Pollinators can detect the color, shape, scent, and even temperature of the flowers they want to visit. Here, we present the previously unappreciated capacity of hoverflies (Eristalis tenax and Cheilosia albipila) to detect the electric field surrounding flowers. Using hoverflies as key dipteran pollinators, we explored the electrical interactions between flies and flowers-how a hoverfly acquired a charge and how their electrical sensing ability for target flowers contributed to nectar identification and pollination. This study revealed that rapid variations in a floral electric field were related to a nectar reward and increased the likelihood of the fly's return visits. We found that thoracic hairs played a role in the polarity of hoverfly charge, revealing their electro-mechanosensory capability, as in bumblebees (Bombus terrestris). Electrophysiological analysis of the hoverfly's antennae did not reveal neural sensitivity to the electric field, which favors the mechanosensory hairs as putative electroreceptive organs in both species of hoverflies.

Biology Department Faculty of Science King Khalid University P O Box 9004 Abha 61413 Saudi Arabia

Department of Biological Sciences College of Science University of Jeddah Jeddah Saudi Arabia

Department of Biotechnology Fatima Jinnah Women University Rawalpindi Pakistan

Department of Botany and Plant Physiology Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamycka 129 165 00 Prague Czechia

Department of Botany University of Gujarat Gujarat 50700 Pakistan

Department of Physics Allama Iqbal Open University Islamabad 44000 Pakistan

Department of Zoology and Fisheries Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamycka 129 165 00 Praha 6 Suchdol Czech Republic

Institute of Apicultural Research Key Laboratory of Pollinating Insect Biology Ministry of Agriculture Chinese Academy of Agricultural Sciences Beijing 100093 China

Laboratory of Apiculture Department of Entomology Pir Mehr Ali Shah Arid Agriculture University Rawalpindi 46000 Pakistan

Research Center for Advanced Materials Science King Khalid University P O Box 9004 Abha 61413 Saudi Arabia

Unit of Bee Research and Honey Production Faculty of Science King Khalid University P O Box 9004 Abha 61413 Saudi Arabia

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Chittka L, Raine NE. Recognition of flowers by pollinators. Curr. Opin. Plant Biol. 2006;9:428–435. doi: 10.1016/j.pbi.2006.05.002. PubMed DOI

Raguso RA. Flowers as sensory billboards: Progress towards an integrated understanding of floral advertisement. Curr. Opin. Plant Biol. 2004;7:434–440. doi: 10.1016/j.pbi.2004.05.010. PubMed DOI

Goulson D, Stout JC, Hawson SA. Can flower constancy in nectaring butterflies be explained by Darwin's interference hypothesis? Oecologia. 1997;112:225–231. doi: 10.1007/s004420050304. PubMed DOI

Goulson D, Wright NP. Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.) (Syrphidae) Behav. Ecol. 1998;9:213–219. doi: 10.1093/beheco/9.3.213. DOI

Von Arx M, Goyret J, Davidowitz G, Raguso RA. Floral humidity as a reliable sensory cue for profitability assessment by nectar-foraging hawkmoths. Proc. Natl. Acad. Sci. 2012;109:9471–9476. doi: 10.1073/pnas.1121624109. PubMed DOI PMC

Leonard AS, Dornhaus A, Papaj DR. Forget-me-not: Complex floral displays, inter-signal interactions, and pollinator cognition. Curr. Zool. 2011;57:215–224. doi: 10.1093/czoolo/57.2.215. DOI

Vaknin Y, Gan-Mor S, Bechar A, Ronen B, Eisikowitch D. The role of electrostatic forces in pollination. Plant Syst. Evol. 2000;222:133–142. doi: 10.1007/bf00984099. DOI

Bowker GE, Crenshaw HC. Electrostatic forces in wind-pollination—Part 2: Simulations of pollen capture. Atmos. Environ. 2007;41:1596–1603. doi: 10.1016/j.atmosenv.2006.10.048. DOI

Erickson E. Surface electric potentials on worker honeybees leaving and entering the hive. J. Apic. Res. 1975;14:141–147. doi: 10.1080/00218839.1975.11099818. DOI

Edwards D. Electrostatic charges on insects due to contact with different substrates. Can. J. Zool. 1962;40:579–584. doi: 10.1139/z62-051. DOI

Vaknin Y, Gan-Mor S, Bechar A, Ronen B, Eisikowitch D. Pollen and Pollination. Springer; 2000. pp. 133–142.

