Winter fruit contribution to the performance of the invasive fruit fly Drosophila suzukii under different thermal regimes

Jordy Larges , Gwenaëlle Deconninck , Romain Ulmer , Vincent Foray , Nathalie Le Bris , Marion Chorin , Hervé Colinet , Olivier Chabrerie , Patrice Eslin , Aude Couty

Insect Science ›› 2026, Vol. 33 ›› Issue (1) : 377 -395.

PDF (1328KB)
Insect Science ›› 2026, Vol. 33 ›› Issue (1) :377 -395. DOI: 10.1111/1744-7917.13494
ORIGINAL ARTICLE
Winter fruit contribution to the performance of the invasive fruit fly Drosophila suzukii under different thermal regimes
Author information +
History +
PDF (1328KB)

Abstract

Polyphagous insect species develop using multiple host plants. Often considered beneficial, polyphagy can also be costly as host nutritional quality may vary. Drosophila suzukii (Matsumura) is an invasive species that can develop on numerous fruit species over the annual cycle. Here, we assessed the contribution of winter-available fruit to the development of seasonal populations of D. suzukii, under fluctuating late winter/early spring temperature regimes. We infested an artificial diet and three suitable fruit species available in winter/early spring (Aucuba japonica, Elaeagnus ×submacrophylla, Viscum album) with D. suzukii larvae under three temperature regimes: constant 20 °C, fluctuating controlled regime of 8–15 °C (12 h of light at 8 °C and 12 h of dark at 15 °C), and uncontrolled outdoor regime during spring. As expected, fly performance was impaired by early spring-like environmental conditions, whatever the development diet, and the winter fruit were suboptimal diets compared to the artificial diet, whatever the thermal regime. However, under cold fluctuating temperature regimes, the ranking of fruit supporting the best performance changed, highlighting the occurrence of physiological trade-offs. Winter-acclimated females preferentially oviposited in A. japonica and/or E. ×submacrophylla, whatever the thermal regime, which does not support the preference–performance hypothesis. This finding is also discussed in the context of D. suzukii management strategies.

Keywords

life history traits / overwintering / polyphagy / preference-performance hypothesis / thermal fluctuations / trade-off

Cite this article

Download citation ▾
Jordy Larges, Gwenaëlle Deconninck, Romain Ulmer, Vincent Foray, Nathalie Le Bris, Marion Chorin, Hervé Colinet, Olivier Chabrerie, Patrice Eslin, Aude Couty. Winter fruit contribution to the performance of the invasive fruit fly Drosophila suzukii under different thermal regimes. Insect Science, 2026, 33 (1) : 377-395 DOI:10.1111/1744-7917.13494

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Abdalla, T.E. (2019) Some wild Elaeagnus species: overview, description, biochemistry, and utilization. In Wild Fruits: Composition, Nutritional Value and Products (ed. A.A. Mariod), pp. 507–522. Springer, Cham.

[2]

Abe, T. (2001) Flowering phenology, display size, and fruit set in an understory dioecious shrub, Aucuba japonica (Cornaceae). American Journal of Botany, 88, 455–461.

[3]

Angilletta, M.J., Steury, T.D. and Sears, M.W. (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integrative and Comparative Biology, 44, 498–509.

[4]

Aouari, I., Barech, G. and Khaldi, M. (2022) First record of the agricultural pest Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) in Algeria. EPPO Bulletin, 52, 471–478.

[5]

Arnó, J., Solà, M., Riudavets, J. and Gabarra, R. (2016) Population dynamics, non-crop hosts, and fruit susceptibility of Drosophila suzukii in Northeast Spain. Journal of Pest Science, 89, 713–723.

[6]

Attisano, A., Moore, A.J. and Moore, P.J. (2012) Reproduction-longevity trade-offs reflect diet, not adaptation. Journal of Evolutionary Biology, 25, 873–880.

[7]

Bale, J.S. and Hayward, S.A.L. (2010) Insect overwintering in a changing climate. Journal of Experimental Biology, 213, 980–994.

[8]

Ballard, J.W.O., Melvin, R.G. and Simpson, S.J. (2008) Starvation resistance is positively correlated with body lipid proportion in five wild caught Drosophila simulans populations. Journal of Insect Physiology, 54, 1371–1376.

