Irradiation dose response under hypoxia for the application of the sterile insect technique in Drosophila suzukii


Autoři: Fabiana Sassù aff001;  Katerina Nikolouli aff001;  Rui Pereira aff002;  Marc J. B. Vreysen aff002;  Christian Stauffer aff001;  Carlos Cáceres aff002
Působiště autorů: Department of Forest and Soil Sciences, Boku, University of Natural Resources and Life Sciences, Vienna, Austria aff001;  Division of Nuclear Techniques in Food and Agriculture, Insect Pest Control Subprogramme, Joint FAO/IAEA, Vienna, Austria aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0226582

Souhrn

Treating insects with a lower oxygen atmosphere before and during exposure to radiation can mitigate some of the negative physiological effects due to the irradiation. The irradiation of pupae under oxygen-reduced environment such as hypoxia or anoxia is routinely used in the sterile insect technique (SIT) of some tephritid species as it provides radiological protection. This treatment allows to have the sterile pupae already in sealed containers facilitating the shipment. SIT is an environment friendly control tactic that could be used to manage populations of Drosophila suzukii in confined areas such as greenhouses. The objectives of this study were to assess the effect of irradiation on the reproductive sterility in D. suzukii males and females under low-oxygen atmosphere (hypoxia) and atmosphere conditions (normoxia). Additionally, we assessed the differences in radiological sensitivity of pupae treated under hypoxia and normoxia conditions. Finally, the effect on emergence rate and flight ability of the irradiated D. suzukii adults exposed to doses that induced >99% of sterility were assessed. Pupae needed a 220 Gy irradiation dose to achieve >99% of egg hatch sterility in males irrespective of the atmosphere condition. For females the same level of sterility was achieved already at 75 Gy and 90 Gy for the normoxia and hypoxia treatments, respectively. Radiation exposure at 170 and 220 Gy under the two atmosphere treatments did not have any effect on the emergence rate and flight ability of D. suzukii males and females. Therefore, hypoxia conditions can be used as part of an area-wide insect pest management program applying SIT to facilitate the protocols of packing, irradiation and shipment of sterile D. suzukii pupae.

Klíčová slova:

Animal flight – Drosophila – Fecundity – Hypoxia – Insect flight – Insect physiology – Oxygen – Pupae


Zdroje

1. Bellamy DE, Sisterson MS, Walse SS. Quantifying host potentials: indexing postharvest fresh fruits for spotted wing drosophila, Drosophila suzukii. PLoS One. 2013;8(4):61227.

2. Calabria G, Máca J, Bächli G, Serra L, Pascual M. First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol. 2012;136(1–2):139–47.

3. Mitsui H, Takahashi KH, Kimura MT. Spatial distributions and clutch sizes of Drosophila species ovipositing on cherry fruits of different stages. Popul Ecol. 2006;48(3):233–7.

4. Ioriatti C, Guzzon R, Anfora G, Ghidoni F, Mazzoni V, Villegas TR, et al. Drosophila suzukii (Diptera: Drosophilidae) contributes to the development of sour rot in grape. J Econ Entomol. 2018;111(1):283–92. doi: 10.1093/jee/tox292 29202199

5. Rombaut A, Guilhot R, Xuéreb A, Benoit L, Chapuis MP, Gibert P, et al. Invasive Drosophila suzukii facilitates Drosophila melanogaster infestation and sour rot outbreaks in the vineyards. R Soc Open Sci. 2017;4(3):170117. doi: 10.1098/rsos.170117 28405407

6. Mazzi D, Bravin E, Meraner M, Finger R, Kuske S. Economic impact of the introduction and establishment of Drosophila suzukii on sweet cherry production in Switzerland. Insects. 2017;8(1)18.

7. De Ros G, Anfora G, Grassi A, Ioriatti C. The potential economic impact of Drosophila suzukii on small fruits production in Trentino (Italy). IOBC-WPRS Bull. 2013;91:317–22.

8. Goodhue RE, Bolda M, Farnsworth D, Williams JC, Zalom FG. Spotted wing drosophila infestation of California strawberries and raspberries: Economic analysis of potential revenue losses and control costs. Pest Manag Sci. 2011;67(11):1396–402. doi: 10.1002/ps.2259 21815244

9. Benito NP, Lopes-da-Silva M, dos Santos RSS. Potential spread and economic impact of invasive Drosophila suzukii in Brazil. Pesqui Agropecu Bras. 2016;51(5):571–8.

10. Farnsworth D, Hamby KA, Bolda M, Goodhue RE, Williams JC, Zalom FG. Economic analysis of revenue losses and control costs associated with the spotted wing drosophila, Drosophila suzukii (Matsumura), in the California raspberry industry. Pest Manag Sci. 2017;73(6):1083–90. doi: 10.1002/ps.4497 27943618

11. Haye T, Girod P, Cuthbertson AGS, Wang XG, Daane KM, Hoelmer KA, et al. Current SWD IPM tactics and their practical implementation in fruit crops across different regions around the world. J Pest Sci (2004). 2016;89(3):643–51.