Eskov E, Sapozhnikov A. Mechanism of generation and perception of electric fields by honey bees. Biofizika. 1976;21:1097–1102. PubMed

Clarke D, Whitney H, Sutton G, Robert D. Detection and learning of floral electric fields by bumblebees. Science. 2013;340:66–69. doi: 10.1126/science.1230883. PubMed DOI

Bowker GE, Crenshaw HC. Electrostatic forces in wind-pollination—Part 1: Measurement of the electrostatic charge on pollen. Atmos. Environ. 2007;41:1587–1595. doi: 10.1016/j.atmosenv.2006.10.047. DOI

Gan-Mor S, Schwartz Y, Bechar A, Eisikowitch D, Manor G. Relevance of electrostatic forces in natural and artificial pollination. Can. Agric. Eng. 1995;37:189–194.

Colin M, Richard D, Chauzy S. Measurement of electric charges carried by bees: Evidence of biological variations. J. Bioelectr. 1991;10:17–32. doi: 10.3109/15368379109031397. DOI

Pinillos V, Cuevas J. Artificial pollination in tree crop production. Horticult. Rev. 2008;2:2.

Corbet SA, Beament J, Eisikowitch D. Are electrostatic forces involved in pollen transfer? Plant Cell Environ. 1982;5:125–129. doi: 10.1111/1365-3040.ep11571488. DOI

Inouye DW, Larson BM, Ssymank A, Kevan PG. Flies and flowers III: Ecology of foraging and pollination. J. Pollin. Ecol. 2015;16:115–133. doi: 10.26786/1920-7603(2015)15. DOI

Kanstrup J, Olesen JM. Plant-flower visitor interactions in a neotropical rain forest canopy: Community structure and generalisation level. The Scand. Assoc. Pollin. Ecol. honours knut Fægri. 2000;2:33–42.

Orford KA, Vaughan IP, Memmott J. The forgotten flies: The importance of non-syrphid Diptera as pollinators. Proc. R. Soc. B Biol. Sci. 2015;282:20142934. doi: 10.1098/rspb.2014.2934. PubMed DOI PMC

Sakurai A, Takahashi K. Flowering phenology and reproduction of the Solidago virgaurea L. complex along an elevational gradient on M t N orikura, central Japan. Plant Sp. Biol. 2017;32:270–278. doi: 10.1111/1442-1984.12153. DOI

Forup ML, Henson KS, Craze PG, Memmott J. The restoration of ecological interactions: Plant–pollinator networks on ancient and restored heathlands. J. Appl. Ecol. 2008;45:742–752. doi: 10.1111/j.1365-2664.2007.01390.x. DOI

Solomon, M. & Kendall, D. Pollination by the syrphid fly, Eristalis tenax. (1970).

Kendall D, Wilson D, Guttridge C, Anderson H. Testing Eristalis as a pollinator of covered crops. Long Ashton Res. Stn. Rep. 1971;1971:120–121.

Ohsawa R, Namai H. The effect of insect pollinators on pollination and seed setting in Brassica campestris cv. Nozawana and Brassica juncea cv Kikarashina. Jpn. J. Breed. 1987;37:453–463. doi: 10.1270/jsbbs1951.37.453. DOI

Jauker F, Wolters V. Hover flies are efficient pollinators of oilseed rape. Oecologia. 2008;156:819–823. doi: 10.1007/s00442-008-1034-x. PubMed DOI

Rader R, et al. Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop. J. Appl. Ecol. 2009;46:1080–1087. doi: 10.1111/j.1365-2664.2009.01700.x. DOI

Kalmijn AJ. The electric sense of sharks and rays. J. Exp. Biol. 1971;55:371–383. doi: 10.1242/jeb.55.2.371. PubMed DOI

Clarke D, Morley E, Robert D. The bee, the flower, and the electric field: Electric ecology and aerial electroreception. J. Comp. Physiol. A. 2017;203:737–748. doi: 10.1007/s00359-017-1176-6. PubMed DOI PMC

Greggers U, et al. Reception and learning of electric fields in bees. Proc. R. Soc. B Biol. Sci. 2013;280:20130528. doi: 10.1098/rspb.2013.0528. PubMed DOI PMC

Casas J, Dangles O. Physical ecology of fluid flow sensing in arthropods. Annu. Rev. Entomol. 2010;55:505–520. doi: 10.1146/annurev-ento-112408-085342. PubMed DOI

