Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-28T01:07:55.498Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of starvation on the cold tolerance of adult Drosophila suzukii (Diptera: Drosophilidae)

Published online by Cambridge University Press:  24 August 2021

Madelena De Ro ,
Thomas Enriquez ,
Jochem Bonte ,
Negin Ebrahimi ,
Hans Casteels ,
Patrick De Clercq  and
Hervé Colinet Open the ORCID record for Hervé Colinet [Opens in a new window]
Madelena De Ro
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant – Crop Protection – Entomology, Burgemeester Van Gansberghelaan 96, 9820 Merelbeke, Belgium Faculty of Bioscience Engineering, Department of Plants and Crops, Ghent University, Coupure Links 653, 9000 Gent, Belgium
Thomas Enriquez
Affiliation:
University of Rennes, CNRS, ECOBIO [(Ecosystèmes, biodiversité, évolution)] – UMR 6553, F-35000 Rennes, France
Jochem Bonte
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant – Crop Protection – Entomology, Burgemeester Van Gansberghelaan 96, 9820 Merelbeke, Belgium
Negin Ebrahimi
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant – Crop Protection – Entomology, Burgemeester Van Gansberghelaan 96, 9820 Merelbeke, Belgium
Hans Casteels
Affiliation:
Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant – Crop Protection – Entomology, Burgemeester Van Gansberghelaan 96, 9820 Merelbeke, Belgium
Patrick De Clercq
Affiliation:
Faculty of Bioscience Engineering, Department of Plants and Crops, Ghent University, Coupure Links 653, 9000 Gent, Belgium
Hervé Colinet*
Affiliation:
University of Rennes, CNRS, ECOBIO [(Ecosystèmes, biodiversité, évolution)] – UMR 6553, F-35000 Rennes, France
*
Author for correspondence: Hervé Colinet, Email: herve.colinet@univ-rennes1.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

The spotted wing drosophila, Drosophila suzukii, is an invasive pest in Europe and North America. Access to resources may be challenging in late fall, winter and early spring and flies may suffer from food deprivation along with cold stress in these periods. Whereas a plethora of studies have been performed on the overwintering capacity of D. suzukii, the effects of starvation on the fly's cold tolerance have not been addressed. In the present study, young D. suzukii adults (reared at 25°C, LD 12:12 h) were deprived of food for various periods (0, 12, 24 and 36 h), after which chill coma recovery time, critical thermal minimum, as well as acute and chronic cold tolerance were assessed. Additionally, the body composition of adults (body mass, water content, total lipid, glycerol, triglycerides, glucose and proteins) before and after starvation periods was analysed to confirm that starvation had detectable effects. Starved adults had a lower body mass, and both lipid and carbohydrate levels decreased with starvation time. Starvation slightly increased critical thermal minimum and affected chill coma recovery time; however, these changes were not gradual with starvation duration. Starvation promoted acute cold tolerance in both sexes. This effect appeared faster in males than in females. Food deprivation also led to enhanced survival to chronic cold stress. Short-term starvation was thus associated with significant changes in body composition in D. suzukii, and these alterations could alter some ecologically relevant traits related to cold tolerance, particularly in females. Our results suggest that food deprivation during short time (<36 h) can promote cold tolerance (especially survival after a cold stress) of D. suzukii flies. Future studies should address the ecological significance of these findings as short food deprivation may occur in the fields on many occasions and seasons.

