The effect of pupal cold treatment on chill-coma recovery time and reproductive success in two Drosophila suzukii (Diptera: Drosophilidae) population

Year 2025, Volume: 53 Issue: 3, 71 - 80, 01.07.2025

Ezgi Çobanoğlu , Seda Demirel , Banu Şebnem Önder

https://doi.org/10.15671/hjbc.1612422

Abstract

Drosophila suzukii (Matsumura, 1931) is an invasive species causing significant economic losses. Effective control techniques for this species fall within a broad scope of study. However, due to population-specific differences based on local adaptations, population-specific approaches in effective control are crucial for sustainability. In this study, we examined chill coma recovery time (CCRT) and reproductive success in two temperate zone D. suzukii populations, utilizing differentiated treatments involving cold exposure during both pupal and adult stages. While no significant differences were found in CCRT between populations, notable variations were observed among treatment groups and sexes. Cold treatment during the pupal stage enabled faster recovery from chill coma in adults of both populations. However, this effect exhibited variation based on population and sex. Significantly different reproductive success was noted between the control group and the Pupa + Adult and Adult cold-treated groups. In contrast to CCRT, differences in reproductive success due to cold treatment during the adult stage resulted in opposite effects in populations. These findings suggest that strategies devised for combating this species should be tailored according to the local adaptations acquired by populations.

Keywords

Cold tolerance, Drosophila suzukii, reproductive success, invasive pest.

