Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T16:52:30.482Z Has data issue: false hasContentIssue false
  • English
  • Français

Hypoxia combined with chilling maintains the quality of irradiated Drosophila flies: a simulated shipment experiment

Published online by Cambridge University Press:  25 August 2021

Thomas Enriquez Open the ORCID record for Thomas Enriquez [Opens in a new window] ,
Fabiana Sassù Open the ORCID record for Fabiana Sassù [Opens in a new window] ,
Carlos Cáceres Open the ORCID record for Carlos Cáceres [Opens in a new window]  and
Hervé Colinet Open the ORCID record for Hervé Colinet [Opens in a new window]
Thomas Enriquez
Affiliation:
University of Rennes, CNRS, ECOBIO [(Ecosystèmes, biodiversité, évolution)], UMR 6553, F-35000 Rennes, France
Fabiana Sassù
Affiliation:
Insect Pest Control Section, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Wagramerstrasse 5, PO Box 100, 1400 Vienna, Austria Department of Forest and Soil Sciences, Boku, University of Natural Resources and Life Sciences, Vienna, Austria
Carlos Cáceres
Affiliation:
Insect Pest Control Section, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Wagramerstrasse 5, PO Box 100, 1400 Vienna, Austria
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

Drosophila suzukii is an invasive fruit pest in Europe and America. Females lay eggs into mature fruit that larvae consume causing important losses. Sterile insect technique (SIT) is under development to control this pest. The efficiency of this technique relies on insect quality. However, during the process from mass production to field release, several steps may compromise insect quality and therefore SIT success. Shipment of sterile insects after irradiation is a key step of SIT programmes. Generally, insects are shipped as pupae and conditions during transport need to be adapted to prevent emergence before field release, while guaranteeing insect quality. To do so, transport is usually performed under low temperature, hypoxia or a combination of both. However, the impact of multiple stressors such as irradiation followed by chilling combined with hypoxia is poorly described and has not been studied in D. suzukii. Therefore, the aim of this study was to simulate a shipment of D. suzukii pupae (irradiated or not) under different conditions (chilling combined or not with hypoxia) for various durations, and to assess consequences on emerged adults. Irradiation followed by hypoxia and/or chilling only weakly altered emergence. However, 48 h of hypoxia without chilling altered the flight ability of flies whether or not they were irradiated. Conversely, when hypoxia was combined with chilling, flight ability remained similar to that of untreated flies. The use of chilling in combination with hypoxia for 48 h could be implemented as a transportation method for SIT programme on D. suzukii.

Keywords

Drosophila suzukiiinsect qualitylow temperaturesterile insect techniquetransport
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 6 , December 2021 , pp. 645 - 657
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.)

Footnotes

*

These authors made equal contributions to the publication.

