cold storage; fluctuating thermal regimes; life-history traits; recovery; spotted wing drosophila; Animals; Drosophila/physiology; Female; Fertility; Male; Sexual Behavior, Animal; Cold-Shock Response; Life History Traits; Drosophila; Ecology, Evolution, Behavior and Systematics; Agronomy and Crop Science; Biochemistry, Genetics and Molecular Biology (all); Insect Science; General Biochemistry, Genetics and Molecular Biology
Abstract :
[en] Drosophila suzukii is an invasive pest causing severe damages to a large panel of cultivated crops. To facilitate its biocontrol with strategies such as sterile or incompatible insect techniques, D. suzukii must be mass-produced and then stored and transported under low temperature. Prolonged cold exposure induces chill injuries that can be mitigated if the cold period is interrupted with short warming intervals, referred to as fluctuating thermal regimes (FTR). In this study, we tested how to optimally use FTR to extend the shelf life of D. suzukii under cold storage. Several FTR parameters were assessed: temperature (15, 20, 25 °C), duration (0.5, 1, 2, 3 h), and frequency (every 12, 24, 36, 48 h) of warming intervals, in two wild-type lines and in two developmental stages (pupae and adults). Generally, FTR improved cold storage tolerance with respect to constant low temperatures (CLT). Cold mortality was lower when recovery temperature was 20 °C or higher, when duration was 2 h per day or longer, and when warming interruptions occurred frequently (every 12 or 24 h). Applying an optimized FTR protocol to adults greatly reduced cold mortality over long-term storage (up to 130 d). Consequences of FTR on fitness-related traits were also investigated. For adults, poststorage survival was unaffected by FTR, as was the case for female fecundity and male mating capacity. On the other hand, when cold storage occurred at pupal stage, poststorage survival and male mating capacity were altered under CLT, but not under FTR. After storage of pupae, female fecundity was lower under FTR compared to CLT, suggesting an energy trade-off between repair of chill damages and egg production. This study provides detailed information on the application and optimization of an FTR-based protocol for cold storage of D. suzukii that could be useful for the biocontrol of this pest.
Disciplines :
Entomology & pest control Environmental sciences & ecology
Author, co-author :
Enriquez, Thomas ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs ; CNRS, ECOBIO-UMR 6553, Université de Rennes, Rennes, France
Ruel, David; CNRS, ECOBIO-UMR 6553, Université de Rennes, Rennes, France
Charrier, Maryvonne ; CNRS, ECOBIO-UMR 6553, Université de Rennes, Rennes, France
Colinet, Hervé ; CNRS, ECOBIO-UMR 6553, Université de Rennes, Rennes, France
Language :
English
Title :
Effects of fluctuating thermal regimes on cold survival and life history traits of the spotted wing Drosophila (Drosophila suzukii).
ANR - Agence Nationale de la Recherche [FR] FWF - Austrian Science Fund [AT]
Funding text :
This study was funded by SUZUKILL project (The French National Research Agency): ANR-15-CE21-0017 and Austrian Science Fund (FWF): I 2604-B25. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We would like to thanks Gaëtan CORMY, bachelor student, for his valuable help on the flies mating assays.
Araripe, L.O., Klaczko, L.B., Moreteau, B. and David, J.R. (2004) Male sterility thresholds in a tropical cosmopolitan drosophilid. Zaprionus indianus. Journal of Thermal Biology, 29, 73–80.
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.
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.
Basson, C.H., Nyamukondiwa C. and Terblanche, J.S. (2012) Fitness costs of rapid cold-hardening in Ceratitis capitata. Evolution, 66, 296–304.
Boardman, L., Sørensen, J.G. and Terblanche, J.S. (2013) Physiological responses to fluctuating thermal and hydration regimes in the chill susceptible insect, Thaumatotibia leucotreta. Journal of Insect Physioliogy, 59, 781–794.
Calabria, G., Máca, J., Bächli, G., Serra, L. and Pascual, M. (2012) First records of the potential pest species Drosophila suzukii in Europe. Journal of Applied Entomology, 136, 139–147.
Carroll, A.L. and Quiring, D.T. (1993) Interactions between size and temperature influence fecundity and longevity of a tortricid moth, Zeiraphera canadensis. Oecologia, 93, 233–241.
Cini, A., Ioratti, C. and Anforta, G. (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bulletin of Insectology, 65, 149–160.
Clark, M.S. and Worland, M.R. (2008) How insects survive the cold: molecular mechanisms—a review. Journal of Comparative Physiology B, 178, 917–933.
Colinet, H. and Hance, T. (2009) Male reproductive potential of Aphidius colemani (Hymenoptera: Aphidiinae) exposed to constant or fluctuating thermal regimes. Environmental Entomolology, 38, 242–249.
