Exposure to sublethal concentration of flupyradifurone alters sexual behavior and cuticular hydrocarbon profile in Heriades truncorum, an oligolectic solitary bee

Abstract

The aboveground oligolectic bee, Heriades truncorum, is a particularly good model for studying the impact of pesticides on sexual communication, since some aspects of its mating behavior have previously been described. We have tested (1) the interference of the pesticide flupyradifurone on male precopulatory behavior and male mating partner preferences, (2) the way that the pesticide interferes in male quality assessment by the female, and (3) the effects of the pesticide on the chemical compounds in the female cuticle. We exposed bees of both sexes to a sublethal concentration of flupyradifurone. Various behaviors were registered in a mating arena with two females (one unexposed and one exposed) and one male (either unexposed or exposed). Unexposed males were quicker to attempt to mate. Treatment also impacted precopulatory behavior and male quality assessment by females. Males approached unexposed females more quickly than insecticide-exposed ones. Females exposed to insecticide produced lower amounts of some cuticular hydrocarbons (sex pheromone candidates) and appeared less choosy than unexposed females. Our findings suggest that insecticide exposure affects sexual communication, playing a role both in male preference and in male quality assessment by the female.

Keywords

courtship display / female choice / flupyradifurone / male partner preference / sex communication / sublethal effects

References

[1] Adams,K.L., Sawadogo, S.P., Nignan,C., Niang,A., Paton,D.G., Robert Shaw,W. et al. (2021) Cuticular hydrocarbons are associated with mating success and insecticide resistance in malaria vectors. Communications Biology, 4, 911.

[2] Al Naggar,Y. and Baer, B. (2019) Consequences of a short time exposure to a sublethal dose of fupyradifurone (Sivanto) pesticide early in life on survival and immunity in the honeybee (Apis mellifera). Scientific Reports, 9, 19753.

[3] Ayasse,M., Paxton, R.J. and Tengö,J. (2001) Mating behavior and chemical communication in the order Hymenoptera. Annual Review of Entomology, 46, 31–78.

[4] Biesmeijer,J.C., Roberts, S.P.M., Reemer,M., Ohlemüller,R., Edwards, M., Peeters,T. et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313, 351–354.

[5] Boff,S. (2022) Mating behaviour of the large–head resin bee Heriades truncorum (Megachilidae: Osminii) suggests female plastic strategy in selection of a mating partner and male quality assessment. Apidologie, 53, 9.

[6] Boff,S., Conrad, T., Raizer,J., Wehrhahn,M., Bayer,M., Friedel,A. et al. (2022) Low toxicity crop fungicide (fenbuconazole) impacts reproductive male quality signals leading to a reduction of mating success in a wild solitary bee. Journal of Applied Ecology, 59, 1596–1607.

[7] Bonduriansky,R. (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biological Reviews, 76, 305–339.

[8] Böröczky,K., Crook, D.J., Jones,T.H., Kenny,J.C., Zylstra, K.E., Mastro,V.C. et al. (2009) Monoalkenes as contact sex pheromone components of the woodwasp Sirex noctilio. Journal of Chemical Ecology, 35, 1202–1211.

[9] Brooks,T.M., Mittermeier, R.A., Mittermeier,C.G., Da Fonseca,G.A., Rylands, A.B., Konstant,W.R. et al. (2002) Habitatloss and extinction in the hotspots of biodiversity. Conservation Biology, 16, 909–923.

[10] Buckner,J.S., Pitts-Singer, T.L., Guédot,C., Hagen,M.M., Fatland, C.L. and Kemp,W.P. (2009) Cuticular lipids of female solitary bees, Osmia lignaria Say and Megachile rotundata (F.) (Hymenoptera: Megachilidae). Comparative Biochemistry and Physiology-B Biochemistry and Molecular Biology, 153, 200–205.

[11] Candolin,U., Salesto, T. and Evers,M. (2007) Changed environmental conditions weaken sexual selection in sticklebacks. Journal of Evolutionary Biology, 20, 233–239.

