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Overwintering survival of Drosophila suzukii (Diptera: Drosophilidae) in temperature regimes emulating partly protected winter conditions in a cold–temperate climate of Québec, Canada

Published online by Cambridge University Press:  17 March 2021

Conrad Cloutier Open the ORCID record for Conrad Cloutier [Opens in a new window] ,
Jean-Frédéric Guay ,
William Champagne-Cauchon  and
Valérie Fournier
Conrad Cloutier*
Affiliation:
Département de Biologie, Pavillon Alexandre-Vachon, Université Laval, 1045 avenue de la Médecine, Québec, Québec, G1V 0A6, Canada
Jean-Frédéric Guay
Affiliation:
Département de Biologie, Pavillon Alexandre-Vachon, Université Laval, 1045 avenue de la Médecine, Québec, Québec, G1V 0A6, Canada
William Champagne-Cauchon
Affiliation:
Département de Biologie, Pavillon Alexandre-Vachon, Université Laval, 1045 avenue de la Médecine, Québec, Québec, G1V 0A6, Canada
Valérie Fournier
Affiliation:
Département de Phytologie, Centre de recherche et d’innovation sur les végétaux, Université Laval, 2480 boulevard Hochelaga, Québec, Québec, G1V 0A6, Canada
*
*Corresponding author. Email: conrad.cloutier@bio.ulaval.ca
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Abstract

Field-acclimated Drosophila suzukii (Diptera: Drosophilidae) from the Saguenay–Lac-Saint-Jean region, Québec, Canada, were examined over two years for winter survival, under the hypothesis that flies select protected overwintering microhabitats. In 2016–2017, flies trapped alive in the field or emerged from infested fruits were submitted to four winter regimes of either constant or daily fluctuating temperatures of 5 °C (2–8 °C) or 10 °C (7–13 °C). In 2017–2018, two fluctuating regimes averaging either 1 °C (–2 to 4 °C) or 3 °C (0–6 °C) were tested. Survival was modelled using Cox proportional hazard models testing probability that mortality risk varies with cold winter regime, fly sex, and fly provenance. Hazard ratios were about 1.7 times higher for males than for females. Models indicate that flies in constant and fluctuating 10 °C, in constant 5 °C, or in fluctuating 1 °C with daily exposure to –2 °C would not survive a six-month winter. Female survival extended to the next summer in fluctuating regimes averaging 5 °C or 3 °C. Estimates of 0.95 quantile survival (5%) indicate that overwintering D. suzukii experiencing such cold temperature regimes during winter, with no prolonged sub-zero temperatures, could survive until July of the following year, which is likely at the high population densities observed.

Résumé

Résumé

La survie hivernale de Drosophila suzukii (Diptera: Drosophilidae) provenant du Saguenay–Lac-Saint-Jean, Québec, Canada, a été étudiée durant deux ans, en supposant que les mouches choisissent leur microhabitat hivernal. En 2016–2017, des mouches piégées en champ ou émergées de fruits infestés ont été exposées à quatre régimes froids de températures constantes ou fluctuantes de 5 °C ou 10 °C. En 2017–2018, deux régimes fluctuants furent testés, dont la moyenne était 1 °C avec gel, ou 3 °C sans gel. Des modèles de risque proportionnel de Cox ont testé l’hypothèse que la mortalité dépend du régime froid hivernal, du sexe et de la provenance des mouches. Le rapport de risques instantanés des mâles était 1.7 fois plus élevé que celui des femelles. Des mouches hivernant sous un régime constant ou fluctuant de 10 °C, constant de 5 °C, ou fluctuant de 1 °C avec minimum de –2 °C, ne survivraient pas à l’hiver. La survie des femelles s’étendrait jusqu’à l’été sous un régime fluctuant de 5 °C ou 3 °C. Des estimés du quantile 0.95 de survie indiquent que des nombres substantiels de D. suzukii survivraient aux hivers locaux sous ces régimes fluctuants, sans gels prolongés, compte tenu des fortes densités automnales observées.

