Neonicotinoid pesticide applications affect pollinator abundance and visitation, leading to implications for sunflower production (Helianthus annuus L.)

References

• Aytekin, A. M., & Agatay, C. N. (2008). Observations on the pollination of sunflower (Helianthus annuus L.). Mellifera, 8(14), 2–16.
   Google Scholar
• Badar, H. (2000). Economics of sunflower production in the province of Punjab (Pakistan) [ M.Sc. (Hons.) Thesis] Department of Agricultural Economics, Univ.
   Google Scholar
• Belzunces, L. P., Tchamitchian, S., & Brunet, J.-L. (2012). Neural effects of insecticides in the honey bee. Apidologie, 43(3), 348–370. https://doi.org/10.1007/s13592-012-0134-0
   Web of Science ®Google Scholar
• Biesmeijer, J. C., Roberts, S. P. M., Reemer, M., Ohlemuller, R., Edwards, M., Peeter, T., Schaffers, A. P., Potts, S. G., Kleukers, M. R., Thomas, C. D., Settele, J., & Kunin, W. E. (2006). Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313(5785), 351–354. https://doi.org/10.1126/science.1127863
   PubMed Web of Science ®Google Scholar
• Bortolotti, L., Montanari, R., Marcelino, J., Medrzycki, P., Maini, S., & Porrini, C. (2003). Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bulletin of Insectology, 56(1), 63–68.
   Google Scholar
• Botías, C., David, A., Hill, E. M., & Goulson, D. (2016). Contamination of wild plants near neonicotinoid seed-treated crops, and implications for non-target insects. The Science of the Total Environment 566, 269–278. [CrossRef] [PubMed]. https://doi.org/10.1016/j.scitotenv.2016.05.065
   PubMed Web of Science ®Google Scholar
• Carvalheiro, L. G., Veldtman, R., Shenkute, A. G., Tesfay, G. B., Pirk, C. W. W., Donaldson, J. S., & Nicolson, S. W. (2011). Natural and within-farmland biodiversity enhances crop productivity. Ecology Letters, 14(3), 251–259. https://doi.org/10.1111/j.1461-0248.2010.01579.x
   PubMed Web of Science ®Google Scholar
• Chacoff, N. P., & Aizen, M. A. (2005). Edge effects on flower-visiting insects in grapefruit plantations bordering premontane subtropical forest. The Journal of Applied Ecology, 43(1), 18–27. https://doi.org/10.1111/j.1365-2664.2005.01116.x
   Web of Science ®Google Scholar
• Dag, A., Zipori, I., & Pleser, Y. (2006). Using bumblebees to improve almond pollination by the honeybee. Journal of Apicultural Research, 45(4), 215–216. https://doi.org/10.1080/00218839.2006.11101350
   Web of Science ®Google Scholar
• Damalas, C. A. (2009). Understanding benefits and risks of pesticide use. Scientific Research and Essays, 4(10), 945–949.
   Google Scholar
• Damalas, C. A., & Eleftherohorinos, I. G. (2011). Pesticide exposure, safety issues, and risk assessment indicators. International Journal of Environmental Research & Public Health, 8(5), 1402–1419. https://doi.org/10.3390/ijerph8051402
   PubMed Web of Science ®Google Scholar
• Da Silva, I. P., Oliveira, F. A. S., Pedroza, H. P., Gadelha, I. C. N., Melo, M. M., & Soto-Blanco, B. (2015). Pesticide exposure of honey bees (Apis mellifera) pollinating melon crops. Apidologi, 46(6), 703–715. https://doi.org/10.1007/s13592-015-0360-3
   Web of Science ®Google Scholar
• Degrandi-Hoffman, G., & Watkins, J. C. (2000). The foraging activity of honey bees Apis mellifera and non—Apis bees on hybrid sunflowers (Helianthus annuus) and its influence on cross—pollination and seed set. Journal of Apicultural Research, 39(1–2), 37–45. https://doi.org/10.1080/00218839.2000.11101019
   Web of Science ®Google Scholar
• De Marco, P., & Coelho, F. M. (2004). Services performed by the ecosystem: Forest remnants influence agricultural cultures' pollination and production. Biodiversity and Conservation, 13, 1245–1255. https://doi.org/10.1023/B:BIOC.0000019402.51193.e8
   Web of Science ®Google Scholar
• Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52(1), 81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440
   PubMed Web of Science ®Google Scholar
• Elston, C., Thompson, H. M., & Walters, K. F. A. (2013). Sub-lethal effects of thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (bombus terrestris) micro-colonies. Apidologie, 44(5), 563–574. https://doi.org/10.1007/s13592-013-0206-9
   Web of Science ®Google Scholar
• Free, J. B. (1993). Insect pollination of crops. Academic Press.