[9]

Begon, M. (1975) Population densities in Drosophila obscura Fallén and D. subobscura Collin to naturally-occuring fruits. Ecological Entomology, 3, 1–12.

[10]

Berger, D., Walters, R. and Gotthard, K. (2008) What limits insect fecundity? Body size-and temperature-dependent egg maturation and oviposition in a butterfly. Functional Ecology, 22, 523–529.

[11]

Biere, A., Marak, H.B. and Van Damme, J.M.M. (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia, 140, 430–441.

[12]

Blacher, P., Huggins, T.J. and Bourke, A.F.G. (2017) Evolution of ageing, costs of reproduction and the fecundity—longevity trade-off in eusocial insects. Proceedings of the Royal Society B: Biological Sciences, 284, 20170380.

[13]

Boggs, C.L. and Ross, C.L. (1993) The effect of adult food limitation on life history traits in Speyeria mormonia (Lepidoptera: Nymphalidae). Ecology, 74, 433–441.

[14]

Brankatschk, M., Gutmann, T., Knittelfelder, O., Palladini, A., Prince, E., Grzybek, M. et al. (2018) A temperature-dependent switch in feeding preference improves Drosophila development and survival in the cold. Developmental Cell, 46, 781–793.

[15]

Bühlmann, I. and Gossner, M.M. (2022) Invasive Drosophila suzukii outnumbers native controphics and causes substantial damage to fruits of forest plants. NeoBiota, 77, 39–77.

[16]

Burrack, H.J., Fernandez, G.E., Spivey, T. and Kraus, D.A. (2013) Variation in selection and utilization of host crops in the field and laboratory by Drosophila suzukii Matsumara (Diptera: Drosophilidae), an invasive frugivore. Pest Management Science, 69, 1173–1180.

[17]

Butterworth, N.J., Benbow, M.E. and Barton, P.S. (2023) The ephemeral resource patch concept. Biological Reviews, 98, 697–726.

[18]

Cha, D.H., Adams, T., Rogg, H. and Landolt, P.J. (2012) Identification and field evaluation of fermentation volatiles from wine and vinegar that mediate attraction of spotted wing Drosophila, Drosophila suzukii. Journal of Chemical Ecology, 38, 1419–1431.

[19]

Chakraborty, A., Walter, G.M., Monro, K., Alves, A.N., Mirth, C.K. and Sgrò, C.M. (2023) Within-population variation in body size plasticity in response to combined nutritional and thermal stress is partially independent from variation in development time. Journal of Evolutionary Biology, 36, 264–279.

[20]

Clavé, C., Sugio, A., Morlière, S., Pincebourde, S., Simon, J.C. and Foray, V. (2022) Physiological costs of facultative endosymbionts in aphids assessed from energy metabolism. Functional Ecology, 36, 2580–2592.

[21]

Clemente, M., Fusco, G., Tonina, L. and Giomi, F. (2018) Temperature-induced phenotypic plasticity in the ovipositor of the invasive species Drosophila suzukii. Journal of Thermal Biology, 75, 62–68.

[22]

Clusella Trullas, S., Van Wyk, J.H. and Spotila, J.R. (2007) Thermal melanism in ectotherms. Journal of Thermal Biology, 32, 235–245.

[23]

Colinet, H. and Kustre, A. (2024) The apparent seasonal biphenism in Drosophila suzukii stems in reality from continuous reaction norm. Pest Management Science, https://doi.org/10.1002/ps.8452.

[24]

Danks, H.V. (1978) Modes of seasonal adaptation in the insects: I. winter survival. The Canadian Entomologist, 110, 1167–1205.

[25]

David, J.R., Gibert, P., Gravot, E., Petavy, G., Morin, J.P., Karan, D. et al. (1997) Phenotypic plasticity and developmental temperature in Drosophila: analysis and significance of reaction norms of morphological traits. Journal of Thermal Biology, 22, 441–451.

[26]

De Loof, A. (2011) Longevity and aging in insects: Is reproduction costly; cheap; beneficial or irrelevant? A critical evaluation of the “trade-off” concept. Journal of Insect Physiology, 57, 1–11.