Colinet, H. and Hance, T. (2010) Interspecific variation in the response to low temperature storage in different aphid parasitoids. Annals of Applied Biology, 156, 147–156.
Colinet, H. and Renault, D. (2012) Metabolic effects of CO2 anesthesia in Drosophila melanogaster. Biology Letters, 8, 1050–1054.
Colinet, H., Chertemps, T., Boulogne, I. and Siaussat, D. (2015a) Age-related decline of abiotic stress tolerance in young Drosophila melanogaster adults. Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 71, 1574–1580.
Colinet, H., Lalouette, L. and Renault, D. (2011) A model for the time–temperature–mortality relationship in the chill-susceptible beetle, Alphitobius diaperinus, exposed to fluctuating thermal regimes. Journal of Thermal Biology, 36, 403–408.
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.
Colinet, H., Overgaard, J., Com, E. and Sørensen, J.G. (2013) Proteomic profiling of thermal acclimation in Drosophila melanogaster. Insect Biochemistry and Molecular Biology, 43, 352–365.
Colinet, H., Renault, D., Hance, T. and Vernon, P. (2006) The impact of fluctuating thermal regimes on the survival of a cold-exposed parasitic wasp, Aphidius colemani. Physioligical Entomology, 31, 234–240.
Colinet, H., Renault, D., Javal, M., Berková, P., Šimek, P. and Koštál, V. (2016) Uncovering the benefits of fluctuating thermal regimes on cold tolerance of Drosophila flies by combined metabolomic and lipidomic approach. Biochimica et Biophysica Acta Molecular and Cell Biology of Lipids, 1861, 1736–1745.
Colinet, H., Rinehart, J.P., Yocum, G.D. and Greenlee, K.J. (2018) Mechanisms underpinning the beneficial effects of fluctuating thermal regimes in insect cold tolerance. Journal of Experimental Biology, 221, jeb164806. https://doi.org/10.1242/jeb.164806.
Colinet, H., Sinclair, B.J., Vernon, P. and Renault, D. (2015b) Insects in fluctuating thermal environments. Annual Review of Entomology, 60, 123–140.
Crawley, M.J. (2007) The R Book. Wiley, Chichester, UK/ Hoboken, NJ.
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.
David, J.R., Araripe, L.O., Chakir, M., Legout, H., Lemos, B., Petavy, G. et al. (2005) Male sterility at extreme temperatures: a significant but neglected phenomenon for understanding Drosophila climatic adaptations. Journal of Evolutionary Biology, 18, 838–846.
Denlinger, D.L. and Lee, R.E. Jr. (2010) Low Temperature Biology of Insects. Cambridge University Press, Cambridge, UK.
Dollo, V.H., Yi, S.X. and Lee, R.E. Jr. (2010) High temperature pulses decrease indirect chilling injury and elevate ATP levels in the flesh fly, Sarcophaga crassipalpis. Cryobiology, 60, 351–353.
Eben, A., Reifenrath, M., Briem, F., Pink, S., and Vogt, H. (2018) Response of Drosophila suzukii (Diptera: Drosophilidae) to extreme heat and dryness. Agricultural and Forest Entomology, 20, 113–121.
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.
Evans, R.K., Toews, M.D. and Sial, A.A. (2017) Diel periodicity of Drosophila suzukii (Diptera: Drosophilidae) under field conditions. PLoS ONE, 12, e0171718. https://doi.org/10.1371/journal.pone.0171718.
Fox, J. (2003) Effect displays in R for generalized linear models. Journal of Statistical Software, 8, 1–27.
Fox, J. and Weisberg, S. (2011) An {R} Companion to Applied Regression. 2nd edn. Sage, Thousand Oaks.
Gelman, A. and Su, Y.S. (2014) Arm: data analysis using regression and multilevel/hierarchical models. R package version 1.7-07. Available at http://CRAN.R-project.org/package=arm, Access date: May-2018.
Goodhue, E.G., Bolda, M., Farnsworth, D., Williams, J.C. and Zalom, F.G. (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.
Gruntenko, N.E., Bownes, M., Terashima, J., Sukhanova, M.Z. and Raushenbach, I.Y. (2003) Heat stress affects oogenesis differently in wild-type Drosophila virilis and a mutant with altered juvenile hormone and 20-hydroxyecdysone levels. Insect Molecular Biology, 12, 393–404.
Hanč, Z. and Nedvéd, O. (1999) Chill injury at alternating temperatures in Orchesella cincta (Collembola: Entomobryidae) and Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). European Journal of Entomology, 96, 165–168.
Hardeland, R. (1972) Species differences in the diurnal rhythmicity of courtship behavior within the melanogaster group of the genus Drosophila. Animal Behaviour, 20, 170–174.