   Google Scholar
• Freitas, B. M., & Pinheiro, J. N. (2010). Efeitos sub-letais dos pesticidas agrıcolas e seus impactos no manejo de polinizadores dos agroecossistemas brasileiros. Oecologia Australis, 14(1), 282–298. https://doi.org/10.4257/oeco.2010.1401.17
   Google Scholar
• Freitas, B. M., & Pinheiro, J. N. (2012). Polinizadores e pesticidas: Princıpios e manejo para os agroecossistemas brasileiros. MMA.
   Google Scholar
• Garantonakis, N., Varikou, K., Birouraki, A., Edwards, M., Kalliakaki, V., & Andrinopoulos, F. (2016). Comparing the pollination services of honey bees and wild bees in a watermelon field. Scientia Horticulturae 204, 138–144. [CrossRef]. https://doi.org/10.1016/j.scienta.2016.04.006
   Web of Science ®Google Scholar
• Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., Aizen, M. A., Bommarco, R., Cunningham, S. A., Kremen, C., Carvalheiro, L. G., Harder, L. D., Afik, O., Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N. P., Dudenhoffer, J. H., Freitas, B. M., Ghazoul, J. … Williams, N. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339(6127), 1608–1611. https://doi.org/10.1126/science.1230200
   PubMed Web of Science ®Google Scholar
• Godfray, H. C., Blacquiere, T., Field, L. M., Hails, R. S., Petrokofsky, G., Potts, S. G., Raine, N. E., Vanbergen, A. J., & McLean, A. R. (2014). A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B: Biological Sciences, 281(1786), 20140558. https://doi.org/10.1098/rspb.2014.0558
   PubMed Web of Science ®Google Scholar
• Goulson, D., & Kleijn, D. (2013). Review: An overview of the environmental risks posed by neonicotinoid insecticides. The Journal of Applied Ecology, 50(4), 977–987. https://doi.org/10.1111/1365-2664.12111
   Web of Science ®Google Scholar
• Goulson, D., Nicholls, E., Botías, C., & Rotheray, E. L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229), 1255957. https://doi.org/10.1126/science.1255957
   PubMed Web of Science ®Google Scholar
• Greenleaf, S. S., & Kremen, C. (2006). Wild bees enhance honey bees’ pollination of hybrid sunflower. Proceedings of the National Academy of Sciences, 103(37), 13890–13895. https://doi.org/10.1073/pnas.0600929103
   PubMed Web of Science ®Google Scholar
• Henry, M., Be´guin, M., Requier, F., Rollin, O., Odoux, J. F., Aupinel, P., Aptel, J., Tchamitchian, S., & Decourtye, A. (2012). A common pesticide decreases foraging success and survival in honey bees. Science, 336(6079), 348–350. https://doi.org/10.1126/science.1215039
   PubMed Web of Science ®Google Scholar
• Hung, K.-L. J., Kingston, J. M., Albrecht, M., Holway, D. A., & Kohn, J. R. (2018). The worldwide importance of honey bees as pollinators in natural habitats. Proceedings of the Royal Society B: Biological Sciences, 285(1870), 20172140–20172147. [CrossRef]. https://doi.org/10.1098/rspb.2017.2140
   PubMed Web of Science ®Google Scholar
• Jacques, A., Laurent, M., Consortium, E., Ribière-Chabert, M., Saussac, M., Bougeard, S., Budge, G. E., Hendrikx, P., & Chauzat, M.-P. (2017). A pan-European epidemiological study reveals honey bee colony survival depends on beekeeper education and disease control. PLoS ONE, 12(3), e0172591. [Google Scholar] [CrossRef][Green Version]. https://doi.org/10.1371/journal.pone.0172591
   PubMed Web of Science ®Google Scholar
• Jadhav, J. A., Sreedevi, K., & Prasad, P. R. (2011). Insect pollinator diversity and abundance in sunflower ecosystem. Current Biotica, 5(3), 344–350.