Keywords

Body compositioncold hardinessenergy reservesfood deprivationspotted wing drosophila
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 6 , December 2021 , pp. 694 - 704
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andersen, JL, Findsen, A and Overgaard, J (2013) Feeding impairs chill coma recovery in the migratory locust (Locusta migratoria). Journal of Insect Physiology 59, 1041–1048.CrossRefGoogle Scholar
Andersen, JL, Manenti, T, Sørensen, JG, MacMillan, HA, Loeschcke, V and Overgaard, J (2015) How to assess Drosophila cold tolerance: chill coma temperature and lower lethal temperature are the best predictors of cold distribution limits. Functional Ecology 29, 55–65.CrossRefGoogle Scholar
Asplen, MK, Anfora, G, Biondi, A, Choi, D-S, Chu, D, Daane, KM, Gibert, P, Gutierrez, AP, Hoelmer, KA, Hutchison, WD, Isaacs, R, Jiang, Z-L, Kárpáti, Z, Kimura, MT, Pascual, M, Philips, CR, Plantamp, C, Ponti, L, Vétek, G, Vogt, H, Walton, VM, Yu, Y, Zappalà, L and Desneux, N (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. Journal of Pest Science 88, 469–494.CrossRefGoogle Scholar
Bale, JS (1993) Classes of insect old hardiness. Functional Ecology 7, 751–753.Google Scholar
Baust, JG and Morrissey, R (1975) Supercooling phenomenon and water content independence in the overwintering beetle, Coleomegilla maculata. Journal of Insect Physiology 21, 1751–1754.CrossRefGoogle Scholar
Bolda, MP, Goodhue, RE and Zalom, FG (2010) Spotted wing drosophila: potential economic impact of a newly established pest. Agricultural and Resource Economics Update 13, 5–8.Google Scholar
Bubliy, OA and Loeschcke, V (2005) Correlated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaster. Journal of Evolutionary Biology 18, 789–803.CrossRefGoogle Scholar
Calabria, G, Máca, J, Bächli, G, Serra, L and Pascual, M (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. Journal of Applied Entomology 136, 139–147.CrossRefGoogle Scholar
Chapman, RF (2013) The Insects: Structure and Function. Cambridge, UK: Cambridge University Press.Google Scholar
Chown, SL and Terblanche, JS (2006) Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33, 50–152.CrossRefGoogle ScholarPubMed
Colinet, H and Hoffmann, AA (2012) Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster. Functional Ecology 26, 84–93.CrossRefGoogle Scholar
Colinet, H, Siaussat, D, Bozzolan, F and Bowler, K (2013) Rapid decline of cold tolerance at young age is associated with expression of stress genes in Drosophila melanogaster. Journal of Experimental Biology 216, 253–259.Google ScholarPubMed
Colinet, H, Sinclair, BJ, Vernon, P and Renault, D (2015) Insects in fluctuating thermal environments. Annual Review of Entomology 60, 123–140.CrossRefGoogle ScholarPubMed
Danks, HV (1996) The wider integration of studies on insect cold-hardiness. European Journal of Entomology 93, 383–403.Google Scholar
David, RJ, Gibert, P, Pla, E, Petavy, G, Karan, D and Moreteau, B (1998) Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster. Journal of Thermal Biology 23, 291–299.CrossRefGoogle Scholar
David, JR, Gibert, P, Moreteau, B, Gilchrist, GW and Huey, RB (2003) The fly that came in from the cold: geographic variation of recovery time from low-temperature exposure in Drosophila subobscura. Functional Ecology 17, 425–430.CrossRefGoogle Scholar
Denlinger, DL and Lee, RE Jr (2010) Low Temperature Biology of Insects. Cambridge, UK: Cambridge University Press.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.CrossRefGoogle ScholarPubMed