12. Haviland DR, Beers EH. Chemical control programs for Drosophila suzukii that comply with international limitations on pesticide residues for exported sweet cherries. J Integr Pest Manag. 2012;3(2):1–6.

13. Rossi Stacconi MV, Grassi A, Ioriatti C, Anfora G. Augmentative releases of Trichopria drosophilae for the suppression of early season Drosophila suzukii populations. BioControl. 2019;64(1):9–19.

14. Leach H, Moses J, Hanson E, Fanning P, Isaacs R. Rapid harvest schedules and fruit removal as non-chemical approaches for managing spotted wing Drosophila. J Pest Sci. 2018;91(1):219–26.

15. Snellings Y, Herrera B, Wildemann B, Beelen M, Zwarts L, Wenseleers T, et al. The role of cuticular hydrocarbons in mate recognition in Drosophila suzukii. Sci Rep. 2018;8(1):4996. doi: 10.1038/s41598-018-23189-6 29567945

16. Nikolouli K, Colinet H, Renault D, Enriquez T, Mouton L, Gibert P, et al. Sterile insect technique and Wolbachia symbiosis as potential tools for the control of the invasive species Drosophila suzukii. J Pest Sci. 2018;9(12):489–503.

17. Sial AA, Roubos CR, Gautam BK, Fanning PD, Van Timmeren S, Spies J, et al. Evaluation of organic insecticides for management of spotted-wing drosophila (Drosophila suzukii) in berry crops. J Appl Entomol. 2019;143(6):593–608.

18. Krüger AP, Schlesener DCH, Martins LN, Wollmann J, Deprá M, Garcia FRM. Effects of irradiation dose on sterility induction and quality parameters of Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol. 2018;111(2):741–6. doi: 10.1093/jee/tox349 29415132

19. Schetelig MF, Lee KZ, Otto S, Talmann L, Stökl J, Degenkolb T, et al. Environmentally sustainable pest control options for Drosophila suzukii. J Appl Entomol. 2018;142(1–2):3–17.

20. Lanouette G, Brodeur J, Fournier F, Martel V, Vreysen M, Cáceres C, et al. The sterile insect technique for the management of the spotted wing drosophila, Drosophila suzukii: Establishing the optimum irradiation dose. PLoS One. 2017;12(9).

21. Knipling EF. Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol. 1955;48(4):459–62.

22. Klassen W. Area-wide integrated pest management and the sterile insect technique. In: Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. 2005. pp. 39–68.

23. Bakri A, Mehta K, Lance DR. Sterilizing insects with ionizing radiation. In: Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. 2005. pp. 233–68.

24. Williamson DL, Mitchell S, Seo ST. Gamma irradiation of the Mediterranean fruit fly (Diptera: Tephritidae): Effects of puparial age under induced hypoxia and female sterility. Ann Entomol Soc Am. 1985;78(1):101–6.

25. Vreysen MJB, Gerardo-Abaya J, Cayol JP. Lessons from area-wide integrated pest management (AW-IPM) programmes with an SIT component: An FAO//IAEA perspective. In: Area-Wide Control of Insect Pests: From Research to Field Implementation. 2007. p. 723–44.

26. Cáceres C, McInnis D, Shelly T, Jang E, Robinson A, Hendrichs J. Quality management systems for fruit fly (Diptera: Tephritidae) sterile insect technique. Florida Entomol. 2007;90(1):1–9.

27. Cáceres C, Hendrichs J, Vreysen MJB. Development and improvement of rearing techniques for fruit flies (Diptera: Tephritidae) of economic importance. Int J Trop Insect Sci. 2014;34(S1):S1–12.

28. Willard WK, Cherry DS. Comparative radiosensitivity in the class insecta. J Theor Biol. 1975;52(1):149–58. doi: 10.1016/0022-5193(75)90046-6 1152478

29. Whitten M, Mahon R. Misconceptions and Constraints. In: Sterile Insect Technique. Berlin/Heidelberg: Springer-Verlag; 2005. pp. 601–26.

30. Arthur V, Machi A, Mastrangelo T. Ionizing radiations in entomology. In: Evolution of Ionizing Radiation Research. 2015:213–34.

31. Von Sonntag C. The chemistry of free-radical-mediated DNA damage. Basic Life Sci. 1991;58:287–321. doi: 10.1007/978-1-4684-7627-9_10 1811474

32. Mastrangelo T, Walder J. Use of radiation and isotopes in insects. In: Radioisotopes—Applications in Bio-Medical Science. 2011:67–92.

33. Nestel D, Nemny-Lavy E, Mohammad Islam S, Wornoayporn V, Cáceres C. Effect of pre-irradiation conditioning of Medfly pupae (Diptera: Tephritidae): hypoxia and quality of sterile males. Florida Entomol. 2007;90(1):80–7.