Hauser, M. (2011) A historic account of the invasion of Drosophila suzukii in the continental United States, with remarks on their identification. Pest Management Science, 67, 1352–1357.
Hauser, M., Gaimari, S. and Damus, M. (2009) Drosophila suzukii new to North America. Fly, 43, 12–15.
Hawes, T.C., Bale, J.S., Worland, M.R. and Convey, P. (2008) Trade-offs between microhabitat selection and physiological plasticity in the Antarctic springtail, Cryptopygus antarcticus (Willem). Polar Biology, 31, 681–689.
Hothorn, T., Bretz, F. and Westfall, P. (2008) Simultaneous inference in general parametric models. Biometrical Journal, 50, 346–363.
Ismail, M., Vernon, P., Hance, T. and van Baaren, J. (2010) Physiological costs of cold exposure on the parasitoid Aphidius ervi, without selection pressure and under constant or fluctuating temperatures. BioControl, 55, 729–740.
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.
Javal, M., Renault, D. and Colinet, H. (2016) Impact of fluctuating thermal regimes on Drosophila melanogaster survival to cold stress. Animal Biology, 66, 427–444.
Jones, S.R. and Kunz, S.E. (1998) Effects of cold stress on survival and reproduction of Haematobia irritans (Diptera: Muscidae). Journal of Medical Entomology, 35, 725–731.
Kalmus, H. (1943) A factorial experiment on the mineral requirements of a Drosophila culture. The American Naturalist, 77, 376–380.
Kanzawa, T. (1939) Studies on Drosophila suzukii Mats. Yamanashi: Kofu, Yamanashi Applied Experimental Station, 1–49. Abstract in The Review of Applied Entomology, 29:622.
Kelty, J.D., Killian, K.A. and Lee, R.E. (1996) Cold shock and rapid cold-hardening of pharate adult flesh flies (Sarcophaga crassipalpis): effects on behaviour and neuromuscular function following eclosion. Physiological Entomology, 21, 283–288.
Kim, M.J., Kim, J.S., Park, J.S., Choi, D.S., Park, J. and Kim, I. (2015) Oviposition and development potential of the spotted-wing drosophila, Drosophila suzukii (Diptera: Drosophilidae), on uninjured Campbell Early grape. Entomological Research, 45, 354–359.
Kimura, M.T. (2004) Cold and heat tolerance of Drosophilid flies with reference to their latidudinal distributions. Oecologia, 140, 442–449.
Klockmann, M., Kleinschmidt, F. and Fischer, K. (2017) Carried over: heat stress in the egg stage reduces subsequent performance in a butterfly. PLoS ONE, 12, e0180968, https://doi.org/10.1371/journal.pone.0180968.
Koštál, V., Korbelová, J., Štětina, T., Poupardin, R., Colinet, H., Zahradníčková, H. et al. (2016) Physiological basis for low-temperature survival and storage of quiescent larvae of the fruit fly Drosophila melanogaster. Scientific Reports, 6, 32346.
Koštál, V., Renault, D., Mehrabianova, 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 A, 147, 231–238.
Koštál, V., Vambera, J. and Bastl, J. (2004) On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in adults of Pyrrhocoris apterus. Journal of Experimental Biology, 207, 1509–1521.
Lacoume, S., Bressac, C. and Chevrier, C. (2007) Sperm production and mating potential of males after a cold shock on pupae of the parasitoid wasp Dinarmus basalis (Hymenoptera: Pteromalidae). Journal of Insect Physiology, 53, 1008–1015.
Lalouette, L., Koštál, V., Colinet, H., Gagneul, D. and Renault, D. (2007) Cold exposure and associated metabolic changes in adult tropical beetles exposed to fluctuating thermal regimes. FEBS Journal, 274, 1759–1767.
Lalouette, L., Williams, C.M., Hervant, F., Sinclair, B.J. and Renault, D. (2011) Metabolic rate and oxidative stress in insects exposed to low temperature thermal fluctuations. Comparative Biochemistry and Physiology A, 158, 229–234.
MacMillan, H.A. and Sinclair, B.J. (2011) Mechanisms underlying insect chill-coma. Journal of Insect Physiology, 57, 12–20.
Mitsui, H., Takahashi, K.H. and Kimura, M.T. (2006) Spatial distributions and clutch sizes of Drosophila species ovipositing on cherry fruits of different stages. Population Ecology, 48, 233–237.
Murdoch, V.J., Cappuccino, N. and Mason, P.G. (2013) The effects of periodic warming on the survival and fecundity of Diadromus pulchellus during long-term storage. Biocontrol Science and Technology, 23, 211–219.
Mutika, G.N., Kabore, I., Parker, A.G. and Vreysen, M.J. (2014) Storage of male Glossina palpalis gambiensis pupae at low temperature: effect on emergence, mating and survival. Parasites & Vectors, 7, 465.
