Insights on the nutritional ecology of a nocturnal pollinating insect

Evan Force , Caroline Suray , Charlotte Girardin , Michel B.C. Sokolowski , Matthieu Dacher

Insect Science ›› 2026, Vol. 33 ›› Issue (3) : 1123 -1141.

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Insect Science ›› 2026, Vol. 33 ›› Issue (3) :1123 -1141. DOI: 10.1111/1744-7917.70011
ORIGINAL ARTICLE
Insights on the nutritional ecology of a nocturnal pollinating insect
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Abstract

Nutritional ecology examines the environmental effects on nutritional needs, food intake and foraging behaviors, and the use of nutrients ingested by animals. Adults of many insects’ species feed on nectars rich in sugars allowing them to match the nutritional needs necessary for reproduction. Among insects, Lepidoptera are often considered opportunistic foragers that visit a wide variety of available flowers, although with some preferences. While nutritional ecology of diurnal Lepidoptera is beginning to be explored, very little work focuses on nocturnal species because they are complicated to study in the wild. To address this, we used new laboratory approaches to study feeding behaviors (number and duration of visits to artificial flowers, food preferences associated with the texture and odors of the flowers) as well as gustatory detection by antennae (proboscis extension reflex) in the male crop pest moth Agrotis ipsilon. We showed that (i) food responsiveness is age-dependent and increases mainly with sugar quantity and marginally with sugar quality, (ii) diet quality impacts feeding behaviors in the first days of adulthood, and (iii) male moths choose their food through floral cues. Taken together, these data allow to define this species as a generalist forager with a preference for flowers with sugary nectars rich in sucrose, fructose, and glucose. Our results thus provide considerable information on the close links between food sources and nutritional ecology in this species, which is important for guiding future studies on their behavioral ecology, population dynamics, as well as for population monitoring and for regional pest management.

Keywords

Agrotis ipsilon / feeding dynamics / food preferences / food responsiveness / Lepidoptera / nectar

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Evan Force, Caroline Suray, Charlotte Girardin, Michel B.C. Sokolowski, Matthieu Dacher. Insights on the nutritional ecology of a nocturnal pollinating insect. Insect Science, 2026, 33 (3) : 1123-1141 DOI:10.1111/1744-7917.70011

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References

[1]

Aguilar, P., Bourgeois, T., Maria, A., Couzi, P., Demondion, E., Bozzolan, F. et al. (2023) Methoprene-tolerant and Krüppel homolog 1 are actors of juvenile hormone-signaling controlling the development of male sexual behavior in the moth Agrotis ipsilon. Hormones and Behavior, 150, 105330.

[2]

Aigner, P.A. and Scott, P.E. (2002) Use and pollination of a hawkmoth plant, Nicotiana attenuata, by migrant hummingbirds. The Southwestern Naturalist, 47, 1–11.

[3]

Baker, H.G. and Baker, I. (1983) Floral nectar sugar constituents in relation to pollinator type. In Handbook of Experimental Pollination Biology (eds. C.E. Jones & R.J. Little), pp. 117–141. Van Nostrand Reinhold, New York.

[4]

Bąkowski, M., Filipiak, A. and Fric, Z. (2010) Foraging behaviour and nectar use in adult Large Copper Butterflies, Lycaena dispar (Lepidoptera: Lycaenidae). Entomologica Fennnica, 21, 49–57.

[5]

Bernays, E.A. and Chapman, R.F. (1998) Phenotypic plasticity in numbers of antennal chemoreceptors in a grasshopper: effects of food. Journal of Comparative Physiology A, 183, 69–76.

[6]

Carlucci, M., Kriščiūnas, A., Li, H., Gibas, P., Koncevičius, K., Petronis, A. et al. (2019) DiscoRhythm: an easy-to-use web application and R package for discovering rhythmicity. Bioinformatics, 36, 1952–1954.

[7]

Causse, R., Buts, R., Barthes, J., Toubon, J.F. and Poitout, H.S. (1989) Utilisation du piégeage sexuel pour l’étude des migrations de Agrotis ipsilon Hufnagel (Lepidoptera: Noctuidae). Comparaison avec le piégeage lumineux. Bulletin SROP, 12, 49–50.

[8]

Chang, H., Guo, J., Fu, X., Liu, Y., Wyckhuys, K.A.G., Hou, Y. et al. (2018) Molecular-assisted pollen grain analysis reveals spatiotemporal origin of long-distance migrants of a noctuid moth. International Journal of Molecular Sciences, 19, 567.

[9]

Chapman, J.W., Reynolds, D.R. and Wilson, K. (2015) Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences. Ecology Letters, 18, 287–302.