Type
Research Papers
Information
The Canadian Entomologist , Volume 153 , Issue 3 , June 2021 , pp. 259 - 278
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Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

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Footnotes

Subject editor: Katie Marshall

References

Alkema, J.T., Dicke, M., and Wertheim, B. 2019. Context-dependence and the development of push–pull approaches for integrated management of Drosophila suzukii . Insects, 10: article 454. http//doi.org/10.3390/insects10120454.CrossRefGoogle ScholarPubMed
Andreazza, F., Bernardi, D., dos Santos, R.S.S., Garcia, F.R.M., Oliveira, E.E., Botton, M., and Nava, D.E. 2017. Drosophila suzukii in southern Neotropical region: current status and future perspectives. Neotropical Entomology, 46: 591–605.CrossRefGoogle ScholarPubMed
Asplen, M.K., Anfora, G., Biondi, A., Choi, D.S., Chu, D., Daane, K.M., et al. 2015. Invasion biology of spotted wing drosophila (Drosophila suzukii): a global perspective and future priorities. Journal of Pest Science, 88: 469–494.CrossRefGoogle Scholar
Beers, E.H., Van Steenwyk, R.A., Shearer, P.W., Coates, W.W., and Grant, J.A. 2011. Developing Drosophila suzukii management programs for sweet cherry in the western United States. Pest Management Science, 67: 1386–1395. http//doi.org/10.1002/ps.2279.CrossRefGoogle ScholarPubMed
Blackburn, S., van Heerwaarden, B., Kellermann, V., and Sgrò, S.M. 2014. Evolutionary capacity of upper thermal limits: beyond single trait assessments. The Journal of Experimental Biology, 217: 1918–1924. http//doi.org/10.1242/jeb.099184.CrossRefGoogle ScholarPubMed
Bondi, A., Traugott, M., and Desneux, N. 2016. Special issue on Drosophila suzukii: from global invasion to sustainable control. Journal of Pest Science, 89: 603–851.CrossRefGoogle Scholar
Bowler, K. and Terblanche, J.S. 2008. Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biological Reviews, 83: 339–355. http://doi.org/10.1111/j.1469-185X.2008.00046.x.CrossRefGoogle ScholarPubMed
Bradshaw, W.E. and Holzapfel, C.M. 2010. Insects at not so low temperature: climate change in the temperate zone and its biotic consequences. Chapter 10. In Low temperature biology of insects. Edited by D.L. Denlinger and R.E. Lee, Jr. Cambridge University Press, Cambridge, United Kingdom. http://doi.org/10.1017/CBO9780511675997.011.Google Scholar
Bruck, D.J., Bolda, M., Tanigoshi, L., Klick, J., Kleiber, J., DeFrancesco, J., et al. 2011. Laboratory and field comparisons of insecticides to reduce infestation of Drosophila suzukii in berry crops. Pest Management Science, 67: 1375–1385.CrossRefGoogle ScholarPubMed
Centre for Agriculture and Bioscience. 2019. Invasive species compendium: Drosophila suzukii (spotted wing drosophila) [online]. Available from www.cabi.org/isc/datasheet/109283 [accessed 20 March 2020].Google Scholar
Champagne-Cauchon, W., Guay, J.-F., Fournier, V., and Cloutier, C. 2020. Phenology and spatial distribution of spotted wing drosophila in lowbush blueberry in Saguenay-Lac-Saint-Jean, Québec, Canada. The Canadian Entomologist, 152: 432–449.CrossRefGoogle Scholar
Cini, A., Ioratti, C., and Anfora, G. 2012. A review of the invasion of Drosophila suzukii in Europe: a draft research agenda for integrated pest management. Bulletin of Insectology, 65: 149–160.Google Scholar
Colinet, H., Nguyen, T.T.A., Cloutier, C., Michaud, D., and Hance, T. 2007. Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochemistry and Molecular Biology, 37: 1177–1188.CrossRefGoogle ScholarPubMed
Colinet, H., Rinehart, J.P., Yocum, G.D., and Greenlee, K.L. 2018. Mechanisms underpinning the beneficial effects of fluctuating thermal regimes in insect cold tolerance. Journal of Experimental Biology, 221: jeb164806. http//doi.org/10.1242/jeb.164806.CrossRefGoogle ScholarPubMed