[27]

Deconninck, G., Boulembert, M., Eslin, P., Couty, A., Bonis, A., Borowiec, N. et al. (2024a) Environmental factors driving infestations of a keystone winter fruit by an invasive and a native fruit fly. Arthropod-Plant Interactions, 18, 867–880

[28]

Deconninck, G., Boulembert, M., Eslin, P., Couty, A., Dubois, F., Gallet-Moron, E. et al. (2024b) Fallen fruit: a backup resource during winter shaping fruit fly communities. Agricultural and Forest Entomology, 26, 232–248.

[29]

Deconninck, G., Boulembert, M., Eslin, P., Couty, A., Dubois, F., Gallet-Moron, E. et al. (2024c) Winter fleshy-fruited plants are the catalysts for spring populations of an invasive fruit fly. Ecological Entomology, https://doi.org/10.1111/een.13397.

[30]

Denlinger, D.L. and Lee, J., R.E. (2010) Low Temperature Biology of Insects. Cambridge University Press, Cambridge.

[31]

Dettler, M.A., Barrientos, G.N., Ansa, M.A., Martínez, E., Vazquez, F.A., Santadino, M.V. et al. (2024) A performance index as a measure of the host suitability to Drosophila suzukii Matsumura (Diptera: Drosophilidae). Neotropical Entomology, 53, 29–37.

[32]

Edgar, B.A. (2006) How flies get their size: genetics meets physiology. Nature Reviews Genetics, 7, 907–916.

[33]

Edwards, D. (2017) A new name for an Elaeagnus hybrid. The Plantsman, 16, 222–223.

[34]

Enriquez, T., Renault, D., Charrier, M. and Colinet, H. (2018) Cold acclimation favors metabolic stability in Drosophila suzukii. Frontiers in Physiology, 9, 1506.

[35]

Ewing, A.W. (1964) The influence of wing area on the courtship behaviour of Drosophila melanogaster. Animal Behaviour, 12, 316–320.

[36]

Folwarczny, M., Otterbring, T., Sigurdsson, V. and Gasiorowska, A. (2022) Seasonal cues to food scarcity and calorie cravings: winter cues elicit preferences for energy-dense foods. Food Quality and Preference, 96, 104379.

[37]

Foray, V., Pelisson, P.F., Bel-Venner, M.C., Desouhant, E., Venner, S., Menu, F. et al. (2012) A handbook for uncovering the complete energetic budget in insects: the van Handel's method (1985) revisited. Physiological Entomology, 37, 295–302.

[38]

Fragnière, A.L., Bacher, S. and Kehrli, P. (2024) Identifying candidate host plants for trap cropping against Drosophila suzukii in vineyards. Journal of Pest Science, 97, 1975–1991.

[39]

Fraimout, A., Jacquemart, P., Villarroel, B., Aponte, D.J., Decamps, T., Herrel, A. et al. (2018) Phenotypic plasticity of Drosophila suzukii wing to developmental temperature: implications for flight. Journal of Experimental Biology, 221, jeb166868.

[40]

Frazier, M.R., Harrison, J.F., Kirkton, S.D. and Roberts, S.P. (2008) Cold rearing improves cold-flight performance in Drosophila via changes in wing morphology. Journal of Experimental Biology, 211, 2116–2122.

[41]

García-Robledo, C. and Horvitz, C.C. (2012) Parent-offspring conflicts, “optimal bad motherhood” and the “mother knows best” principles in insect herbivores colonizing novel host plants. Ecology and Evolution, 2, 1446–1457.

[42]

Gilchrist, G.W., Huey, R.B. and Serra, L. (2001) Rapid evolution of wing size clines in Drosophila subobscura. Genetica, 1, 273–286.

[43]

Gill, H.K., Goyal, G. and Chahil, G. (2017) Insect diapause: a review. Journal of Agricultural Science and Technology A, 7, 454–473.

[44]

Giron, D. and Casas, J. (2003) Mothers reduce egg provisioning with age. Ecology Letters, 6, 273–277.

[45]

Grandison, R.C., Piper, M.D.W. and Partridge, L. (2009) Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature, 462, 1061–1064.

[46]

Grassi, A., Gottardello, A., Dalton, D.T., Tait, G., Rendon, D., Ioriatti, C. et al. (2018) Seasonal reproductive biology of Drosophila suzukii (Diptera : Drosophilidae) in temperate climates. Environmental Entomology, 47, 166–174.