References

Andress, E, Jones, E, War, M and Shelly, T (2013) Effects of pre-release chilling on the flight ability of sterile males of the Mediterranean fruit fly (Diptera: Tephritidae). Florida Entomologist 95, 587–592.CrossRefGoogle Scholar
Anfora, G, Cini, A and Ioriatti, C (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.Google Scholar
Bellamy, DE, Sisterson, MS and Walse, SS (2013) Quantifying host potentials: indexing postharvest fresh fruits for spotted wing Drosophila, Drosophila suzukii. PLoS ONE 8, 61227.CrossRefGoogle ScholarPubMed
Benelli, M, Ponton, F and Taylor, PW (2019) Cool storage of Queensland fruit fly eggs for increased flexibility in rearing programs. Pest Management Science 75, 1056–1064.CrossRefGoogle ScholarPubMed
Berrigan, D and Partridge, L (1997) Influence of temperature and activity on the metabolic rate of adult Drosophila melanogaster. Comparative Biochemistry and Physiology. Part A, Physiology 118, 1301–1307.CrossRefGoogle ScholarPubMed
Birkenmeyer, DR and Dame, DA (1975) Storage and sexual separation of Glossina morsitans morsitans Westwood puparia. Annals of Tropical Medicine & Parasitology 69, 399–405.CrossRefGoogle ScholarPubMed
Blomefield, T, Carpenter, JE and Vreysen, MJB (2011) Quality of mass-reared Codling moth (Lepidoptera: Tortricidae) after long-distance transportation: 1. Logistics of shipping procedures and quality parameters as measured in the laboratory. Journal of Economic Entomology 104, 814–822.CrossRefGoogle ScholarPubMed
Boardman, L, Sørensen, JG, Koštál, V, Šimek, P and Terblanche, JS (2016) Chilling slows anaerobic metabolism to improve anoxia tolerance of insects. Metabolomics 12, 176.CrossRefGoogle Scholar
Cáceres, C, Hendrichs, J and Vreysen, MJB (2014) Development and improvement of rearing techniques for fruit flies (Diptera: Tephritidae) of economic importance. International Journal of Tropical Insect Science 34, S1–S12.CrossRefGoogle Scholar
Calkins, CO and Parker, AG (2005) Sterile insect quality. In Sterile Insect Technique. Dordrecht: Springer, pp. 269–296.CrossRefGoogle Scholar
Chung, H-N, Rodriguez, SD, Gonzales, KK, Vulcan, J, JJ, Cordova, Mitra, S, CG, Adams, Moses-Gonzales, N, Tam, N, JW, Cluck, GM, Attardo and Hansen, IA (2018) Toward implementation of mosquito sterile insect technique: the effect of storage conditions on survival of male Aedes aegypti mosquitoes (Diptera: Culicidae) during transport. Journal of Insect Science 18, 2.CrossRefGoogle ScholarPubMed
Colinet, H and Renault, D (2018) Similar post-stress metabolic trajectories in young and old flies. Experimental Gerontology 102, 43–50.CrossRefGoogle Scholar
Collins, SR, Weldon, CW, Banos, C and Taylor, PW (2008) Effects of irradiation dose rate on quality and sterility of Queensland fruit flies, Bactrocera tryoni (Froggatt). Journal of Applied Entomology 132, 398–405.CrossRefGoogle Scholar
Cuisance, D and Itard, J (1973) Comportement de mâles stériles de Glossina tachinoides West. lâchés dans les conditions naturelles – environs de Fort-Lamy (Tchad). I. Transport, lâchers, rythme d'activité, action sur la population sauvage. Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux 26, 55–76.Google Scholar
Culbert, NJ, Balestrino, F, Dor, A, Herranz, GS, Yamada, H, Wallner, T and Bouyer, J (2018) A rapid quality control test to foster the development of genetic control in mosquitoes. Scientific Reports 8, 1–9.CrossRefGoogle ScholarPubMed
Dalton, DT, Walton, VM, Shearer, PW, Walsh, DB, 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
Deutscher, AT, Reynolds, OL and Chapman, TA (2017) Yeast: an overlooked component of Bactrocera tryoni (Diptera: Tephritidae) larval gut microbiota. Journal of Economic Entomology 110, 298–300.Google ScholarPubMed