Enriquez, T and Colinet, H (2019a) Cold acclimation triggers lipidomic and metabolic adjustments in the spotted wing drosophila Drosophila suzukii (Matsumara). American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 316, R751–R763.CrossRefGoogle Scholar
Enriquez, T and Colinet, H (2019b) Cold acclimation triggers major transcriptional changes in Drosophila suzukii. BMC Genomics 20, 413.CrossRefGoogle Scholar
Enriquez, T, Renault, D, Charrier, M and Colinet, H (2018) Cold acclimation favors metabolic stability in Drosophila suzukii. Frontiers in Physiology 9, 1506.CrossRefGoogle ScholarPubMed
Enriquez, T, Ruel, D, Charrier, M and Colinet, H (2020) Effects of fluctuating thermal regimes on cold survival and life history traits of the spotted wing Drosophila (Drosophila suzukii). Insect Science 27, 317–335.CrossRefGoogle Scholar
EPPO. Global Database. (2021) Last updated: 2021-01-27. Available at https://gd.eppo.int/taxon/DROSSU/distribution (Accessed 31 March 2021).Google Scholar
Everman, ER, Freda, PJ, Brown, M, Schieferecke, AJ, Ragland, GJ and Morgan, TJ (2018) Ovary development and cold tolerance of the invasive pest Drosophila suzukii (Matsumura) in the central plains of Kansas, United States. Environmental Entomology 47, 1013–1023.CrossRefGoogle ScholarPubMed
Fox, J and Weisberg, S (2011) An R Companion to Applied Regression. Thousand Oaks, California, USA: Sage Publications.Google Scholar
Gerken, AR, Eller, OC, Hahn, DA and Morgan, TJ (2015) Constraints, independence, and evolution of thermal plasticity: probing genetic architecture of long- and short-term thermal acclimation. Proceedings of the National Academy of Sciences of the USA 112, 4399–4404.CrossRefGoogle ScholarPubMed
Gibert, P and Huey, RB (2001) Chill-coma temperature in Drosophila: effects of developmental temperature, latitude and phylogeny. Physiological and Biochemical Zoology 74, 429–434.CrossRefGoogle ScholarPubMed
Goodhue, RE, Bolda, M, Farnsworth, D, Williams, JC and Zalom, FG (2011) Spotted wing drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Management Science 67, 1396–1402.CrossRefGoogle ScholarPubMed
Grumiaux, C, Andersen, MK, 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
Hamby, KA, Bellamy, DE, Chiu, JC, Lee, JC, Walton, VM, Wiman, NG, York, RM and Biondi, A (2016) Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. Journal of Pest Science 89, 605–619.CrossRefGoogle Scholar
Hauser, M (2011) A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Management Science 67, 1352–1357.CrossRefGoogle ScholarPubMed
Haye, T, Girod, P, Cuthbertson, AGS, Wang, XG, Daane, KM, Hoelmer, KA, Baroffio, C, Zhang, JP and Desneux, N (2016) Current SWD IPM tactics and their practical implementation in fruit crops across different regions around the world. Journal of Pest Science 89, 643–651.CrossRefGoogle Scholar
Hazell, SP and Bale, JS (2011) Low temperature thresholds: are chill coma and CTmin synonymous? Journal of Insect Physiology 57, 1085–1089.CrossRefGoogle Scholar
Henry, Y and Colinet, H (2018) Microbiota disruption leads to reduced cold tolerance in Drosophila flies. Science of Nature 105, 59.CrossRefGoogle ScholarPubMed
Henry, Y, Renault, D and Colinet, H (2018) Hormesis-like effect of mild larval crowding on thermotolerance in Drosophila flies. Journal of Experimental Biology 221, jeb169342.CrossRefGoogle ScholarPubMed
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, A 241, 110626.CrossRefGoogle ScholarPubMed
Hoffmann, AA, Hallas, R, Anderson, AR and Telonis-Scott, M (2005) Evidence for a robust sex-specific trade-off between cold resistance and starvation resistance in Drosophila melanogaster. Journal of Evolutionary Biology 18, 804–810.CrossRefGoogle ScholarPubMed