[47]

Greenberg, C.H. and Walter, S.T. (2010) Fleshy fruit removal and nutritional composition of winter-fruiting plants: a comparison of non-native invasive and native species. Natural Areas Journal, 30, 312–321.

[48]

Gripenberg, S., Mayhew, P.J., Parnell, M. and Roslin, T. (2010) A meta-analysis of preference-performance relationships in phytophagous insects. Ecology Letters, 13, 383–393.

[49]

Henry, Y., Overgaard, J. and Colinet, H. (2020) Dietary nutrient balance shapes phenotypic traits of Drosophila melanogaster in interaction with gut microbiota. Comparative Biochemistry and Physiology Part A : Molecular and Integrative Physiology, 241, 110626.

[50]

Herrera, C.M. (1982) Defence of ripe fruit from pests: its significance in relation to plant-disperser interactions. The American Naturalist, 120, 218–241.

[51]

Holliday, R. (1989) Food, reproduction and longevity: is the extended lifespan of calorie-restricted animals an evolutionary adaptation? BioEssays, 10, 125–127.

[52]

House, H.L. (1969) Effects of different proportions of nutrients on insects. Entomologia Experimentalis et Applicata, 12, 651–669.

[53]

Huisamen, E.J., Colinet, H., Karsten, M. and Terblanche, J.S. (2022) Dietary salt supplementation adversely affects thermal acclimation responses of flight ability in Drosophila melanogaster. Journal of Insect Physiology, 140, 104403.

[54]

Hunt, J., Brooks, R., Jennions, M.D., Smith, M.J., Bentsen, C.L. and Bussière, L.F. (2004) High-quality male field crickets invest heavily in sexual display but die young. Nature, 432, 1024–1027.

[55]

Jaenike, J. (1990) Host specialization in phytophagous insects. Annual Review of Ecology and Systematics, 21, 243–273.

[56]

Janz, N. (2003) The cost of polyphagy: oviposition decision time vs error rate in a butterfly. Oikos, 100, 493–496.

[57]

Jaramillo, S.L., Mehlferber, E. and Moore, P.J. (2015) Life-history trade-offs under different larval diets in Drosophila suzukii (Diptera: Drosophilidae). Physiological Entomology, 40, 2–9.

[58]

Kenis, M., Tonina, L., Eschen, R., Van der Sluis, B., Sancassani, M., Mori, N. et al. (2016) Non-crop plants used as hosts by Drosophila suzukii in Europe. Journal of Pest Science, 89, 735–748.

[59]

Kennedy, G.G. and Storer, N.P. (2000) Life systems of polyphagous arthropod pests in temporally unstable cropping systems. Annual Review of Entomology, 45, 467–493.

[60]

Kristensen, T.N., Hoffmann, A.A., Overgaard, J., Sørensen, J.G., Hallas, R. and Loeschcke, V. (2008) Costs and benefits of cold acclimation in field-released Drosophila. Proceedings of the National Academy of Sciences USA, 105, 216–221.

[61]

Le Lann, C., Wardziak, T., Van Baaren, J. and van Alphen, J.J. (2011) Thermal plasticity of metabolicrates linked to life-history traits and foraging behaviour in a parasitic wasp. Functional Ecology, 25, 641–651.

[62]

Lee, J.C., Dreves, A.J., Cave, A.M., Kawai, S., Isaacs, R., Miller, J.C. et al. (2015) Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Annals of the Entomological Society of America, 108, 117–129.

[63]

Lee, K.P., Simpson, S.J., Clissold, F.J., Brooks, R., Ballard, J.W.O., Taylor, P.W. et al. (2008) Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proceedings of the National Academy of Sciences USA, 105, 2498–2503.

[64]

Lehmann, P., Van Der Bijl, W., Nylin, S., Wheat, C.W. and Gotthard, K. (2017) Timing of diapause termination in relation to variation in winter climate. Physiological Entomology, 42, 232–238.

[65]

Lenth, R.V., Bolker, B., Buerkner, P., Giné-Vázquez, I., Herve, M., Jung, M. et al. (2024) emmeans: estimated marginal means, aka least-squares means. R package version 1.10.4. https://cran.r-project.org/package=emmeans.