[12] Carleton,J. (2014) Environmental fate and ecological risk assessment for foliar, soil drench, and seed treatment uses of the new insecticide flupyradifurone (BYI 02960). Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

[13] Conrad,T., Stöcker, C. and Ayasse,M. (2017) The effect of temperature on male mating signals and female choice in the red mason bee, Osmia bicornis (L.). Ecology and Evolution, 7, 8966–8975.

[14] Cuervo,M., Rakosy, D., Martel,C., Schulz,S. and Ayasse, M. (2017) Sexual deception in the Eucera-pollinated Ophrys leochroma: a chemical intermediate between wasp- and Andrena-pollinated species. Journal of Chemical Ecology, 43, 469–479.

[15] De Almeida Correa,M.L.M. (1980) Contribution a l’étude de la biologie d’Heriades truncorum L. (Hymenoptera, Apoidea, Megachilidae). Apidologie, 11, 309–339.

[16] Fletcher,R.J., Didham, R., Banks-Leite,C., Barlow,J., Ewers,R., Rosindell,J. et al. (2018) Is habitat fragmentation good for biodiversity? Biological Conservation, 226, 9–15.

[17] Foley,J.A., Defries, R., Asner,G.P., Barford,C., Bonan,G., Carpenter,S.R. et al. (2005) Global consequences of land use. Science, 309, 570–574.

[18] Ganuza,C., Ayasse, M. and Boff,S. (2022) Chemical and mechanical signals trigger courtship in the wild large-headed resin bee Heriades truncorum. Journal of Insect Behavior, 35, 160–170.

[19] Gefen,E. and Gibbs, A.G. (2009) Interactions between environmental stress and male mating success may enhance evolutionary divergence of stress-resistant Drosophila populations. Evolution; International Journal of Organic Evolution, 63, 1653–1659.

[20] Giannini,T.C., Boff,S., Cordeiro,G.D., Cartolano,E.A., Veiga,A.K., Imperatriz-Fonseca,V.L. et al. (2015) Crop pollinators in Brazil: a review of reported interactions. Apidologie, 46, 209–223.

[21] Godfray,H.C.J., Blacquière, T., Field,L.M., Hails,R.S., Petrokofsky, G., Potts,S.G. et al. (2015) A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B: Biological Sciences, 281, 20140558.

[22] Goulson,D., Nicholls, E., Botías,C. and Rotheray,E.L. (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347, 1255957.

[23] Grillet,M., Dartevelle, L. and Ferveur,J.F. (2006) A Drosophila male pheromone affects female sexual receptivity. Proceedings of the Royal Society B: Biological Sciences, 273, 315–323.

[24] Hartig,F. (2020) DHARMa: residual diagnostics for hierarchical (Multi-Level/Mixed) regression models. R package version 0.3.3.0. Available from: https://florianhartig.github.io/DHARMa/

[25] Harwood,G.P., Prayugo, V. and Dolezal,A.G. (2022) Butenolide insecticide flupyradifurone affects honey bee worker antiviral immunity and survival. Frontiers in Insect Science, 2, 907555.

[26] Hesselbach,H. and Scheiner, R. (2018) Effects of the novel pesticide flupyradifurone (Sivanto) on honeybee taste and cognition. Scientific Reports, 8, 4954.

[27] Hesselbach,H. and Scheiner, R. (2019) The novel pesticide flupyradifurone (Sivanto) affects honeybee motor abilities. Ecotoxicology (London, England), 28, 354–366.

[28] Hesselbach,H., Seeger, J., Schilcher,F., Ankenbrand,M. and Scheiner, R. (2020) Chronic exposure to the pesticide flupyradifurone can lead to premature onset of foraging in honeybees Apis mellifera. Journal of Applied Ecology, 57, 609–618.

[29] Hofmann,M., Fleischmann, A. and Renner,S. (2020) Foraging distances in six species of solitary bees with body lengths of 6 to 15 mm, inferred from individual tagging, suggest 150 m-rule-of-thumb for flower strip distances. Journal of Hymenoptera Research, 77, 105–117.

[30] Jiang,N., Chang,H., Weißflog,J., Eberl,F., Veit,D., Weniger,K. et al. (2023) Ozone exposure disrupts insect sexual communication. Nature Communications, 14, 1186.