Jakobs, R, Gariepy, TD and Sinclair, BJ (2015) Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii. Journal of Insect Physiology 79, 1–9.CrossRefGoogle Scholar
Jakobs, R, Ahmadi, B, Houben, S, Gariepy, TD and Sinclair, BJ (2016) Cold tolerance of third-instar Drosophila suzukii larvae. Journal of Insect Physiology 96, 45–52.CrossRefGoogle ScholarPubMed
Kenis, M, Tonina, L, Eschen, R, van der Sluis, B, Sancassani, M, Mori, N, Haye, T and Helsen, H (2016) Non-crop plants used as hosts by Drosophila suzukii in Europe. Journal of Pest Science 89, 735–748.CrossRefGoogle ScholarPubMed
Kimura, MT (2004) Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia 140, 442–449.CrossRefGoogle ScholarPubMed
Kubrak, OI, Nylin, S, Flatt, T, Nässel, DR and Leimar, O (2017) Adaptation to fluctuating environments in a selection experiment with Drosophila melanogaster. Ecology and Evolution 7, 3796–3807.CrossRefGoogle Scholar
Leather, SR, Walters, KFA and Bale, JS (1993) The Ecology of Insect Overwintering. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Le Bourg, É (2013) Fasting can protect young and middle-aged Drosophila melanogaster flies against a severe cold stress. Biogerontology 14, 513–529.CrossRefGoogle Scholar
Le Bourg, É (2015) Fasting and other mild stresses with hormetic effects in Drosophila melanogaster can additively increase resistance to cold. Biogerontology 16, 517–527.CrossRefGoogle Scholar
Le Bourg, É and Massou, I (2015) Fasting increases survival to cold in FOXO, DIF, autophagy mutants and in other genotypes of Drosophila melanogaster. Biogerontology 16, 411–421.CrossRefGoogle ScholarPubMed
Lee, KP and Jang, T (2014) Exploring the nutritional basis of starvation resistance in Drosophila melanogaster. Functional Ecology 25, 1144–1155.CrossRefGoogle Scholar
Lee, JC, Bruck, DJ, Curry, H, Edwards, D, Haviland, DR, Van Steenwyk, RA and Yorgey, BM (2011) The susceptibility of small fruits and cherries to the spotted-wing drosophila, Drosophila suzukii. Pest Management Science 67, 1358–1367.CrossRefGoogle ScholarPubMed
Lenth, R (2018) Emmeans: estimated marginal means, aka least-squares means. R package version 1.1.3. Available at https://CRAN.R-project.org/package=emmeans.Google Scholar
MacMillan, HA and Sinclair, BJ (2011) Mechanisms underlying insect chill-coma. Journal of Insect Physiology 57, 12–20.CrossRefGoogle ScholarPubMed
Marron, MT, Markow, TA, Kain, KJ and Gibbs, AG (2003) Effects of starvation and desiccation on energy metabolism in desert and mesic Drosophila. Journal of Insect Physiology 49, 261–270.CrossRefGoogle ScholarPubMed
Mazzi, D, Bravin, E, Meraner, M, Finger, R and Kuske, S (2017) Economic impact of the introduction and establishment of Drosophila suzukii on sweet cherry production in Switzerland. Insects 8, 18.CrossRefGoogle ScholarPubMed
Mitchell, KA, Boardman, L, Clusella-Trullas, S and Terblanche, JS (2017) Effects of nutrient and water restriction on thermal tolerance: a test of mechanisms and hypotheses. Comparative Biochemistry and Physiology A 212, 15–23.CrossRefGoogle ScholarPubMed
Mitsui, H, Beppu, K and Kimura, MT (2010) Seasonal life cycles and resource uses of flower- and fruit-feeding drosophilid flies (Diptera: Drosophilidae) in central Japan. Entomological Science 13, 60–67.CrossRefGoogle Scholar
Nikolouli, K, Colinet, H, Renault, D, Enriquez, T, Mouton, L, Gibert, P, Sassu, F, Cáceres, C, Stauffer, C, Pereira, R and Bourtzis, K (2017) 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.CrossRefGoogle ScholarPubMed