[66]

Little, C.M., Rizzato, A.R., Charbonneau, L., Chapman, T. and Hillier, N.K. (2019) Color preference of the spotted wing Drosophila, Drosophila suzukii. Scientific Reports, 9, 16051.

[67]

MacLean, H.J., Sørensen, J.G., Kristensen, T.N., Loeschcke, V., Beedholm, K., Kellermann, V. et al. (2019) Evolution and plasticity of thermal performance: an analysis of variation in thermal tolerance and fitness in 22 Drosophila species. Philosophical Transactions of the Royal Society B: Biological Sciences, 374, 20180548.

[68]

Marshall, K.E. and Sinclair, B.J. (2010) Repeated stress exposure results in a survival-reproduction trade-off in Drosophila melanogaster. Proceedings of the Royal Society B: Biological Sciences, 277, 963–969.

[69]

Menezes, B.F., Vigoder, F.M., Peixoto, A.A., Varaldi, J. and Bitner-Mathé, B.C. (2013) The influence of male wing shape on mating success in Drosophila melanogaster. Animal Behaviour, 85, 1217–1223.

[70]

Miller, B., Anfora, G., Buffington, M., Daane, K.M., Dalton, D.T., Hoelmer, K.M. et al. (2015) Seasonal occurrence of resident parasitoids associated with Drosophila suzukii in two small fruit production regions of Italy and the USA. Bulletin of Insectology, 68, 255–263.

[71]

Mitsui, H., Beppu, K. and Kimura, M.T. (2010) Seasonal life cycles and resource uses of flower-and fruit-feeding Drosophilid flies (Diptera: Drosophilidae) in central Japan. Entomological Science, 13, 60–67.

[72]

Moore, M.V. and Lee, R.E. (1991) Surviving the big chill: Overwintering strategies of aquatic and terrestrial insects. American Entomologist, 37, 111–118.

[73]

Olazcuaga, L., Rode, N.O., Foucaud, J., Facon, B., Ravigné, V., Ausset, A. et al. (2019) Oviposition preference and larval performance of Drosophila suzukii (Diptera: Drosophilidae), Spotted-Wing Drosophila: effects of fruit identity and composition. Environmental Entomology, 48, 867–881.

[74]

Ørsted, I.V. and Ørsted, M. (2019) Species distribution models of the Spotted Wing Drosophila (Drosophila suzukii, Diptera: Drosophilidae) in its native and invasive range reveal an ecological niche shift. Journal of Applied Ecology, 56, 423–435.

[75]

Panel, A.D.C., Pen, I., Pannebakker, B.A., Helsen, H.H.M. and Wertheim, B. (2020) Seasonal morphotypes of Drosophila suzukii differ in key life-history traits during and after a prolonged period of cold exposure. Ecology and Evolution, 10, 9085–9099.

[76]

Panel, A.D.C., Zeeman, L., Van der Sluis, B.J., Van Elk, P., Pannebakker, B.A., Wertheim, B. et al. (2018) Overwintered Drosophila Suzukii are the main source for infestations of the first fruit crops of the season. Insects, 9, 145.

[77]

Plantamp, C., Estragnat, V., Fellous, S., Desouhant, E. and Gibert, P. (2017) Where and what to feed? Differential effects on fecundity and longevity in the invasive Drosophila Suzukii. Basic and Applied Ecology, 19, 56–66.

[78]

Poyet, M., Havard, S., Prevost, G., Chabrerie, O., Doury, G., Gibert, P. et al. (2013) Resistance of Drosophila suzukii to the larval parasitoids Leptopilina heterotoma and Asobara japonica is related to haemocyte load. Physiological Entomology, 38, 45–53.

[79]

Poyet, M., Le Roux, V., Gibert, P., Meirland, A., Prévost, G., Eslin, P. et al. (2015) The wide potential trophic niche of the Asiatic fruit fly Drosophila suzukii: The key of its invasion success in temperate Europe? PLoS ONE, 10, e0142785.

[80]

Prior, W.D. (1881) Hardy Shrubs. G. Routledge, Oxford, London.

[81]

R Core Team. (2021) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

[82]

Ray, R.P., Nakata, T., Henningsson, P. and Bomphrey, R.J. (2016) Enhanced flight performance by genetic manipulation of wing shape in Drosophila. Nature Communications, 7, 10851.