   Google Scholar
• Jensen, E. (2015). Banning neonicotinoids: Ban first, ask questions later. Seattle Journal of Environ Law, 5(1). https://digitalcommons.law.seattleu.edu/sjel/vol5/iss1/3
   Google Scholar
• Ke, L., Chen, X., Dai, P., & Liu, Y. J. (2023). Chronic larval exposure to thiacloprid impairs honeybee antennal selectivity, learning and memory performances. Frontiers in Physiology, 14, 1114488. https://doi.org/10.3389/fphys.2023.1114488
   PubMed Web of Science ®Google Scholar
• Klein, A. M., Vaissiere, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274(1608), 303–313. https://doi.org/10.1098/rspb.2006.3721
   PubMed Web of Science ®Google Scholar
• Kreitlow, R., Antonio, L. I. M. A., Pinheiro, M., Mendelson, L. I. M. A., Santos, F., & Loureiro, E. (2014). Efici^encia da polinizac¸~ao de Apis mellifera L. (Hymenoptera: Apidae) na cultura do girassol (Helianthus annuus L.) proximo a fragment de mata nativa. Cadernos de Agroecologia, 9(4), 2236–7934.
   Google Scholar
• Kremen, C., Williams, N. M., & Thorp, R. W. (2002). Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences USA, 99(26), 16812–16816. https://doi.org/10.1073/pnas.262413599
   PubMed Web of Science ®Google Scholar
• Kumar, N., & Singh, R. (2005). Relative abundance of Apis sp. on rabi season sunflower (Helianthus annus. Journal of Entomology Research, 29(1), 65–69.
   Google Scholar
• Ladurner, E., Bosch, J., Kemp, W. P., & Maini, S. (2005). Assessing delayed and acute toxicity of five formulated fungicides to Osmia lignaria say and Apis mellifera. Apidologie, 36(3), 449–460. https://doi.org/10.1051/apido:2005032
   Web of Science ®Google Scholar
• Losey, J., & Vaughn, M. (2006). The economic value of ecological services provided by insects. BioScience, 56(4), 311–323. https://doi.org/10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2
   Web of Science ®Google Scholar
• Mallinger, R. E., Franco, J. G., Prischmann-Voldseth, D. A., & Prasifka, J. R. (2019). Annual cover crops for managed and wild bees: Optimal plant mixtures depend on pollinator enhancement goals. Agriculture, Ecosystems & Environment 273, 107–116. [Google Scholar] [CrossRef]. https://doi.org/10.1016/j.agee.2018.12.006
   Web of Science ®Google Scholar
• McGregor, S. E. (1976). Insect pollination of cultivated crop plants. Agricultural Research Service. US Department of Agriculture.
   Google Scholar
• Mommaerts, V., Reynders, S., Boulet, J., Besard, L., Sterk, G., & Smagghe, G. (2010). Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology, 19(1), 207–215. https://doi.org/10.1007/s10646-009-0406-2
   PubMed Web of Science ®Google Scholar
• Morandin, L. A., & Winston, M. L. (2005). Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecological Applications: A Publication of the Ecological Society of America, 15(3), 871–881. https://doi.org/10.1890/03-5271
   Web of Science ®Google Scholar
• Nauen, R., Ebbinghaus-Kintscher, U., Salgado, V. L., & Kaussmann, M. (2003). Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pesticide Biochemistry and Physiology, 76(2), 55–69. https://doi.org/10.1016/S0048-3575(03)00065-8
   Web of Science ®Google Scholar
• Nderitu, J., Nyamasyo, G., Kasina, M., & Oronje, M. L. (2008). Diversity of sunflower pollinators and their effect on seed yield in Makueni District, Eastern Kenya. Spanish Journal of Agricultural Research, 6(2), 271–278. https://doi.org/10.5424/sjar/2008062-318
   Web of Science ®Google Scholar
• Nigg, H. N., Russ, R. V., Mahon, W. D., Stamper, J. H., & Knapp, J. L. (1991). Contamination of sucrose solution with aldicarb sulfoxide inhibits foraging by honey bees (Hymenoptera: Apidae). Journal of Economic Entomology, 84(3), 810–813. https://doi.org/10.1093/jee/84.3.810
   Web of Science ®Google Scholar
• Olmstead, A. L., & Wooten, D. W. (1987). Bee pollination and productivity growth: The case of alfalfa. American Journal of Agricultural Economics, 69(1), 56–63. https://doi.org/10.2307/1241306
   Web of Science ®Google Scholar
• Oz, M., Karasu, A., Cakmak, I., Goksoy, A. T., & Turan, Z. M. (2009). Effects of honeybee (Apis mellifera) pollination on seed set in hybrid sunflower (Helianthus annuus L.) afr. Journal of Biotechnology, 8(6), 1037–1043.