Diallo, S, Seck, MT, Rayaissé, JB, Fall, AG, Bassene, MD, Sall, B, Sanon, A, Vreysen, MJB, Takac, P, Parker, AG, Gimonneau, G and Bouyer, J (2019) Chilling, irradiation and transport of male Glossina palpalis gambiensis pupae: effect on the emergence, flight ability and survival. PLoS ONE 14, e0216802.CrossRefGoogle ScholarPubMed
Dyck, VA, Hendrichs, J and Robinson, AS (2005) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer.CrossRefGoogle Scholar
Enkerlin, WR and Quinlan, MM (2002) Development of an international standard to facilitate the transboundary shipment of sterile insects, In Proceedings, Symposium: 6th International Symposium on Fruit Flies of Economic Importance, pp. 6–10.Google Scholar
Enkerlin, W, Gutiérrez Ruelas, J, Pantaleon, R, Soto Litera, C, Villaseñor Cortés, A, Zavala López, J, Orozco Dávila, D, Montoya Gerardo, P, Silva Villarreal, L, Cotoc Roldán, E, Hernández López, F, Arenas Castillo, A, Castellanos Dominguez, D, Valle Mora, A, Rendón Arana, P, Cáceres Barrios, C, Midgarden, D, Villatoro, C, Lira Prera, E, Zelaya Estradé, O, Castañeda Aldana, R, López Culajay, J, Ramírez y Ramírez, F, Liedo Fernández, P, Ortíz Moreno, G, Reyes Flores, J and Hendrichs, J (2017) The Moscamed Regional Programme: review of a success story of area-wide sterile insect technique application. Entomologia Experimentalis et Applicata 164, 188–203.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, Renault, D, Charrier, M and Colinet, H (2018a) Cold acclimation favors metabolic stability in Drosophila suzukii. Frontiers in Physiology 9, 1506.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
FAO/IAEA/USDA (2014) Product quality control for sterile mass-reared and released Tephritid fruit flies, version 6.0.Google Scholar
Farnsworth, D, Hamby, KA, Bolda, M, Goodhue, RE, Williams, JC and Zalom, FG (2017) Economic analysis of revenue losses and control costs associated with the spotted wing Drosophila, Drosophila suzukii (Matsumura), in the California raspberry industry. Pest Management Science 73, 1083–1090.CrossRefGoogle Scholar
Feala, JD, Coquin, L, McCulloch, AD and Paternostro, G (2007) Flexibility in energy metabolism supports hypoxia tolerance in Drosophila flight muscle: metabolomic and computational systems analysis. Molecular Systems Biology 3, 99.CrossRefGoogle ScholarPubMed
Frazier, MR, Woods, HA and Harrison, JF (2001) Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiological and Biochemical Zoology 74, 641–650.CrossRefGoogle ScholarPubMed
Guzy, RD, Hoyos, B, Robin, E, Chen, H, Liu, L, Mansfield, KD, Simon, MC, Hammerling, U and Schumacker, PT (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metabolism 1, 401–408.CrossRefGoogle ScholarPubMed
Haddad, GG, Sun, Y-A, Wyman, RJ and Xu, T (1997) Genetic basis of tolerance to O2 deprivation in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 94, 10809–10812.CrossRefGoogle ScholarPubMed
Hermes-Lima, M and Zenteno-Savín, T (2002) Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 133, 537–556.Google ScholarPubMed
Hoback, WW and Stanley, DW (2001) Insects in hypoxia. Journal of Insect Physiology 47, 533–542.CrossRefGoogle ScholarPubMed
Ioriatti, C, Guzzon, R, Anfora, G, Ghidoni, F, Mazzoni, V, Villegas, TR, Dalton, DT and Walton, VM (2018) Drosophila suzukii (Diptera: Drosophilidae) contributes to the development of sour rot in grape. Journal of Economic Entomology 111, 283–292.CrossRefGoogle ScholarPubMed
Jaffe, BD and Guédot, C (2019) Vertical and temporal distribution of spotted-wing Drosophila (Drosophila suzukii) and pollinators within cultivated raspberries. Pest Management Science 75, 2188–2194.CrossRefGoogle ScholarPubMed