34. López-Martínez G, Hahn DA. 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. J Exp Biol. 2012;215(12):2150–61.

35. FAO/IAEA/USDA. Manual for product quality control and shipping procedures for sterile mass-reared tephritid fruit flies. 2003.

36. Fisher K. Irradiation effects in air and in nitrogen on mediterranean fruit fly (Diptera: Tephritidae) pupae in western Australia. J Econ Entomol. 1997;90(6):1609–14.

37. Hallman GJ, Hellmich RL. Modified atmosphere storage may reduce efficacy of irradiation phytosanitary treatments. In: Acta Horticulturae. 2010. pp. 159–62.

38. Deutscher AT, Reynolds OL, Chapman TA. Yeast: An overlooked component of Bactrocera tryoni (Diptera: Tephritidae) larval gut microbiota. J Econ Entomol. 2017;110(1):298–300. doi: 10.1093/jee/tow262 28039426

39. International Atomic Energy Agency. Dosimetry System for SIT—Manual for Gafchromic film. 2004. Available from: http://www-naweb.iaea.org/nafa/ipc/public/Dosimetry_SOP_v11.pdf

40. Ruhm ME, Calkins CO. Eye‐color changes in Ceratitis capitata pupae, a technique to determine pupal development. Entomol Exp Appl. 1981;29(2):237–40.

41. FAO/IAEA/USDA. Product quality control for sterile mass-reared and released tephritid fruit flies. 2014.

42. R Core Team. R Development Core Team. R: A Language and Environment for Statistical Computing. 2019.

43. Bates D, Maechler M, Bolker BM, Walker S. Fitting linear mixed-effects models using lme4}. J Stat Softw. 2015;67(1):1–48.

44. Robinson AS. Genetic basis of the sterile insect technique. In: Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. 2005. pp. 95–114.

45. Hooper GHS. The effect of ionizing radiation on reproduction. World Crop pests. 1989;(3):153–64.

46. Toledo J, Rull J, Oropeza A, Hernández E, Liedo P. Irradiation of Anastrepha obliqua (Diptera: Tephritidae) revisited: optimizing sterility induction. J Econ Entomol. 2004;97(2):383–9. doi: 10.1093/jee/97.2.383 15154459

47. Ohinata K, Ashraf M, Harris EJ. Mediterranean fruit flies: sterility and sexual competitiveness in the laboratory after treatment with gamma irradiation in air, carbon dioxide, helium, nitrogen or partial vacuum. J Econ Entomol. 1977;70(2):165–8. doi: 10.1093/jee/70.2.165 558235

48. Younes MWF, Shehata NF, Mahmoud YA. Histopathological effects of gamma irradiation on the peach fruit fly, Bactrocera zonata (Saund.) female gonads. J Appl Sci Res. 2009;5(3):305–10.

49. Nation JL, Smittle BJ, Milne K, Dykstra TM. Influence of irradiation on development of Caribbean fruit fly (Diptera: Tephritidae) larvae. Ann Entomol Soc Am. 1995;88(3):348–352.

50. IDIDAS. International Database on Insect Disinfestation and Sterilization. Available from: http://www-ididas.iaea.org/IDIDAS/start.htm. 2009.

51. Allinghi A, Calcagno G, Petit-Marty N, Gómez Cendra P, Segura D, Vera T, et al. Compatibility and competitiveness of a laboratory strain of Anastrepha fraterculus (Diptera: Tephritidae) after irradiation treatment. Florida Entomol. 2007;90(1):27–32.

52. Henneberry TJ. Effects of gamma radiation on the fertility and longevity of Drosophila melanogaster. J Econ Entomol. 1963;56(3):279–81.

53. O’Brien RD, Wolfe LS, American Institute of Biological Sciences., U.S. Atomic Energy Commission. Radiation, radioactivity, and insects: Prepared Under the Direction of the American Institute of Biological Sciences for the Division of Technical Information, United States Atomic Energy Commission. Elsevier. 1964.

54. Calkins CO, Parker AG. Sterile insect quality. In: Dyck VA, Hendrichs J, Robinson AS, editors. Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht: Springer; 2005. pp. 269–96.

55. Balock JW, Burditt AK, Christenson LD. Effects of gamma radiation on various stages of three fruit fly species. J Econ Entomol. 2015;56(1):42–6.

56. Langley PA, Curtis CF, Brady J. The viability, fertility and behaviour of tsetse flies (Glossina morsitans) sterilized by irradiation under various conditions. Entomol Exp Appl. 1974;17(1):97–111.

57. Robinson AS. Influence of anoxia during gamma irradiation on the fertility and competitiveness of the adult male codling moth, Laspeyresia pomonella (L.). Radiat Res. 2006;61(3):526.

58. Condon CH, White S, Meagher RL, Jeffers LA, Bailey WD, Hahn DA. Effects of low-oxygen environments on the radiation tolerance of the cabbage looper moth (Lepidoptera: Noctuidae). J Econ Entomol. 2017;110(1):80–6. doi: 10.1093/jee/tow273 28031469


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