[10]

Coates, J.M., Keaney, B., Scheele, B.C. and Cunningham, S.A. (2023) Endangered Bogong moths (Agrotis infusa) forage from local flowers after annual mass migration to alpine sites. Global Ecology and Conservation, 44, e02482.

[11]

Corbet, S. (2000) Butterfly nectaring flowers: butterfly morphology and flower form. Entomologia Experimentalis et Applicata, 96, 289–298.

[12]

Cunningham, J.P., Moore, C.J., Zalucki, M.P. and Cribb, B.W. (2006) Insect odour perception: recognition of odour components by flower foraging moths. Proceedings of the Royal Society B: Biological Sciences, 273, 2035–2040.

[13]

Cunningham, J.P., Moore, C.J., Zalucki, M.P. and West, S.A. (2004) Learning, odour preference and flower foraging in moths. Journal of Experimental Biology, 207, 87–94.

[14]

Dahanukar, A., Hallem, E.A. and Carlson, J.R. (2005) Insect chemoreception. Current Opinion in Neurobiology, 15, 423–430.

[15]

Dahanukar, A., Lei, Y.T., Kwon, J.Y. and Carlson, J.R. (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron, 56, 503–516.

[16]

Eckhardt, M., Haider, M., Dorn, S. and Müller, A. (2014) Pollen mixing in pollen generalist solitary bees: a possible strategy to complement or mitigate unfavourable pollen properties? Journal of Animal Ecology, 83, 588–597.

[17]

Force, E., Couzi, P., Dacher, M. and Debernard, S. (2023a) Diet impacts the reproductive system's maturation in the male moth Agrotis ipsilon (Noctuidae, Lepidoptera). Journal of Insect Physiology, 148, 104532.

[18]

Force, E., Sokolowski, M.B.C., Suray, C., Debernard, S., Chatterjee, A. and Dacher, M. (2023b) Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insect. Frontiers in Physiology, 14, 1304626.

[19]

Force, E., Suray, C., Dacher, M. and Debernard, S. (2024a) Effect of adult male diet on fertilization and hatching in an insect. MicroPublication Biology, https://doi.org/10.17912/micropub.biology.001074.

[20]

Force, E., Suray, C., Monsempes, C., Danis, C., Bonfils, G., Debernard, S. et al. (2024b) Diet acts on sexual behavior development in a male moth. Insect Science, https://doi.org/10.1111/1744-7917.13457.

[21]

Freeman, E.G., Wisotsky, Z. and Dahanukar, A. (2014) Detection of sweet tastants by a conserved group of insect gustatory receptors. Proceedings of the National Academy of Sciences USA, 111, 1598–1603.

[22]

Gilbert, L.E. and Singer, M.C. (1975) Butterfly ecology. Annual Review of Ecology and Systematics, 6, 365–397.

[23]

Glendinning, J.I., Jerud, A. and Reinherz, A.T. (2007) The hungry caterpillar: an analysis of how carbohydrates stimulate feeding in Manduca sexta. Journal of Experimental Biology, 210, 3054–3067.

[24]

Goulson, D., Ollerton, J. and Sluman, C. (1997) Foraging strategies in the small skipper butterfly, Thymelicus flavus: when to switch? Animal Behaviour, 53, 1009–1016.

[25]

Groot, A.T. (2014) Circadian rhythms of sexual activities in moths: a review. Frontiers in Ecology and Evolution, 2, 43.

[26]

Gu, S.H., Sun, L., Yang, R.N., Wu, K.M., Guo, Y.Y., Li, X.C. et al. (2014) Molecular characterization and differential expression of olfactory genes in the antennae of the black cutworm moth Agrotis ipsilon. PLoS ONE, 9, e103420.

[27]

He, L., Jiang, S., Chen, Y., Wyckhuys, K.A.G., Ge, S., He, W. et al. (2021) Adult nutrition affects reproduction and flight performance of the invasive fall armyworm, Spodoptera frugiperda in China. Journal of Integrative Agriculture, 20, 715–726.

[28]

He, L., Zhao, S., He, W. and Wu, K. (2022) Pollen and nectar have different effects on the development and reproduction of noctuid moths. Frontiers in Ecology and Evolution, 10, 976987.

[29]

He, Y., Feng, B., Guo, Q. and Du, Y. (2017) Age influences the olfactory profiles of the migratory oriental armyworm mythimna separate at the molecular level. BMC Genomics, 18, 32.