Colinet, H., Sinclair, B.J., Vernon, P., and Renault, D. 2015. Insects in fluctuating thermal environments. Annual Review of Entomology, 6: 123–140.CrossRefGoogle Scholar
Dalton, D.T., Walton, V.M., Shearer, P.W., Walsh, D.B., Caprile, J., and Isaacs, R. 2011. Laboratory survival of Drosophila suzukii under simulated winter conditions of the Pacific Northwest and seasonal field trapping in five primary regions of small and stone fruit production in the United States. Pest Management Science, 67: 1368–1374.CrossRefGoogle ScholarPubMed
Diepenbrock, L.M., Hardin, J.A., Hannah, J., and Burrack, H.J. 2017. Season-long programs for control of Drosophila suzukii in southeastern U.S. blackberries. Crop Protection, 98: 149–156.CrossRefGoogle Scholar
Dos Santos, L.A., Mendes, M.F., Krüger, A.P., Blauth, M.L., Gottschalk, M.S., and Garcia, F.R. 2017. Global potential distribution of Drosophila suzukii (Diptera: Drosophilidae). PLOS One, 12: e0174318.CrossRefGoogle Scholar
Enriquez, T. and Colinet, H. 2017. Basal tolerance to heat and cold exposure of the spotted wing drosophila, Drosophila suzukii . PeerJ, 5: e3112. https://doi.org/10.7717/peerj.3112.CrossRefGoogle ScholarPubMed
Enriquez, T., Renault, D., Charrier, M., and Colinet, H. 2018a. Cold acclimation favors metabolic stability in Drosophila suzukii . Frontiers in Physiology, 9: 1506. http://doi.org/10.3389/fphys.2018.01506.CrossRefGoogle ScholarPubMed
Enriquez, T., Ruel, D., Charrier, M., and Colinet, H. 2018b. Effects of fluctuating thermal regimes on cold survival and life history traits of the spotted wing drosophila (Drosophila suzukii). Insect Science, 27: 317–335. http://doi.org/10.1111/1744-7917.12649.CrossRefGoogle Scholar
Grumiaux, C., Andersena, M.K., Colinet, H., and Overgaard, J. 2019. Fluctuating thermal regime preserves physiological homeostasis and reproductive capacity in Drosophila suzukii . Journal of Insect Physiology, 113: 33–41.CrossRefGoogle ScholarPubMed
Gullickson, M.G., Rogers, M.A., Burkness, E.C., and Hutchison, W.D. 2019. Efficacy of organic and conventional insecticides for Drosophila suzukii when combined with erythritol, a non-nutritive feeding stimulant. Crop Protection, 125: 104878. https://doi.org/10.1016/j.cropro.2019.104878.CrossRefGoogle Scholar
Jakobs, R., Gariepy, T.D., and Sinclair, B.J. 2015. Adult plasticity of cold tolerance in a continental–temperate population of Drosophila suzukii . Journal of Insect Physiology 79: 1–9.CrossRefGoogle Scholar
Kassambara, A. 2020. survminer v0.4.8: drawing survival curves using ‘ggplot2’ [online]. Available from https://www.rdocumentation.org/packages/survminer/versions/0.4.8.Google Scholar
Kimura, M.T. 2004. Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia, 140: 442–449.CrossRefGoogle ScholarPubMed
Kostal, V., Renault, D., Mehrabianov, A., and Bastl, J. 2007. Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comparative Biochemistry and Physiology, Part A, 147: 231–238.CrossRefGoogle ScholarPubMed
Langille, A.B., Arteca, E.M., Ryan, G.D., Emiljanowicz, L.M., and Newman, J.A. 2016. North American invasion of spotted-wing drosophila (Drosophila suzukii): a mechanistic model of population dynamics. Ecological Modelling, 336: 70–81.CrossRefGoogle Scholar
Langille, A.B., Arteca, E.M., and Newman, J.A. 2017. The impacts of climate change on the abundance and distribution of the spotted wing drosophila (Drosophila suzukii) in the United States and Canada. PeerJ, 5: e3192. http://doi.org/10.7717/peerj.3192.CrossRefGoogle ScholarPubMed
Lee, R.E. Jr. 2010. A primer on insect cold-tolerance. In Low temperature biology of insects. Chapter 1. Edited by D.L. Denlinger and R.E. Lee, Jr. Cambridge University Press, Cambridge, United Kingdom. https://doi.org/10.1017/CBO9780511675997.002.Google Scholar