References

• P. Pyšek, D.M. Richardson, Invasive species, environmental change and management, and health. Annu. Rev. Environ. Resour., 35 (2010) 25-55.
• M. Kenis, M.A. Auger-Rozenberg, A. Roques, L. Timms, C. Péré, M. J. Cock, J. Settele, S. Augustin, C. Lopez-Vaamonde, Ecological effects of invasive alien insects. Biol. Invasions, 11 (2009) 21-45.
• C.J.A. Bradshaw, B. Leroy, C. Bellard, D. Roiz, C. Albert, A. Fournier, M. Barbet-Massin, J.M. Salles, F. Simard, F. Courchamp, Massive yet grossly underestimated global costs of invasive insects. Nat. Commun., 7 (2016) 1-8.
• K.A. Hamby, D.E. Bellamy, J.C. Chiu, J.C. Lee, V.M. Walton, N.G. Wiman, R.M. York, A. Biondi, Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. J. Pest Sci., 89 (2016) 605-619.
• A.K. Sakai, F.W. Allendorf, J. S. Holt, D. M. Lodge, J. Molofsky, K. A. With, S. Baughman, R. J. Cabin, J. E. Cohen, N. C. Ellstrand, D. E. McCauley, P. O’Neil, I. M. Parker, J. N. Thompson, S. G. Weller, The population biology of invasive species. Annu. Rev. Ecol. Evol. Syst., 32 (2001) 305-332.
• P.M. O’Grady, R. DeSalle, Phylogeny of the Genus Drosophila. Genetics, 209 (2018) 1-25.
• D.B. Walsh, M.P. Bolda, R.E. Goodhue, A.J. Dreves, J. Lee, D.J. Bruck, V. M. Walton, S.D.O’Neal, F.G. Zalom, Drosophila suzukii (Diptera: Drosophilidae): Invasive Pest of Ripening Soft Fruit Expanding its Geographic Range and Damage Potential. J. Integr. Pest Manag., 2 (2011) G1-G7.
• J.C. Lee, H.J. Burrack, L.D. Barrantes, E.H. Beers, A.J. Dreves, K.A. Hamby, D.R. Haviland, R. Isaacs, T.A. Richardson, P.W. Shearer, C.A. Stanley, D.B. Walsh, V.M. Walton, F.G. Zalom, D.J. Bruck, Evaluation of monitoring traps for Drosophila suzukii (Diptera: Drosophilidae) in North America. J. Econ. Entomol., 105 (2012) 1350-1357.
• O. Rota-Stabelli, M. Blaxter, G. Anfora, Drosophila suzukii. Curr. Biol., 23 (2013) R8-9.
• S. Terhzaz, L. Alford, J.G. Yeoh, R. Marley, A.J. Dornan, J.A. Dow, S.A. Davies, Renal neuroendocrine control of desiccation and cold tolerance by Drosophila suzukii. Pest Manag. Sci., 74 (2018) 800-810.
• F.T. Peng, On some species of Drosophila from China. Annot. Zool. Jpn., 16 (1937) 20-27.
• Y.J. Chung, Collection of wild Drosophila on Quelpart Island, Korea. DIS, 29 (1955) 111.
• Y.S. Kang, K.W. Moon, Drosophilid Fauna of Six Regions Near the Demilitarized Zone in Korea. Korean J. Zool., 11 (1969) 65-68.
• R. Parshad, K.K. Duggal, Drosophilidae of Kashmir, India. DIS, 40 (1965) 44.
• T. Okada, New distribution records of the Drosophilids in the oriental region. Acta Dipterologica, 8 (1976) 1-8.
• F.J. Lin, H. C. Tseng, W.Y. Lee, A catalogue of the family Drosophilidae in Taiwan (Diptera). Quart. J. Taiwan Mus., 30 (1977) 345-372.
• V. S. Sidorenko, New and unrecorded species of Drosophilidae from Soviet Far East (Diptera, Brachycera). Spixiana., 15 (1992) 93-95.
• M. Amin ud Din, K. Mazhar, S. Haque, M. Ahmed, A preliminary report on Drosophila fauna of Islamabad (Capital, Pakistan). DIS, 88 (2005) 6-7.
• G. Calabria, J. Máca, G. Bächli, L. Serra, M. Pascual, First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J. Appl. Entomol., 136 (2012) 139-147.
• I. Toševski, S. Milenković, O. Krstić, A. Kosovac, M. Jakovljević, M. Mitrović, T. Cvrković, J. Jović, Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae): A new invasive pest in Serbia. Zašt. bilja, 65 (2014) 99-104.
• S. Radonjić, S. Hrncic, First Record Of Spotted Wing Drosophila Drosophila suzukii (Diptera: Drosophilidae) In Montenegro. Pestic. Phytomed., 1 (2015): 35-40.
• B.H. Labanowska, W. Piotrowski, The Spotted Wing Drosophila Drosophila suzukii (Matsumura, 1931)-Monitoring and First Records in Poland. J. Hort. Res., 23 (2015) 49-57.
• A. Orhan, R. Aslantaş, B.Ş. Önder, G. Tozlu, First record of the invasive vinegar fly Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) from eastern Turkey. Turk. J. Zool., 40 (2016) 290-293.
• M. Hauser, S. Gaimari, M. Damus, Drosophila suzukii new to North America. Fly times, 43 (2009) 12-15.
• J. Saguez, J. Lasnier, C. Vincent, First record of Drosophila suzukii in Quebec vineyards. OENO One, 47 (2013) 69-72.
• M. Deprá, J.L. Poppe, H.J. Schmitz, D.C. De Toni, V.L. Valente, The first records of the invasive pest Drosophila suzukii in the South American continent. J. Pest Sci., 87 (2014) 379-383.
• R. Lasa, E. Tadeo, Invasive Drosophilid Pests Drosophila suzukii and Zaprionus indianus (Diptera: Drosophilidae) in Veracruz, Mexico. Fla. Entomol., 98 (2015) 987-988.
• L.E. Bennardo, L.E. Kreiman, L.M. Gandini, J. Rondón, L. Turdera, J. Hurtado, E. Hasson, First record of Spotted-wing drosophila Drosophila suzukii (Diptera: Drosophilidae) In Martín García Island wildlife refuge, Argentina. Rev. Soc. Entomol. Arg., 80 (2021) 53-57.
• I. Aouari, G. Barech, M. Khaldi, First Record of the Agricultural Pest Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) in Algeria. EPPO Bulletin, 2 (2022) 471-478.
• P.J. Fernandez Iriarte, J. Balanya, M. Pascual, F. Mestres, E.R. Hasson, A. Fontdevila, L. Serra, Tracking the origin of an invasive species: Drosophila subobscura in Argentina. J. Evol. Biol., 22 (2009) 650-658.