Tautz J, Rostás M. Honeybee buzz attenuates plant damage by caterpillars. Curr. Biol. 2008;18:R1125–R1126. doi: 10.1016/j.cub.2008.10.038. PubMed DOI

Bathellier B, Steinmann T, Barth FG, Casas J. Air motion sensing hairs of arthropods detect high frequencies at near-maximal mechanical efficiency. J. R. Soc. Interface. 2011;9:1131–1143. doi: 10.1098/rsif.2011.0690. PubMed DOI PMC

Newland PL, et al. Static electric field detection and behavioural avoidance in cockroaches. J. Exp. Biol. 2008;211:3682–3690. doi: 10.1242/jeb.019901. PubMed DOI

Sutton GP, Clarke D, Morley EL, Robert D. Mechanosensory hairs in bumblebees (Bombus terrestris) detect weak electric fields. Proc. Natl. Acad. Sci. 2016;113:7261–7265. doi: 10.1073/pnas.1601624113. PubMed DOI PMC

Wędzony M, Filek M. Changes of electric potential in pistils of Petunia hybrida Hort. and Brassica napus L. during pollination. Acta Physiol. Plantarum. 1998;20:291–297. doi: 10.1007/s11738-998-0061-x. DOI

Stout JC, Goulson D. The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Anim. Behav. 2001;62:183–189. doi: 10.1006/anbe.2001.1729. DOI

Weiss MR. Floral color change: A widespread functional convergence. Am. J. Bot. 1995;82:167–185. doi: 10.1002/j.1537-2197.1995.tb11486.x. DOI

Waser NM, Price MV. Pollinator behaviour and natural selection for flower colour in Delphinium nelsonii. Nature. 1983;302:422. doi: 10.1038/302422a0. PubMed DOI

Shimozawa T, Murakami J, Kumagai T. Sensors and Sensing in Biology and Engineering. Springer; 2003. pp. 145–157.

Khan S, Hanif H. Diversity and fauna of hoverflies (Syrphidae) in Chakwal, Pakistan. Int. J of Zool. Stud. 2016;1:22–23.

Khan SA, Hanif H. First record and redescription of Cheilosia albipila syrphid flies from Punjab, Pakistan. Int. J. Zool. Res. 2016;1:2.

Shehzad A, et al. Faunistic study of hover flies (Diptera: Syrphidae) of Pakistan. Orient. Insects. 2017;51:197–220. doi: 10.1080/00305316.2016.1274275. DOI

Nicholas S, Thyselius M, Holden M, Nordström K. Rearing and long-term maintenance of eristalis tenax hoverflies for research studies. JoVE. 2018 doi: 10.3791/57711. PubMed DOI PMC

Gilbert FS. Foraging ecology of hoverflies: Morphology of the mouthparts in relation to feeding on nectar and pollen in some urban species. Ecol. Entomol. 1981;2:2.

Nicholas S, Thyselius M, Holden M, Nordström K. Rearing and long-term maintenance of Eristalis tenax hoverflies for research studies. J. Vis. Exp. JoVE. 2018;2:2. PubMed PMC

Hogg BN, Bugg RL, Daane KM. Attractiveness of common insectary and harvestable floral resources to beneficial insects. Biol. Control. 2011;56:76–84. doi: 10.1016/j.biocontrol.2010.09.007. DOI

McGonigle DF, Jackson CW, Davidson JL. Triboelectrification of houseflies (Musca domestica L.) walking on synthetic dielectric surfaces. J. Electrostat. 2002;54:167–177. doi: 10.1016/S0304-3886(01)00177-2. DOI

Koh, K., Montgomery, C., Clarke, D., Morley, E. & Robert, D. in Journal of Physics: Conference Series. 012001 (IOP Publishing).

Rycroft M, Israelsson S, Price C. The global atmospheric electric circuit, solar activity and climate change. J. Atmos. Solar Terr. Phys. 2000;62:1563–1576. doi: 10.1016/S1364-6826(00)00112-7. DOI

Whitney HM, Dyer A, Chittka L, Rands SA, Glover BJ. The interaction of temperature and sucrose concentration on foraging preferences in bumblebees. Naturwissenschaften. 2008;95:845–850. doi: 10.1007/s00114-008-0393-9. PubMed DOI

Stanković B, Davies E. Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. FEBS Lett. 1996;390:275–279. doi: 10.1016/0014-5793(96)00672-2. PubMed DOI