   Web of Science ®Google Scholar
• Pakistan Economic Survey. (2021-22). Govt. Of Pakistan, Ministry of finance. https://www.finance.gov.pk/survey/chapter_22/PES02-AGRICULTURE.pdf
   Google Scholar
• Partap, T. (2001). Mountain agriculture marginal land and sustainable livelihood: Challenges and opportunities. International Symposium on Mountain Agriculture in HKH region, ICIMOD, Kathmandu, Nepal.
   Google Scholar
• Pettis, J. S., Lichtenberg, E. M., Andree, M., Stitzinger, J., Rose, R., & vanEngelsdorp, D. (2013). Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen nosema ceranae. PLoS ONE, 8(7), e70182. 0070182. https://doi.org/10.1371/journal.pone.0070182
   PubMed Web of Science ®Google Scholar
• Pinheiro, J. N., & Freitas, B. M. (2010). EFEITOS LETAIS DOS PESTICIDAS AGRÍCOLAS SOBRE POLINIZADORES E PERSPECTIVAS DE MANEJO PARA OS AGROECOSSISTEMAS BRASILEIROS. Oecologia Australis, 14(1), 266–281. https://doi.org/10.4257/oeco.2010.1401.16
   Google Scholar
• Pisa, L. W., Amaral-Rogers, V., Belzunces, L. P., Bonmatin, J. M., Downs, C. A., Goulson, D., Kreutzweiser, D. P., Krupke, C., Liess, M., McField, M., Morrissey, C. A., Noome, D. A., Settele, J., Simon-Delso, N., Stark, J. D., Van der Sluijs, J. P., Van Dyck, H., & Wiemers, M. (2015). Effects of neonicotinoids and fipronil on non-target invertebrates. Environmental Science and Pollution Research, 22(1), 68–102. https://doi.org/10.1007/s11356-014-3471-x
   PubMed Web of Science ®Google Scholar
• Rader, R., Bartomeus, I., Garibaldi, L. A., Garratt, M. P. D., Howlett, B. G., Winfree, R., Cunningham, S. A., Mayfield, M. M., Arthur, A. D., Andersson, G. K. S., Bommarco, R., Brittain, C., Carvalheiro, L. G., Chacoff, N. P., Entling, M. H., Foully, B., Freitas, B. M., Gemmill-Herren, B. … Viana, B. F. (2016). Non-bee insects are important contributors to global crop pollination. Proceedings of the National Academy of Sciences of the United States of America, 113(1), 146–151. [Google Scholar] [CrossRef][Green Version]. https://doi.org/10.1073/pnas.1517092112
   PubMed Web of Science ®Google Scholar
• Ricketts, T. H., Regetz, J., Steffan‐Dewenter, I., Cunningham, S. A., Kremen, C., Bogdanski, A., Gemmill-Herren, B., Greenleaf, S. S., Klein, A. M., Mayfield, M. M., Morandin, L. A., Ochieng’, A., & Viana, B. F. (2008). Landscape effects on crop pollination services: Are there general patterns? Ecology Letters, 11(5), 499–515. https://doi.org/10.1111/j.1461-0248.2008.01157.x
   PubMed Web of Science ®Google Scholar
• Rundlöf, M., Andersson, G. K., Bommarco, R., Fries, I., Hederström, V., Herbertsson, L., & Smith, H. G. (2015). Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature, 521(7550), 77–80. https://doi.org/10.1038/nature14420
   PubMed Web of Science ®Google Scholar
• Sanchez-Bayo, F. (2014). The trouble with neonicotinoids. Science, 346(6211), 806–807. https://doi.org/10.1126/science.1259159
   PubMed Web of Science ®Google Scholar
• Schaafsma, A., Limayrios, V., Baute, T., Smith, J., Xue, Y., & Spanoghe, P. (2015). Neonicotinoid insecticide residues in surface water and soil associated with commercial maize (corn) fields in southwestern Ontario. PLoS ONE, 10(2), e0118139. [CrossRef] [PubMed]. https://doi.org/10.1371/journal.pone.0118139
   PubMed Web of Science ®Google Scholar
• Shah, N. A., Aujla, K. M., Ishaq, M., & Farooq, A. (2013). Trends in sunflower production and its potential in increasing domestic edible oil production in Punjab, Pakistan. Sarhad Journal of Agriculture, 29(1), 7–13.
   Google Scholar
• Shaheen, F. A., Khan, K. A., Husain, M., Mahmood, R., & Rafique, M. K. (2017). Role of honey bees (Apis mellifera L.) foraging activities in increased fruit setting and production of apples (Malus domestica). Pakistan Journal of Agricultural Research, 30(1), 1–6.