Kakinohana, H, Kuba, H, Kohama, T, Kinjo, K, Taniguchi, M, Nakamori, H, Tanahara, A and Sokei, Y (1997) Eradication of the melon fly, Bactrocera cucurbitae Coquillett, by mass release of sterile flies in Okinawa prefecture, Japan. Japan Agricultural Research Quarterly 31, 91–100.Google Scholar
Klassen, W and Curtis, CF (2005) History of the sterile insect technique. In Dyck, VA, Hendrichs, J and Robinson, AS (eds), Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht: Springer, pp. 3–36.CrossRefGoogle Scholar
Knipling, EF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. Journal of Economic Entomology 48, 459–462.CrossRefGoogle Scholar
Krüger, AP, Schlesener, DCH, Martins, LN, Wollmann, J, Deprá, M and Garcia, FRM (2018a) Effects of irradiation dose on sterility induction and quality parameters of Drosophila suzukii (Diptera: Drosophilidae). Journal of Economic Entomology 111, 741–746.CrossRefGoogle Scholar
Krüger, AP, Schlesener, DCH, Martins, LN, Wollmann, J, Deprá, M and Garcia, FRM (2018b) Radiation effects on Drosophila suzukii (Diptera: Drosophilidae) reproductive behaviour. Journal of Applied Entomology 143, 88–94.CrossRefGoogle Scholar
Lanouette, G, Brodeur, J, Fournier, F, Martel, V, Vreysen, M, Cáceres, C and Firlej, A (2017) The sterile insect technique for the management of the spotted wing Drosophila, Drosophila suzukii: establishing the optimum irradiation dose. PLoS ONE 12, e0180821.CrossRefGoogle ScholarPubMed
Lee, JC, Dreves, AJ, Cave, AM, Kawai, S, Isaacs, R, Miller, J, Van Timmeren, S and Bruck, DJ (2015) Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Annals of the Entomological Society of America 108, 117–129.CrossRefGoogle Scholar
Lee, JC, Wang, X, Daane, KM, Hoelmer, KA, Isaacs, R, Sial, A and Walton, VM (2019) Biological control of spotted-wing Drosophila (Diptera: Drosophilidae) – current and pending tactics. Journal of Integrated Pest Management 10, 13.CrossRefGoogle Scholar
Lees, RS, Gilles, JR, Hendrichs, J, Vreysen, MJ and Bourtzis, K (2015) Back to the future: the sterile insect technique against mosquito disease vectors. Current Opinion in Insect Science 10, 156–162.CrossRefGoogle ScholarPubMed
López-Martínez, G and Hahn, DA (2012) Short-term anoxic conditioning hormesis boosts antioxidant defenses, lowers oxidative damage following irradiation and enhances male sexual performance in the Caribbean fruit fly, Anastrepha suspensa. Journal of Experimental Biology 215, 2150–2161.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
Melicher, D, Wilson, ES, Bowsher, JH, Peterson, SS, Yocum, GD and Rinehart, JP (2019) Long-distance transportation causes temperature stress in the Honeybee, Apis mellifera (Hymenoptera: Apidae). Environmental Entomology 48, 691–701.CrossRefGoogle Scholar
Mitsui, H, Takahashi, KH and Kimura, MT (2006) Spatial distributions and clutch sizes of Drosophila species ovipositing on cherry fruits of different stages. Population Ecology 48, 233–237.CrossRefGoogle Scholar
Mutika, GN, Opiyo, E and Robinson, AS (2002) Effect of low temperature treatment on the quality male adult Glossina pallidipes (Diptera: Glossinidae) relation to the sterile insect technique. Entomological Science 5, 209–214.Google Scholar
Mutika, GN, Kabore, I, Parker, AG and Vreysen, MJ (2014) Storage of male Glossina palpalis gambiensis pupae at low temperature: effect on emergence, mating and survival. Parasites & Vectors 7, 465.CrossRefGoogle ScholarPubMed
Nikolouli, K, Colinet, H, Renault, D, Enriquez, T, Mouton, L, Gibert, P, Sassu, F, Cáceres, C, Stauffer, C, Pereira, R and Bourtzis, K (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.CrossRefGoogle ScholarPubMed
Nikolouli, K, Sassù, F, Mouton, L, Stauffer, C and Bourtzis, K (2020) Combining sterile and incompatible insect techniques for the population suppression of Drosophila suzukii. Journal of Pest Science 93, 647–661.CrossRefGoogle ScholarPubMed