[31] Kassambara,A. and Kosinski, M.B.P. (2020) Survminer: drawing survival curves using “ggplot2”. R package version 0.4.8.

[32] Kennedy,C.M., Lonsdorf, E., Neel,M.C., Williams,N.M., Ricketts, T.H., Winfree,R. et al. (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecology Letters, 16, 584–599.

[33] Klein,A.M., Vaissière, B.E., Cane,J.H., Steffan-Dewenter,I., Cunningham, S.A., Kremen,C. et al. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274, 303–313.

[34] Knauer,A.C., Alaux,C., Allan,M.J., Dean, R.R., Dievart,V., Glauser,G. et al. (2022) Nutritional stress exacerbates impact of a novel insecticide on solitary bees’ behaviour, reproduction and survival. Proceedings of the Royal Society B: Biological Sciences, 289, 20221013.

[35] Konzmann,S., Kluth,M., Karadana,D. and Lunau, K. (2020) Pollinator effectiveness of a specialist bee exploiting a generalist plant—tracking pollen transfer by Heriades truncorum with quantum dots. Apidologie, 51, 201–211.

[36] Kuppler,J., Neumüller, U., Mayr,A.V., Hopfenmüller,S., Weiss, K., Prosi,R. et al. (2023) Favourite plants of wild bees. Agriculture, Ecosystems and Environment, 342, 108266.

[37] McAfee,A., Metz,B.N., Milone,J.P., Foster, L.J. and Tarpy,D.R. (2022) Drone honey bees are disproportionately sensitive to abiotic stressors despite expressing high levels of stress response proteins. Communications Biology, 5, 141.

[38] Müller,T., Prosche, A. and Müller,C. (2017) Sublethal insecticide exposure affects reproduction, chemical phenotype as well as offspring development and antennae symmetry of a leaf beetle. Environmental Pollution, 230, 709–717.

[39] Paxton,R.J. (2005) Male mating behaviour and mating systems of bees: an overview. Apidologie, 36, 145–156.

[40] Peters,B., Keller, A. and Leonhardt,S.D. (2022) Diets maintained in a changing world: Does land-use intensification alter wild bee communities by selecting for flexible generalists? Ecology and Evolution, 12, e8919.

[41] Pilakouta,N. and Ålund, M. (2021) Sexual selection and environmental change: what do we know and what comes next? Current Zoology, 67, 293–298.

[42] Polerstock,A.R., Eigenbrode, S.D. and Klowden,M.J. (2002) Mating alters the cuticular hydrocarbons of female Anopheles gambiae sensu stricto and Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology, 39, 545–552.

[43] Potts,S.G., Biesmeijer, J.C., Kremen,C., Neumann,P., Schweiger, O. and Kunin,W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution, 25, 345–353.

[44] R Core Team. (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: https://www.r-project.org/.

[45] Raven,P.H. and Wagner, D.L. (2021) Agricultural intensification and climate change are rapidly decreasing insect biodiversity. Proceedings of the National Academy of Sciences USA, 118, e2002548117.

[46] Rundlöf,M., Andersson, G.K.S., Bommarco,R., Fries,I., Hederström, V., Herbertsson,L. et al. (2015) Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature, 521, 77–80.

[47] Sandrock,C., Tanadini, L.G., Pettis,J.S., Biesmeijer,J.C., Potts,S.G. and Neumann,P. (2014) Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agricultural and Forest Entomology, 16, 119–128.

[48] Schiestl,F.P., Ayasse, M., Paulus,H.F., Löfstedt,C., Hansson, B.S., Ibarra,F. et al. (1999) Orchid pollination by sexual swindle. Nature, 399, 421.

[49] Sgolastra,F., Medrzycki, P., Bortolotti,L., Maini,S., Porrini, C., Simon-Delso,N. and Bosch,J. (2020) Bees and pesticide regulation: Lessons from the neonicotinoid experience. Biological Conservation, 241, 108356.

[50] Siviter,H., Bailes, E.J., Martin,C.D., Oliver,T.R., Koricheva, J., Leadbeater,E. et al. (2021) Agrochemicals interact synergistically to increase bee mortality. Nature, 596, 389–392.