[30]

Hostachy, C., Couzi, P., Hanafi-Portier, M., Portemer, G., Halleguen, A., Murmu, M. et al. (2019) Responsiveness to sugar solutions in the moth Agrotis ipsilon: parameters affecting proboscis extension. Frontiers in Physiology, 10, 1423.

[31]

Jiang, X.J., Ning, C., Guo, H., Jia, Y.Y., Huang, L.Q., Qu, M.J. et al. (2015) A gustatory receptor tuned to D-fructose in antennal sensilla chaetica of Helicoverpa armigera. Insect Biochemistry and Molecular Biology, 60, 39–46.

[32]

Jürgens, A. (2004) Nectar sugar composition and floral scent compounds of diurnal and nocturnal Conophytum species (Aizoaceae). South African Journal of Botany, 70, 191–205.

[33]

Kim, W., Gilet, T. and Bush, J.W.M. (2011) Optimal concentrations in nectar feeding. Proceedings of the National Academy of Sciences USA, 108, 16618–16621.

[34]

Kim, Y. and Hong, Y. (2015) Regulation of hemolymph trehalose level by an insulin-like peptide through diel feeding rhythm of the beet armyworm, Spodoptera exigua. Peptides, 68, 91–98.

[35]

Krenn, H.W. (2010) Feeding mechanisms of adult Lepidoptera: structure, function, and evolution of the mouthparts. Annual Review of Entomology, 55, 307–327.

[36]

Lazzari, C.R. and Insausti, T.C. (2008) Circadian rhythms in insects. In Comparative Aspects of Circadian Rhythms (eds. M.L. Fanjul-Moles & R.A. Roblero). Transworld Research Network, Kerala, India.

[37]

Lee, J.C. and Heimpel, G.E. (2008) Effect of floral nectar, water, and feeding frequency on Cotesia glomerata longevity. BioControl, 53, 289–294.

[38]

Liu, K., Zhu, P., Lü, Z., Chen, G., Zhang, J., Lü, Y. et al. (2017) Effects of sesame nectar on longevity and fecundity of seven Lepidoptera and survival of four parasitoid species commonly found in agricultural ecosystems. Journal of Integrative Agriculture, 16, 2534–2546.

[39]

Liu, Y., Fu, X., Mao, L., Xing, Z. and Wu, K. (2016) Host plants identification for adult Agrotis ipsilon, a long-distance migratory insect. International Journal of Molecular Sciences, 17, 851.

[40]

MacArthur, R.H. and Pianka, E.R. (1966) On optimal use of a patchy environment. The American Naturalist, 100, 603–609.

[41]

MacGregor, C.J., Pocock, M.J.O., Fox, R. and Evans, D.M. (2015) Pollination by nocturnal Lepidoptera, and the effects of light pollution: a review. Ecological Entomology, 40, 187–198.

[42]

Machovsky-Capuska, G.E., Miller, M.G.R., Silva, F.R.O., Amiot, C., Stockin, K.A., Senior, A.M. et al. (2018) The nutritional nexus: linking niche, habitat variability and prey composition in a generalist marine predator. Journal of Animal Ecology, 87, 1286–1298.

[43]

Mayack, C., Carmichael, K., Phalen, N., Khan, Z., Hirche, F., Stangl, G.I. et al. (2020) Gas chromatography-mass spectrometry as a preferred method for quantification of insect hemolymph sugars. Journal of Insect Physiology, 127, 104115.

[44]

Morinaga, S., Nagata, K., Ihara, S., Yumita, T., Niimura, Y., Sato, K. et al. (2022) Structural model for ligand binding and channel opening of an insect gustatory receptor. Journal of Biological Chemisty, 298, 102573.

[45]

Norberg, R.Å. (2021) To minimize foraging time, use high-efficiency, energy-expensive search and capture methods when food is abundant but low-efficiency, low-cost methods during food shortages. Ecology and Evolution, 11, 16537–16546.

[46]

Pacini, E., Nepi, M. and Vesprini, J.L. (2003) Nectar biodiversity: a short review. Plant Systematics and Evolution, 238, 7–21.

[47]

Popescu, A., Couton, L., Almaas, T.J., Rospars, J.P., Wright, G.A., Marion-Poll, F. et al. (2013) Function and central projections of gustatory receptor neurons on the antenna of the noctuid moth Spodoptera littoralis. Journal of Comparative Physiology A, 199, 403–416.

[48]

R Core Team (2021) R: the R project for statistical computing [WWW Document]. https://www.r-project.org/ (accessed 2.16.22).

[49]

Raguso, R.A. and Willis, M.A. (2005) Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths, Manduca sexta. Animal Behaviour, 69, 407–418.