Nyamukondiwa, C and Terblanche, JS (2009) Thermal tolerance in adult Mediterranean and Natal fruit flies (Ceratitis capitata and Ceratitis rosa): effects of age, gender and feeding status. Journal of Thermal Biology 34, 406–414.CrossRefGoogle Scholar
Oudman, L, Van Delden, W, Kamping, A and Bijlsma, R (1994) Starvation resistance in Drosophila melanogaster in relation to the polymorphisms at the Adh and αGdph loci. Journal of Insect Physiology 40, 709–713.CrossRefGoogle Scholar
Overgaard, J and MacMillan, HA (2017) The integrative physiology of insect chill tolerance. Annual Review of Physiology 79, 187–208.CrossRefGoogle ScholarPubMed
Pathak, A, Munjal, A and Parkash, R (2018) Cold acclimation conditions constrain plastic responses for resistance to cold and starvation in Drosophila immigrans. Biology Open 7, bio034447.CrossRefGoogle ScholarPubMed
Pelton, E, Gratton, C, Isaacs, R, Van Timmeren, S, Blanton, A and Guédot, C (2016) Earlier activity of Drosophila suzukii in high woodland landscapes but relative abundance is unaffected. Journal of Pest Science 89, 725–733.CrossRefGoogle Scholar
Peters, G-JY (2017) Diamond plots: a tutorial to introduce a visualization tool that facilitates interpretation and comparison of multiple sample estimates while respecting their inaccuracy. PsyArXiv Preprints. Available at http://osf.io/fzh6c.CrossRefGoogle Scholar
Plantamp, C, Salort, K, Gibert, P, Dumet, A, Mialdea, G, Mondy, N and Voituron, Y (2016) All or nothing: survival, reproduction and oxidative balance in spotted wing drosophila (Drosophila suzukii) in response to cold. Journal of Insect Physiology 89, 28–36.CrossRefGoogle Scholar
Ransberry, VE, MacMillan, HA and Sinclair, BJ (2011) The relationship between chill-coma onset and recovery at the extremes of the thermal window of Drosophila melanogaster. Physiological and Biochemical Zoology 84, 553–559.CrossRefGoogle Scholar
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/.Google Scholar
Rion, S and Kawecki, TJ (2007) Evolutionary biology of starvation resistance: what we have learned from Drosophila. Journal of Evolutionary Biology 20, 1655–1664.CrossRefGoogle ScholarPubMed
Rombaut, A, Guilhot, R, Xuéreb, A, Benoit, L, Chapuis, MP, Gibert, P and Fellous, S (2017) Invasive Drosophila suzukii facilitates Drosophila melanogaster infestation and sour rot outbreaks in the vineyards. Royal Society Open Science 4, 170117.CrossRefGoogle ScholarPubMed
Rossi-Stacconi, MV, Kaur, R, Mazzoni, V, Ometto, L, Grassi, A, Gottardello, A, Rota-Stabelli, O and Anfora, G (2016) Multiple lines of evidence for reproductive winter diapause in the invasive pest Drosophila suzukii: useful clues for control strategies. Journal of Pest Science 89, 689–700.CrossRefGoogle Scholar
Ryan, GD, Emiljanowicz, L, Wilkinson, F, Kornya, M and Newman, JA (2016) Thermal tolerances of the spotted-wing drosophila Drosophila suzukii (Diptera: Drosophilidae). Journal of Economic Entomology 109, 746–752.CrossRefGoogle Scholar
Salin, C, Renault, D, Vannier, G and Vernon, P (2000) A sexually dimorphic response in supercooling temperature, enhanced by starvation in the lesser mealworm, Alphitobius diaperinus (Coleoptera: Tenebrionidae). Journal of Thermal Biology 25, 411–418.CrossRefGoogle Scholar
Salt, RW (1953) The influence of food on cold hardiness of insects. Canadian Entomologist 85, 261–269.CrossRefGoogle Scholar
Scharf, I, Wexler, Y, MacMillan, HA, Presman, S, Simson, E and Rosenstein, S (2016) The negative effect of starvation and the positive effect of mild thermal stress on thermal tolerance of the red flour beetle, Tribolium castaneum. Science of Nature 103, 20.CrossRefGoogle ScholarPubMed