[51] Siviter,H. and Muth, F. (2020) Do novel insecticides pose a threat to beneficial insects? Proceedings of the Royal Society B: Biological Sciences, 287, 20201265.

[52] Smith,B.H. and Ayasse, M. (1987) Kin-based male mating preferences in two species of halictine bee. Behavioral Ecology and Sociobiology, 20, 313–318.

[53] Straub,L., Minnameyer, A., Camenzind,D., Kalbermatten,I., Tosi,S., Van Oystaeyen,A. et al. (2022) Thiamethoxam as an inadvertent anti-aphrodisiac in male bees. Toxicology Reports, 9, 36–45.

[54] Stuligross,C. and Williams, N.M. (2020) Pesticide and resource stressors additively impair wild bee reproduction: Stressors additively impair wild bees. Proceedings of the Royal Society B: Biological Sciences, 287, 20201390.

[55] Tabebordbar,F., Shishehbor, P., Ziaee,M. and Sohrabi,F. (2020) Lethal and sublethal effects of two new insecticides spirotetramat and flupyradifurone in comparison to conventional insecticide deltamethrin on Trichogramma evanescens (Hymenoptera: Trichogrammatidae). Journal of Asia-Pacific Entomology, 23, 1114–1119.

[56] Tan,K., Wang,C., Dong,S., Li, X. and Nieh,J.C. (2017) The pesticide flupyradifurone impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Scientific Reports, 7, 17772.

[57] Tappert,L., Pokorny, T., Hofferberth,J. and Ruther,J. (2017) Sublethal doses of imidacloprid disrupt sexual communication and host finding in a parasitoid wasp. Scientific Reports, 7, 42756.

[58] Therneau,T. (2020) A Package for Survival Analysis in R. R package version 3.2-3.

[59] Tong,L., Nieh,J.C. and Tosi,S. (2019) Combined nutritional stress and a new systemic pesticide (flupyradifurone, Sivanto^®) reduce bee survival, food consumption, flight success, and thermoregulation. Chemosphere, 237, 124408.

[60] Tosi,S. and Nieh, J.C. (2019) Lethal and sublethal synergistic effects of a new systemic pesticide, flupyradifurone (Sivanto), on honeybees. Proceedings of the Royal Society B: Biological Sciences, 286, 20190433.

[61] Tosi,S., Nieh,J.C., Brandt,A., Colli, M., Fourrier,J., Giffard,H. et al. (2021) Long-term field-realistic exposure to a next-generation pesticide, flupyradifurone, impairs honey bee behaviour and survival. Communications Biology, 4, 805.

[62] Vereecken,N.J., Mant,J. and Schiestl,F.P. (2007) Population differentiation in female sex pheromone and male preferences in a solitary bee. Behavioral Ecology and Sociobiology, 61, 811–821.

[63] Wang,D., Lü, L. and He,Y. (2018) Effects of insecticides on sex pheromone communication and mating behavior in Trichogramma chilonis. Journal of Pest Science, 91, 65–78.

[64] Willis Chan,D.S. and Raine, N.E. (2021) Population decline in a ground-nesting solitary squash bee (Eucera pruinosa) following exposure to a neonicotinoid insecticide treated crop (Cucurbita pepo). Scientific Reports, 11, 4241.

[65] Wood,T.J., Michez, D., Paxton,R.J., Drossart,M., Neumann, P., Gérard,M. et al. (2020) Managed honey bees as a radar for wild bee decline? Apidologie, 51, 1100–1116.

[66] Woodcock,B.A., Bullock, J.M., Shore,R.F., Heard,M.S., Pereira, M.G., Redhead,J. et al. (2017) Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science, 356, 1393–1395.

[67] Zhang,Q., Wang,Q., Zhai,Y., Zheng, H. and Wang,X. (2022) Impacts of imidacloprid and flupyradifurone insecticides on the gut microbiota of Bombus terrestris. Agriculture, 12, 389.

[68] Zioga,E., White,B. and Stout,J.C. (2023) Pesticide mixtures detected in crop and non-target wild plant pollen and nectar. Science of the Total Environment, 879, 162971.

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