Pagabeleguem, S, Seck, MT, Sall, B, Vreysen, MJ, Gimonneau, G, Fall, AG, Bassene, M, Sidibé, I, Rayaissé, JB, Belem, AM and Bouyer, J (2015) Long distance transport of irradiated male Glossina palpalis gambiensis pupae and its impact on sterile male yield. Parasites & Vectors 8, 259.CrossRefGoogle ScholarPubMed
Powers, SK and Jackson, MJ (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiological Reviews 88, 1243–1276.CrossRefGoogle ScholarPubMed
R Core Team (2016) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Rezende, EL, Castañeda, LE and Santos, M (2014) Tolerance landscapes in thermal ecology. Functional Ecology 28(4), 799–809.CrossRefGoogle Scholar
Robergs, RA, Ghiasvand, F and Parker, D (2004) Biochemistry of exercise-induced metabolic acidosis. American Journal of Physiology – Regulatory Integrative and Comparative Physiology 287, R502–R516.CrossRefGoogle ScholarPubMed
Rombaut, A, Guilhot, R, Xuéreb, A, Benoit, L, Chapuis, MP, Gibert, P and Fellous, S (2015) Long distance transport of irradiated male Glossina palpalis gambiensis pupae and its impact on sterile male yield. Parasites & Vectors 8, 259.Google Scholar
Stacconi, M, Buffington, M, Daane, K, Dalton, D, Grassi, A, Kaçar, G, Miller, B, Miller, J, Baser, N, Ioriatti, C, Walton, V, Wiman, N, Wang, X and Anfora, G (2015) Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biological Control 84, 28–35.CrossRefGoogle Scholar
Rossi Stacconi, MV, Grassi, A, Ioriatti, C and Anfora, G (2019) Augmentative releases of Trichopria drosophilae for the suppression of early season Drosophila suzukii populations. BioControl 64, 9–19.CrossRefGoogle Scholar
Sassù, F, Nikolouli, K, Caravantes, S, Taret, G, Pereira, R, Vreysen, MJB, Stauffer, C and Cáceres, C (2019a) Mass-rearing of Drosophila suzukii for sterile insect technique application: evaluation of two oviposition systems. Insects 10, 448.CrossRefGoogle Scholar
Sassù, F, Nikolouli, K, Pereira, R, Vreysen, MJB, Stauffer, C and Cáceres, C (2019b) Irradiation dose response under hypoxia for the application of the sterile insect technique in Drosophila suzukii. PLoS ONE 14, e0226582.CrossRefGoogle Scholar
Seck, MT, Pagabeleguem, S, Bassene, MD, Fall, AG, Diouf, TA, Sall, B, Vreysen, MJ, Rayaissé, JB, Takac, P, Sidibé, I, Parker, AG, Mutika, GN, Bouyer, J and Gimonneau, G (2015) Quality of sterile male tsetse after long distance transport as chilled, irradiated pupae. PLoS Neglected Tropical Diseases 9, e0004229.CrossRefGoogle ScholarPubMed
Terblanche, JS, Klok, CJ and Chown, SL (2005) Temperature-dependence of metabolic rate in Glossina morsitans morsitans (Diptera, Glossinidae) does not vary with gender, age, feeding, pregnancy or acclimation. Journal of Insect Physiology 51, 861–870.CrossRefGoogle ScholarPubMed
Tochen, S, Dalton, DT, Wiman, N, Hamm, C, Shearer, PW and Walton, VM (2014) Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environmental Entomology 43, 501–510.CrossRefGoogle ScholarPubMed
Vance, JT, Williams, JB, Elekonich, MM and Roberts, SR (2009) The effects of age and behavioral development on Honeybee (Apis mellifera) flight performance. Journal of Experimental Biology 212, 2604–2611.CrossRefGoogle Scholar
Walsh, D, Bolda, M, Goodhue, R, Dreves, A, Lee, JC, Bruck, DJ, Walton, VM, 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
Zhao, HW and Haddad, GG (2011) Review: hypoxic and oxidative stress resistance in Drosophila melanogaster. Placenta 32, S104–S108.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Enriquez et al. supplementary material

Figure S1

Download Enriquez et al. supplementary material(Image)
Image 383 KB