[50]

Raubenheimer, D., Simpson, S.J. and Mayntz, D. (2009) Nutrition, ecology and nutritional ecology: toward an integrated framework. Functional Ecology, 23, 4–16.

[51]

Riffell, J.A. and Alarcón, R. (2013) Multimodal floral signals and moth foraging decisions. PLoS ONE, 8, e72809.

[52]

Rouyar, A., Deisig, N., Dupuy, F., Limousin, D., Wycke, M.A., Renou, M. et al. (2015) Unexpected plant odor responses in a moth pheromone system. Frontiers in Physiology, 6, 148.

[53]

Rowe, C.E., Figueira, W., Raubenheimer, D., Solon-Biet, S.M. and Machovsky-Capuska, G.E. (2018) Effects of temperature on macronutrient selection, metabolic and swimming performance of the Indo-Pacific Damselfish (Abudefduf vaigiensis). Marine Biology, 165, 178.

[54]

Roy, R., Schmitt, A.J., Thomas, J.B. and Carter, C.J. (2017) Review: nectar biology: from molecules to ecosystems. Plant Science, 262, 148–164.

[55]

Rusterholz, H.P. and Erhardt, A.N. (2000) Can nectar properties explain sex-specific flower preferences in the Adonis Blue butterfly Lysandra bellargus? Ecological Entomology, 25, 81–90.

[56]

Sasaki, K. and Asaoka, K. (2006) Swallowing motor pattern triggered and modified by sucrose stimulation in the larvae of the silkworm, Bombyx mori. Journal of Insect Physiology, 52, 528–537.

[57]

Saunders, D.C. (2002) Circadian rhythms of activity in individual insects. In Insect Clocks. 1st edn. (eds. C.G.H. Steel, X. Vafopoulou & R.D. Lewis). Elsevier, Amsterdam, the Netherlands.

[58]

Scheiner, R., Abramson, C.I., Brodschneider, R., Crailsheim, K., Farina, W.M., Fuchs, S. et al. (2013) Standard methods for behavioural studies of Apis mellifera. Journal of Apicultural Research, 52, 1–58.

[59]

Shafir, S. and Yehonatan, L. (2014) Comparative evaluations of reward dimensions in honey bees: evidence from two-alternative forced choice proboscis-extension conditioning. Animal Cognition, 17, 633–644.

[60]

Sherry, D.F. and Strang, C.G. (2015) Contrasting styles in cognition and behaviour in bumblebees and honeybees. Behavioural Processes, 117, 59–69.

[61]

Slone, J., Daniels, J. and Amrein, H. (2007) Sugar receptors in Drosophila. Current Biology, 17, 1809–1816.

[62]

Staddon, J.E.R. and Cerutti, D.T. (2003) Operant conditioning. Annual Review Psychology, 54, 115–144.

[63]

Stöckl, A.L. and Kelber, A. (2019) Fuelling on the wing: sensory ecology of hawkmoth foraging. Journal of Comparative Physiology A, 205, 399–413.

[64]

Suszczynska, A., Kaniewska, M.M., Bebas, P., Giebultowicz, J.M. and Kotwica-Rolinska, J. (2017) Circadian regulation of caterpillar feeding and growth. Journal of Insect Physiology, 101, 113–122.

[65]

Tang, Q.B., Zhan, H., Cao, H., Berg, B.G., Yan, F.M. and Zhao, X.C. (2014) Central projections of gustatory receptor neurons in the medial and the lateral sensilla styloconica of Helicoverpa armigera larvae. PLoS ONE, 9, e95401.

[66]

Tiedge, K. and Lohaus, G. (2017) Nectar sugars and amino acids in day-and night-flowering Nicotiana species are more strongly shaped by pollinators’ preferences than organic acids and inorganic ions. PLoS ONE, 12, e0176865.

[67]

Wester, P. and Lunau, K. (2017) Plant-pollinator communication. In Advances in Botanical Research (ed. G. Becard), pp. 225–257. Academic Press, New York.

[68]

Whitney, H.M., Chittka, L., Bruce, T.J.A. and Glover, B.J. (2009) Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Current Biology, 19, 948–953.

[69]

Zhang, J., Li, S., Li, W., Chen, Z., Guo, H., Liu, J. et al. (2021) Circadian regulation of night feeding and daytime detoxification in a formidable Asian pest Spodoptera litura. Communication Biology, 4, 286.

[70]

Zhang, S.S., Wang, P.C., Ning, C., Yang, K., Li, G.C., Cao, L.L. et al. (2023) Sucrose taste receptors differ in larval and adult stages of a moth. eLife, 12, RP91711.

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