Nikolouli, K., Colinet, H., Renault, D., Enriquez, T., Mouto, L., Gibert, P., et al. 2018. Sterile insect technique and Wolbachia symbiosis as potential tools for the control of the invasive species Drosophila suzukii . Journal of Pest Science, 91: 489–503. http://doi.org/10.1007/s10340-017-0944-y.CrossRefGoogle ScholarPubMed
Noble, R., Dobrovin-Pennington, A., Phillips, A., Cannon, M.F.L., Shaw, B., and Fountain, M.T. 2019. Improved insecticidal control of spotted wing drosophila (Drosophila suzukii) using yeast and fermented strawberry juice baits. Crop Protection, 125: 104902. https://doi.org/10.1016/j.cropro.2019.104878.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Rota-Stabelli, O., Blaxter, M., and Anfora, G. 2013. Drosophila suzukii . Current Biology, 23: R8. https://www.cell.com/current-biology/pdf/S0960-9822(12)01330-9.pdf.CrossRefGoogle ScholarPubMed
Schetelig, M.F., Lee, K.Z., Otto, S., Talmann, L., Stoekl, J., Degenkolb, T., et al. 2018. Environmentally sustainable pest control options for Drosophila suzukii. Journal of Applied Entomology, 142: 3–17. https://doi.org/10.1111/jen.12469.CrossRefGoogle Scholar
Schmidt, J.M., Whitehouse, T.S., Green, K., Krehenwinkel, H., Schmidt-Jeffrise, R., Ashfaq, A. and Sial, A.A. 2019. Local and landscape-scale heterogeneity shape spotted wing drosophila (Drosophila suzukii) activity and natural enemy abundance: implications for trophic interactions. Agriculture, Ecosystems & Environment, 272: 86–94.CrossRefGoogle Scholar
Stockon, D., Wallingford, A., Rendon, D., Fanning, P., Green, C.K., Diepenbrock, L., et al. 2019. Interactions between biotic and abiotic factors affect survival in overwintering Drosophila suzukii (Diptera: Drosophilidae). Environmental Entomology, 20: 1–11. https://doi.org/10.1093/ee/nvy192.Google Scholar
Therneau, T.M. 2020. Coxme: mixed effects Cox models [online]. R package. Version 2.2-16. Available from https://CRAN.R-project.org/package=coxme [accessed 9 January 2021].Google Scholar
Thistlewood, H., Gill, P., Beers, E.H., Shearer, P.W., Walsh, D.B., Rozema, B.M., et al. 2018. Spatial analysis of seasonal dynamics and overwintering of Drosophila suzukii (Diptera: Drosophilidae) in the Okanagan–Columbia Basin, 2010–2014. Environmental Entomology, 47: 221–232. https://doi.org/10.1093/ee/nvx178.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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. https://doi.org/10.1016/j.jinsphys.2016.03.006.CrossRefGoogle ScholarPubMed
Van Timmeren, S., Mota-Sanchez, D., Wise, J.C., and Isaacs, R., 2018. Baseline susceptibility of spotted wing drosophila (Drosophila suzukii) to four key insecticide classes. Pest Management Science, 74: 78–87. https://doi.org/10.1002/ps.4702.CrossRefGoogle ScholarPubMed
Wallingford, A.K. and Loeb, G.M. 2016. Developmental acclimation of Drosophila suzukii (Diptera: Drosophilidae) and its effect on diapauses and winter stress tolerance. Environmental Entomology, 45: 1081–1089.CrossRefGoogle Scholar
Walsh, D.B., Bolda, M.P., Goodhue, R.E., Dreves, A.J., Lee, J., Bruck, D.J., et al. 2011. Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. Journal of Integrated Pest Management, 2: G1–G7.CrossRefGoogle Scholar
Xue, Q., Majeed, M.Z., Zhang, W., and Ma, C. 2019. Adaptation of Drosophila species to climate change. a literature review since 2003. Journal of Integrative Agriculture, 18: 805–814.CrossRefGoogle Scholar
Zerulla, F.N., Schmidt, S., Streitberger, M., Zebitz, C.P.W., and Zelger, R. 2015. On the overwintering ability of Drosophila suzukii in South Tyrol. Journal of Berry Research, 5: 41–48. https://doi.org/10.3233/JBR-150089.CrossRefGoogle Scholar
Zhai, Y., Lin, Q., Zhang, J., Zhang, F., Zheng, L., and Yu, Y. 2016. Adult reproductive diapause in Drosophila suzukii females. Journal of Pest Science, 89: 679–688.CrossRefGoogle Scholar