   Google Scholar
• Solomon, M. G., & Hooker, K. J. M. (1989). Chemical repellents for reducing pesticide hazard to honey bees in apple orchards. Journal of Apicultural Research, 28(4), 223–227. https://doi.org/10.1080/00218839.1989.11101188
   Web of Science ®Google Scholar
• Spadotto, C. A., Gomes, M. A. F., Luchini, L. C., & De Andrea, M. M. (2004). Monitoramento do risco ambiental de agrotoxicos: Princıpios e recomendac¸~oes. Embrapa Meio Ambiente Documentos, 42(1), 223–227.
   Google Scholar
• Stanley, D. A., Garratt, M. P., Wickens, J. B., Wickens, V. J., Potts, S. G., & Raine, N. E. (2015). Neonicotinoid pesticide exposure impairs crop pollination services provided by bumble bees. Nature, 528(7583), 548–550. https://doi.org/10.1038/nature16167
   PubMed Web of Science ®Google Scholar
• Staveley, J. P., Law, S. A., Fairbrother, A., & Menzie, C. A. (2014). A causal analysis of observed declines in managed honey bees (Apis mellifera). Human and Ecological Risk Assessment: An International Journal, 20(2), 566–591. https://doi.org/10.1080/10807039.2013.831263
   PubMed Web of Science ®Google Scholar
• Steffan-Dewenter, I. (2003). Importance of habitat area and landscape context for species richness of bees and wasps in fragmented orchard meadows. Conservation Biology: The Journal of the Society for Conservation Biology, 17(4), 1036–1044. https://doi.org/10.1046/j.1523-1739.2003.01575.x
   Web of Science ®Google Scholar
• Stuligross, C., Melone, G. G., Wang, L., & Williams, N. M. (2023). Sublethal behavioral impacts of resource limitation and insecticide exposure reinforce negative fitness outcomes for a solitary bee. Science of the Total Environment, 867, 161392. https://doi.org/10.1016/j.scitotenv.2023.161392
   PubMed Web of Science ®Google Scholar
• Tan, A. S., Ozturk, A. I., & Karaca, U. (2002). Effect of honeybee pollination on seed yield and quality of sunflower. Anadolu University Science Journal, 12(1), 1–26.
   Google Scholar
• Tomizawa, M., & Casida, J. E. (2005). NEONICOTINOID INSECTICIDE TOXICOLOGY: Mechanisms of selective action. Annual Review of Pharmacology and Toxicology, 45(1), 247–268. https://doi.org/10.1146/annurev.pharmtox.45.120403.095930
   PubMed Web of Science ®Google Scholar
• Tomizawa, M., Lee, D. L., & Casida, J. E. (2000). Neonicotinoid insecticides: Molecular features conferring selectivity for insect versus Mammalian Nicotinic Receptors. Journal of Agricultural & Food Chemistry, 48(12), 6016–6024. 2000. https://doi.org/10.1021/jf000873c
   PubMed Web of Science ®Google Scholar
• Valdovinos-Nu~nez, G. R., Quezada-Euan, J. J. G., Ancona-Xiu, P., Moovalle, H., Carmona, A., & Sanchez, E. R. (2009). Comparative toxicity of pesticides to stingless bees (Hymenoptera: Apidae: Meliponini). Journal of Economic Entomology, 102(5), 1737–1742. https://doi.org/10.1603/029.102.0502
   PubMed Web of Science ®Google Scholar
• Van der Sluijs, J. P., Simon-Delso, N., Goulson, D., Maxim, L., Bonmatin, J.-M., & Belzunces, L. P. (2013). Neonicotinoids, bee disorders and the sustainability of pollinator services. Current Opinion in Environmental Sustainability, 5(3–4), 293–305. 2013. https://doi.org/10.1016/j.cosust.2013.05.007
   Web of Science ®Google Scholar
• Whitehorn, P. R., O’Connor, S., Wackers, F. L., & Goulson, D. (2012). Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science, 336(6079), 351–352. https://doi.org/10.1126/science.1215025
   PubMed Web of Science ®Google Scholar
• Williams, I. H. (1994). The dependence of crop production within the European Union on pollination by honey bees. Agricultural Zoology Reviews, 6, 229–257.
   Google Scholar
• Wright, G. A., Mustard, J. A., Simcock, N. K., Ross-Taylor, A. A., Mcnicholas, L. D., Popescu, A., & Marion-Poll, F. (2010). Parallel reinforcement pathways for conditioned food aversions in the honey bee. Current Biology: CB, 20(24), 2234–2240. https://doi.org/10.1016/j.cub.2010.11.040
   PubMed Web of Science ®Google Scholar