Scharf, I, Daniel, A, MacMillan, HA and Katz, N (2017) The effect of fasting and body reserves on cold tolerance in 2 pit-building insect predators. Current Zoology 63, 287–294.Google ScholarPubMed
Schwasinger-Schmidt, TE, Kachman, SD and Harshman, LG (2012) Evolution of starvation resistance in Drosophila melanogaster: measurement of direct and correlated responses to artificial selection. Journal of Evolutionary Biology 25, 378–387.CrossRefGoogle ScholarPubMed
Shearer, PW, West, JD, Walton, VM, Brown, PH, Svetec, N and Chiu, JC (2016) Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC Ecology 16, 11.CrossRefGoogle ScholarPubMed
Sinclair, BJ, Coello Alvarado, LE and Ferguson, LV (2015) An invitation to measure insect cold tolerance: methods, approaches, and workflow. Journal of Thermal Biology 53, 180–197.CrossRefGoogle ScholarPubMed
Sømme, L (1982) Supercooling and winter survival in terrestrial arthropods. Comparative Biochemistry and Physiology A 73, 519–543.CrossRefGoogle Scholar
Sømme, L and Block, W (1982) Cold hardiness of Collembola at Signy Island, maritime Antarctic. Oikos 38, 168–176.CrossRefGoogle Scholar
Sømme, L and Conradi-Larsen, EM (1977) Cold-hardiness of collembolans and oribatid mites from windswept mountain ridges. Oikos 29, 118–126.CrossRefGoogle Scholar
Stephens, AR (2015) Cold Tolerance of Drosophila Suzukii (Diptera: Drosophilidae) (MSc thesis). University of Minnesota, St. Paul, Minnesota, USA.Google Scholar
Stephens, AR, Asplen, MK, Hutchison, WD and Venette, RC (2015) Cold hardiness of winter-acclimated Drosophila suzukii (Diptera: Drosophilidae) adult. Environmental Entomology 44, 1619–1626.CrossRefGoogle Scholar
Stockton, DG, Wallingford, AK and Loeb, GM (2018) Phenotypic plasticity promotes overwintering survival in a globally invasive crop pest, Drosophila suzukii. Insects 9, 105.CrossRefGoogle Scholar
Tennessen, JM, Barry, WE, Cox, J and Thummel, CS (2014) Methods for studying metabolism in Drosophila. Methods 68, 105–115.CrossRefGoogle ScholarPubMed
Terblanche, JS, Clusella-Trullas, S, Deere, JA and Chown, SL (2008) Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): implications for forecasting climate change impacts. Journal of Insect Physiology 54, 114–127.CrossRefGoogle Scholar
Thistlewood, HMA, Gill, P, Beers, EH, Shearer, PW, Walsh, DB, Rozema, BM, Acheampong, S, Castagnoli, S, Yee, WL, Smytheman, P and Whitener, AB (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.CrossRefGoogle ScholarPubMed
Toxopeus, J, Jakobs, R, Ferguson, LV, Gariepy, TD and Sinclair, BJ (2016) Reproductive arrest and stress resistance in winter-acclimated Drosophila suzukii. Journal of Insect Physiology 89, 37–51.CrossRefGoogle ScholarPubMed
Wallingford, AK and Loeb, GM (2016) Developmental acclimation of Drosophila suzukii (Diptera: Drosophilidae) and its effect on diapause and winter stress tolerance. Environmental Entomology 45, 1081–1089.CrossRefGoogle Scholar
Wallingford, AK, Lee, JC and Loeb, GM (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.CrossRefGoogle Scholar
Walsh, DB, Bolda, MP, Goodhue, RE, Dreves, AJ, Lee, J, Bruck, DJ, Vaughn, MW, O'Neal, SD and Zalom, FG (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
Zerulla, FN, Schmidt, S, Streitberger, M, Zebitz, CPW and Zelger, R (2015) On the overwintering ability of Drosophila suzukii in South Tyrol. Journal of Berry Research 5, 41–48.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