[83]

Raynaud-Berton, B., Gibert, P., Suppo, C., Pincebourde, S. and Colinet, H. (2024) Modelling thermal reaction norms for development and viability in Drosophila suzukii under constant, fluctuating and field conditions. Journal of Thermal Biology, 123, 103891.

[84]

Rendon, D., Buser, J., Tait, G., Lee, J.C. and Walton, V.M. (2018) Survival and fecundity parameters of two Drosophila suzukii (Diptera: Drosophilidae) morphs on variable diet under suboptimal temperatures. Journal of Insect Science, 18, 8.

[85]

Rendon, D., Walton, V., Tait, G., Buser, J., Lemos Souza, I., Wallingford, A. et al. (2019) Interactions among morphotype, nutrition, and temperature impact fitness of an invasive fly. Ecology and Evolution, 9, 2615–2628.

[86]

Reyes-Ramírez, A., Belgaidi, Z., Gibert, P., Pommier, T., Siberchicot, A., Mouton, L. et al. (2023) Larval density in the invasive Drosophila suzukii: immediate and delayed effects on life-history traits. Ecology and Evolution, 13, e10433.

[87]

Roff, D.A. and Fairbairn, D.J. (2013) The costs of being dark: the genetic basis of melanism and its association with fitness-related traits in the sand cricket. Journal of Evolutionary Biology, 26, 1406–1416.

[88]

Rombouts, J.E. and Links, J. (1954) The chemical nature of the antibacterial substance present in Aucuba japonica Thunbg. Experientia, 12, 78–80.

[89]

Rota-Stabelli, O., Blaxter, M. and Anfora, G. (2013) Drosophila suzukii. Current Biology, 23, R8–R9.

[90]

Sánchez-Ramos, I., Fernández, C.E. and González-Núñez, M. (2019) Comparative analysis of thermal performance models describing the effect of temperature on the preimaginal development of Drosophila suzukii. Journal of Pest Science, 92, 523–541.

[91]

Sato, A., Tanaka, K.M., Yew, J.Y. and Takahashi, A. (2021) Drosophila suzukii avoidance of microbes in oviposition choice. Royal Society Open Science, 8, 201601.

[92]

Schlesener, D.C.H., Wollmann, J., Krüger, A.P., Martins, L.N., Teixeira, C.M., Bernardi, D. et al. (2020) Effect of temperature on reproduction, development, and phenotypic plasticity of Drosophila suzukii in Brazil. Entomologia Experimentalis et Applicata, 168, 817–826.

[93]

Sevenster, J.G. and Van Alphen, J.J.M. (1993) A life history trade-off in Drosophila species and community structure in variable environments. Journal of Animal Ecology, 62, 720–736.

[94]

Shearer, P.W., West, J.D., Walton, V.M., Brown, P.H., Svetec, N. and Chiu, J.C. (2016) Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC Ecology, 16, 11.

[95]

Shu, R., Uy, L. and Wong, A.C.N. (2022) Nutritional phenotype underlines the performance trade-offs of Drosophila suzukii on different fruit diets. Current Research in Insect Science, 2, 100026.

[96]

Silva-Soares, N.F., Nogueira-Alves, A., Beldade, P. and Mirth, C.K. (2017) Adaptation to new nutritional environments: larval performance, foraging decisions, and adult oviposition choices in Drosophila suzukii. BMC Ecology, 17, 21.

[97]

Simons, A.M. (2011) Modes of response to environmental change and the elusive empirical evidence for bet hedging. Proceedings of the Royal Society B: Biological Sciences, 278, 1601–1609.

[98]

Sinclair, B.J. (2015) Linking energetics and overwintering in temperate insects. Journal of Thermal Biology, 54, 5–11.

[99]

Singer, M.S. (2010) Evolutionary ecology of polyphagy. In Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects (ed. K. Tilmon), pp. 29–42. University of California Press, Berkeley.

[100]

Storey, K.B. and Storey, J.M. (2012) Insect cold hardiness: metabolic, gene, and protein adaptation. Canadian Journal of Zoology, 90, 456–475.

[101]

Talloen, W., Van Dyck, H. and Lens, L. (2004) The cost of melanization: Butterfly wing coloration under environmental stress. Evolution; International Journal of Organic Evolution, 58, 360–366.

