshita, K., Omotehara, T., Tatsumi, A., Hashiguchi, M., Sekijima, T., Kamisoyama, H., Yokoyama, T., Kitagawa, H., Hoshi, N., Effects of exposure to clothianidin on the reproductive system of male quails. J. Vet. Med. Sci. 75 (2013), 755–760, 10.1292/jvms.12-0544.
Tomizawa, M., Casida, J.E., Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annu. Rev. Entomol. 48 (2003), 339–364, 10.1146/annurev.ento.48.091801.112731.
Tomizawa, M., Casida, J.E., Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu. Rev. Pharmacol. 45 (2005), 247–268, 10.1146/annurev.pharmtox.45.120403.095930.
Walker, C.H., Neurotoxic pesticides and behavioural effects upon birds. Ecotoxicology 12 (2003), 307–316, 10.1023/A:1022523331343.
Wang, Y., Han, Y., Xie, Y., Xu, P., Li, W., The metabolism distribution and effect of dinotefuran in Chinese lizards (Eremias argus). Chemosphere 211 (2018), 591–599, 10.1016/j.chemosphere.2018.07.181.
Williams, O., The Woodcock Network. 2015 http://www.ringwoodcock.net/index.shtml Accessed date: 12 October 2022.
Wintermantel, D., Locke, B., Andersson, G.K., Semberg, E., Forsgren, E., Osterman, J., Pedersen, T.R., Bommarco, R., Smith, H.G., Rundlöf, M., de Miranda, J.R., Field-level clothianidin exposure affects bumblebees but generally not their pathogens. Nat. Commun. 9 (2018), 1–10, 10.1038/s41467-018-07914-3.
Wintermantel, D., Odoux, J.F., Decourtye, A., Henry, M., Allier, F., Bretagnolle, V., Neonicotinoid-induced mortality risk for bees foraging on oilseed rape nectar persists despite EU moratorium. Sci. Total Environ., 704, 2020, 135400, 10.1016/j.scitotenv.2019.135400.
Wood, T.J., Goulson, D., The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Sci. Pol. R. 24 (2017), 17285–17325, 10.1007/s11356-017-9240-x.
Wretenberg, J., Lindström, Å., Svensson, S., Thierfelder, T., Pärt, T., Population trends of farmland birds in Sweden and England: similar trends but different patterns of agricultural intensification. J. Appl. Ecol. 43 (2006), 1110–1120, 10.1111/j.1365-2664.2006.01216.x.
Zhang, C., Li, X., Li, F., Li, G., Niu, G., Chen, H., Ying, G.-G., Huang, M., Accurate prediction and further dissection of neonicotinoid elimination in the water treatment by CTS@ AgBC using multihead attention-based convolutional neural network combined with the time-dependent Cox regression model. J. Hazard Mater., 423, 2022, 127029, 10.1016/j.jhazmat.2021.127029.
Zhang, Q., Hu, S., Dai, W., Gu, S., Ying, Z., Wang, R., Lu, C., The partitioning and distribution of neonicotinoid insecticides in human blood. Environ. Pollut., 2023, 121082, 10.1016/j.envpol.2023.121082.