Nedvěd, O., Lavy, D. and Verhoef, H.A. (1998) Modelling the time–temperature relationship in cold injury and effect of high-temperature interruptions on survival in a chill-sensitive collembolan. Functional Ecology, 12, 816–824.
Nikolouli, K., Colinet, H., Renault, D., Enriquez, T., Mouton, 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.
Partridge, L. and Farquhar, M. (1983) Lifetime mating success of male fruit flies (Drosophila melanogaster) is related to their size. Animal Behaviour, 31, 871–877.
Pio, C.J. and Baust, J.G. (1988) Effects of temperature cycling on cryoprotectant profiles in the goldenrod gall fly, Eurosta solidaginis (Fitch). Journal of Insect Physiology, 34, 767–771.
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.
Porcelli, D., Gaston, K.J., Butlin, R.K. and Snook, R.R. (2017) Local adaptation of reproductive performance during thermal stress. Journal of Evolutionary Biology, 30, 422–429.
R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
Raspi, A., Canale, A., Canovai, R., Conti, B., Loni, A. and Strumia, F. (2011) Insetti delle aree protette del comune di San Giuliano Terme. Felici editore. Pisa: San Giuliano Terme, Italy.
Renault, D., Nedvéd, O., Hervant, F. and Vernon, P. (2004) The importance of fluctuating thermal regimes for repairing chill injuries in the tropical beetle Alphitobius diaperinus (Coleoptera: Tenebrionidae) during exposure to low temperature. Physiological Entomology, 29, 139–145.
Rinehart, J.P., Yocum, G.D. and Denlinger, D.L. (2000) Thermotolerance and rapid cold hardening ameliorate the negative effects of brief exposures to high or low temperatures on fecundity in the flesh fly, Sarcophaga crassipalpis. Physiological Entomology, 25, 330–336.
Rinehart, J.P., Yocum, G.D., Kemp, W.P. and Bowsher, J.H. (2016) Optimizing fluctuating thermal regime storage of developing Megachile rotundata (Hymenoptera: Megachilidae). Journal of Economic Entomology, 109, 993–1000.
Rinehart, J.P., Yocum, G.D., West, M. and Kemp, W.P. (2011) A fluctuating thermal regime improves survival of cold-mediated delayed emergence in developing Megachile rotundata (Hymenoptera: Megachilidae). Journal of Economic Entomology, 104, 1162–1166.
Russell, V.L. (2016) Least-squares means: the R Package lsmeans. Journal of Statistical Software, 69, 1–33.
Ryan, G.D., Emiljanowicz, L., Wilkinson, F., Kornya, M. and Newman, J.A. (2016) Thermal tolerances of the spotted-wing drosophila Drosophila suzukii. Journal of Economic Entomology, 109, 746–752.
Takano, S.I. (2014) Survival of Bactrocera latifrons (Diptera: Tephritidae) adults under constant and fluctuating low temperatures. Applied Entomology and Zoology, 49, 411–419.
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.
Torson, A.S., Yocum, G.D., Rinehart, J.P., Nash, S.A., Kvidera, K.M. and Bowsher, J.H. (2017) Physiological responses to fluctuating temperatures are characterized by distinct transcriptional profiles in a solitary bee. Journal of Experimental Biology, 220, 3372–3380.
Venables, W.N. and Ripley, B.D. (2002) Modern Applied Statistics with S. 4th edn. Springer, New York.
Walsh, D.B., Bolda, M.P., Goodhue, R.E., Dreves, A.J. and Lee, J.C. (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.
Yocum, G.D., Greenlee, K.J., Rinehart, J.P., Bennett, M.M. and Kemp, W.P. (2011) Cyclic CO2 emissions during the high temperature pulse of fluctuating thermal regime in eye-pigmented pupae of Megachile rotundata. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 160, 480–485.
Yocum, G.D., Rinehart, J.P. and Kemp, W.P. (2012) Duration and frequency of a high temperature pulse affect survival of emergence-ready Megachile rotundata (Hymenoptera: Megachilidae) during low-temperature incubation. Journal of Economical Entomology, 105, 14–19.
Yocum, G.D., Žďárek, J., Joplin, K.H., Lee, R.E. Jr, Smith, D.C., Manter, K.D. et al. (1994) Alteration of the eclosion rhythm and eclosion behavior in the flesh fly, Sarcophaga crassipalpis, by low and high temperature stress. Journal of Insect Physiology, 40, 13–21.
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.
Zhang, W., Chang, X.Q., Hoffmann, A., Zhang, S. and Ma, C.S. (2015) Impact of hot events at different developmental stages of a moth: the closer to adult stage, the less reproductive output. Scientific Reports, 5, 10436.