[102]

Taylor, C.E. and Condra, C. (1980) r- and K-Selection in Drosophila pseudoobscura. Evolution; International Journal of Organic Evolution, 34, 1183–1193.

[103]

Thomas, P.A., Dering, M., Giertych, M.J., Iszkuło, G., Tomaszewski, D. and Briggs, J. (2023) Biological flora of Britain and Ireland: Viscum album: No. 303. Journal of Ecology, 111, 701–739.

[104]

Thompson, J.N. and Willson, M.F. (1979) Evolution of temperate fruit/bird interactions: phenological strategies. Evolution; International Journal of Organic Evolution, 33, 973–982.

[105]

Tochen, S., Woltz, J.M., Dalton, D.T., Lee, J.C., Wiman, N.G. and Walton, V.M. (2016) Humidity affects populations of Drosophila suzukii (Diptera: Drosophilidae) in blueberry. Journal of Applied Entomology, 140, 47–57.

[106]

Tochen, S., Dalton, D.T., Wiman, N., Hamm, C., Shearer, P.W. and Walton, V.M. (2014) Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environmental Entomology, 43, 501–510.

[107]

Toxopeus, J., Jakobs, R., Ferguson, L.V., Gariepy, T.D. and Sinclair, B.J. (2016) Reproductive arrest and stress resistance in winter-acclimated Drosophila suzukii. Journal of Insect Physiology, 89, 37–51.

[108]

Tu, M.P. and Tatar, M. (2003) Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell, 2, 327–333.

[109]

Ulmer, R., Couty, A., Eslin, P., Dubois, F., Gallet-Moron, E., Lamotte, N. et al. (2024) Urban ecology of Drosophila suzukii. Urban Ecosystems, 27, 1983–2004.

[110]

Ulmer, R., Couty, A., Eslin, P., Catterou, M., Baliteau, L., Bonis, A. et al. (2022) Macroecological patterns of fruit infestation rates by the invasive fly Drosophila suzukii in the wild reservoir host plant Sambucus nigra. Agricultural and Forest Entomology, 24, 548–563.

[111]

Ulmer, R., Couty, A., Eslin, P., Gabola, F. and Chabrerie, O. (2020) The firethorn (Pyracantha coccinea), a promising dead-end trap plant for the biological control of the spotted-wing Drosophila (Drosophila suzukii). Biological Control, 150, 104345.

[112]

Vivekanandhan, P., Swathy, K. and Shivakumar, M.S. (2022) Stability of insecticidal molecule aucubin and their toxicity on Anopheles stephensi, Aedes aegypti, Culex quinquefasciatus and Artemia salina. International Journal of Tropical Insect Science, 42, 3403–3417.

[113]

Wallingford, A.K., Lee, J.C. and Loeb, G.M. (2016) The influence of temperature and photoperiod on the reproductive diapause and cold tolerance of Spotted-Wing Drosophila, Drosophila suzukii. Entomologia Experimentalis et Applicata, 159, 327–337.

[114]

Wang, X.G., Stewart, T.J., Biondi, A., Chavez, B.A., Ingels, C., Caprile, J. et al. (2016) Population dynamics and ecology of Drosophila suzukii in Central California. Journal of Pest Science, 89, 701–712.

[115]

Wilson, A.J., Schutze, M., Elmouttie, D. and Clarke, A.R. (2012) Are insect frugivores always plant pests? The impact of fruit fly (Diptera: Tephritidae) larvae on host plant fitness. Arthropod-Plant Interactions, 6, 635–647.

[116]

Yeh, S.D. and True, J.R. (2014) The genetic architecture of coordinately evolving male wing pigmentation and courtship behavior in Drosophila elegans and Drosophila gunungcola. G3: Genes, Genomes, Genetics, 4, 2079–2093.

[117]

Young, Y., Buckiewicz, N. and Long, T.A.F. (2018) Nutritional geometry and fitness consequences in Drosophila suzukii, the spotted-wing Drosophila. Ecology and Evolution, 8, 2842–2851.

[118]

Zera, A.J. and Harshman, L.G. (2001) The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics, 32, 95–126.

RIGHTS & PERMISSIONS

2025 The Author(s). Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.

PDF (1328KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/