• G. Tait, A. Grassi, F. Pfab, C.M. Crava, D.T. Dalton, R. Magarey, L. Ometto, S. Vezzulli, M.V. Rossi-Stacconi, A. Gottardello, A. Pugliese, G. Firrao, V.M. Walton, G. Anfora, Large-scale spatial dynamics of Drosophila suzukii in Trentino, Italy. J. Pest Sci., 91(2018) 1213-1224.
• O. Rota-Stabelli, L. Ometto, G. Tait, S. Ghirotto, R. Kaur, F. Drago, J. González, V.M. Walton, G. Anfora, M.V. Rossi-Stacconi, Distinct genotypes and phenotypes in European and American strains of Drosophila suzukii: implications for biology and management of an invasive organism. J. Pest Sci., 93 (2020) 77-89.
• T. Enriquez, H. Colinet, Cold acclimation triggers major transcriptional changes in Drosophila suzukii. BMC Genomics, 20 (2019) 1-17.
• D.T. Dalton, V.M. Walton, P.W. Shearer, D.B. Walsh, J. Caprile, R. Isaacs, 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 Manag. Sci., 67 (2011) 1368–1374.
• G.D. Ryan, L. Emiljanowicz, F. Wilkinson, M. Kornya, J. A. Newman, Thermal tolerances of the spotted-wing Drosophila Drosophila suzukii (Diptera: Drosophilidae). J. Econ. Entomol., 109 (2016) 746-752.
• T. Enriquez, H. Colinet, Basal tolerance to heat and cold exposure of the spotted wing Drosophila, Drosophila suzukii. PeerJ, 5 (2017) e3112.
• D. Stockton, A. Wallingford, G. Loeb, Phenotypic plasticity promotes overwintering survival in a globally invasive crop pest, Drosophila suzukii. Insects., 9 (2018) 105.
• C. Grumiaux, M.K. Andersen, H. Colinet, J. Overgaard, Fluctuating thermal regime preserves physiological homeostasis and reproductive capacity in Drosophila suzukii. J. Insect Physiol., 113 (2019) 33-41.
• M. Kimura, T. Ohtsu, T. Yoshida, T. Awasaki, F. Lin, Climatic Adaptations and Distributions in the Drosophila-Takahashii Species Subgroup (Diptera, Drosophilidae). J. Nat. Hist., 28 (1994) 401-409.
• R. Jakobs, T.D. Gariepy, B.J. Sinclair, Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii. J. Insect Physiol., 79 (2015) 1-9.
• R. Jakobs, B. Ahmadi, S. Houben, T.D. Gariepy, B.J. Sinclair, Cold tolerance of third-instar Drosophila suzukii larvae. J. Insect Physiol., 96 (2017) 45-52.
• R. J. David, P. Gibert, E. Pla, G. Petavy, D. Karan, B. Moreteau, Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster. J. Therm. Biol., 23 (1998) 291-299.
• H.A. MacMillan, B.J. Sinclair, Mechanisms underlying insect chill-coma. J. Insect Physiol., 57 (2011) 12-20.
• F.M. Norry, A.C. Scannapieco, P. Sambucetti, C.I. Bertoli & V. Loeschcke, QTL for the thermotolerance effect of heat hardening, knockdown resistance to heat and chill-coma recovery in an intercontinental set of recombinant inbred lines of Drosophila melanogaster. Mol. Ecol., 17(2008) 4570-4581.
• T. Enriquez, D. Renault, M. Charrier, H. Colinet, Cold acclimation favors metabolic stability in Drosophila suzukii. Front. Physiol., 9 (2018) 1506.
• M. De Ro, T. Enriquez, J. Bonte, N. Ebrahimi, H. Casteels, P. De Clercq, H. Colinet, Effect of starvation on the cold tolerance of adult Drosophila suzukii (Diptera: Drosophilidae). Bull. Entom. Res., 111 (2021): 694-704.
• F.A. Putero, J. Mensch, P.E. Schilman, 2023. Effect of brief exposures of anesthesia on thermotolerance and metabolic rate of the spotted-wing fly, Drosophila suzukii: Differences between sexes? J. Insect Physiol., 149 (2023) 104549.
• A.A. Hoffmann, C.M. Sgro, Climate change and evolutionary adaptation. Nature, 470 (2011) 479-485.
• S.C. Stearns, The Evolution of Life Histories, Oxford University Press, New York, USA, 1992.
• R Core Team, R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. 2021.
• D. Bates, M. Maechler, B. Bolker, S. Walker, Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw., 67 (2015) 1-48.
• J. Fox, S. Weisberg. An {R} Companion to Applied Regression, Sage Publishing, USA, 2019.
• R.V. Lenth, emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.8.4-1. https://CRAN.R-project.org/package=emmeans, 2023.
• D. Renault, O. Nedved, F. Hervant, P. Vernon, The importance of fluctuating thermal regimes for repairing chill injuries in the tropical beetle Alphitobius diaperinus (Coleoptera: Tenebrionidae) during exposure to low temperature. Physiol. Entomol., 29 (2004) 139 – 145.
• A.K. Tran, W.D. Hutchison, M.K. Asplen, Morphometric criteria to differentiate Drosophila suzukii (Diptera: Drosophilidae) seasonal morphs. PLoS One. 15 (2020) e0228780.
• S. Tochen, V.M. Walton, J.C. Lee, Impact of floral feeding on adult Drosophila suzukii survival and nutrient status. J. Pest Sci., 89 (2016) 793-802.
• R.A. Krebs, V. Loeschcke, Resistance to thermal stress in adult Drosophila buzzatii: acclimation and variation among populations. Biol. J. Linn. Soc., 56 (1995) 505-515.
• L. Stazione, F.M. Norry, P. Sambucetti, Heat-hardening effects on mating success at high temperature in Drosophila melanogaster. J. Therm. Biol., 80 (2019) 172-177.
• E.R. Everman, J.L. Delzeit, F. Kate Hunter, J.M. Gleason, T.J. Morgan, Costs of cold acclimation on survival and reproductive behavior in Drosophila melanogaster. PLoS One, 13 (2018) 1-18.