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Reduced quality of sterile Queensland fruit fly following post-production stress from hypoxia, irradiation and vibration

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Abstract

The sterile insect technique (SIT), a benign pest control strategy, is currently undergoing a substantial renewal for controlling the Queensland fruit fly (Q-fly), a major horticultural pest in Australia. Production and delivery of high-quality flies is fundamental to effective SIT. While efforts are commonly made to improve production at a factory level (both quantity and quality), the methods and conditions during post-production operations also need to be tuned to minimize reductions in fly quality. Hypoxia, irradiation and vibration are important stressors that are experienced by pupae during production, packing and transportation. However, little is known about the impacts of such stressors on Q-fly quality. We conducted two laboratory experiments to investigate the response of Q-fly to such post-production stressors, with the aim of then developing guidelines that minimize quality reductions for SIT programs. In Experiment 1, Q-fly pupae of different ages (3, 6 or 9-day old) were exposed to vibrations for 5, 30, 60 and 300 s. Flight ability tests revealed that 6- and 9-day-old pupae were the most sensitive to vibration, with significant reduction in emergence and percentage of fliers. In Experiment 2, the effect of hypoxia, irradiation and vibration, in isolation or in combination, was evaluated on 9-day-old pupae. Irradiation and vibration exhibited a multiplicative negative effect on flight ability parameters. It is recommended not to subject pupae to intense or extensive vibration during the late pupal stage and to avoid prolonged periods of hypoxia.

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Data availability

The datasets generated during the current study are available from the corresponding author on reasonable request.

References

  • Allinghi A, Calcagno G, Petit-Marty N, Cendra PG, Segura D, Vera T, Cladera J, Gramajo C, Willink E, Vilardi JC (2007) Compatibility and competitiveness of a laboratory strain of Anastrepha fraterculus (Diptera: Tephritidae) after irradiation treatment. Fla Entomol 90:27–33

    Google Scholar 

  • Arredondo J, Ruiz L, Hernández E, Montoya P, Díaz-Fleischer F (2016) Comparison of Anastrepha ludens (Diptera: Tephritidae) bisexual and genetic sexing (Tapachula-7) strains: effect of hypoxia, fly density, chilling period, and food type on fly quality. J Econ Entomol 109:572–579

    CAS  PubMed  Google Scholar 

  • Arredondo J, Ruiz L, Montoya P, Díaz-Fleischer F (2018) Packing and postirradiation handling of the Anastrepha ludens (Diptera: Tephritidae) Tapachula-7 genetic sexing strain: combined effects of hypoxia, pupal size, and temperature on adult quality. J Econ Entomol 111:570–574

    PubMed  Google Scholar 

  • Bakri A, Mehta K, Lance DR (2005) Sterilizing insects with ionising radiation. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide pest management. Springer, Dordrecht, pp 233–268

    Google Scholar 

  • Balock JW, Burditt AK Jr, Christenson LD (1963) Effects of gamma radiation on various stages of three fruit fly species. J Econ Entomol 56:42–46

    Google Scholar 

  • Barry JD, McInnis DO, Gates D, Morse JG (2003) Effects of irradiation on Mediterranean fruit flies (Diptera: Tephritidae): emergence, survivorship, lure attraction, and mating competition. J Econ Entomol 96:615–622

    PubMed  Google Scholar 

  • Biosecurity Tasmania (2018) Biosecurity Alert: Queensland fruit fly detection in Tasmania 2018. Department of Primary Industries, Parks, Water and Environment

  • Blomefield T, Carpenter JE, 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. J Econ Entomol 104:814–822

    CAS  PubMed  Google Scholar 

  • Boardman L, Sørensen JG, Koštál V, Šimek P, Terblanche JS (2016) Chilling slows anaerobic metabolism to improve anoxia tolerance of insects. Metabolomics 12:176

    Google Scholar 

  • Cáceres C, Rendón P, Jessup AJ (2012) The FAO/IAEA spreadsheet for designing and operation of insect mass rearing facilities. Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture

  • Calcagno GE, Manso F, Vilardi JC (2002) Comparison of mating performance of medfly (Diptera: Tephritidae) genetic sexing and wild type strains: field cage and video recording experiments. Fla Entomol 85:41–51

    Google Scholar 

  • Calkins CO, Chambers DL, Boller EF (1982) Quality control of fruit flies in a sterile insect release programme. International Atomic Energy Agency (IAEA), Vienna

    Google Scholar 

  • Campbell AJ, Bowman G, Dominiak BC, Barchia IM, Mudford EM (2008) Comparison of loose and bagged eclosion methods at varying pupal densities for the production of adult sterile Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Gen Appl Entomol 37:7–11

    Google Scholar 

  • Campbell AJ, Lynch AJ, Dominiak B, Nicol H (2009) Effects of radiation, dye, day of larval hopping and vibration on eclosion of Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Gen Appl Entomol 38:49–53

    Google Scholar 

  • Chang CL, Vargas RI, Cáceres C, Jang E, Cho IK (2006) Development and assessment of a liquid larval diet for Bactrocera dorsalis (Diptera: Tephritidae). Ann Entomol Soc Am 99:1191–1198

    Google Scholar 

  • Clarke AR, Powell KS, Weldon CW, Taylor PW (2011) The ecology of Bactrocera tryoni (Diptera: Tephritidae): what do we know to assist pest management? Ann Appl Biol 158:26–54

    Google Scholar 

  • Collins SR, Taylor PW (2010) Flight ability procedures for mass-reared Queensland fruit flies, Bactrocera tryoni: an assessment of some variations. Entomol Exp Appl 136:308–311

    Google Scholar 

  • Collins SR, Taylor PW (2011) Fecundity, fertility and reproductive recovery of irradiated Queensland fruit fly Bactrocera tryoni. Physiol Entomol 36:247–252

    Google Scholar 

  • Collins SR, Weldon CW, Banos C, Taylor PW (2009) Optimizing irradiation dose for sterility induction and quality of Bactrocera tryoni. J Econ Entomol 102:1791–1800

    CAS  PubMed  Google Scholar 

  • Dominiak BC (2019) Components of a systems approach for the management of Queensland fruit fly Bactrocera tryoni (Froggatt) in a post dimethoate fenthion era. Crop Prot 116:56–67

    Google Scholar 

  • Dominiak BC, Ekman JH (2013) The rise and demise of control options for fruit fly in Australia. Crop Prot 51:57–67

    CAS  Google Scholar 

  • Dominiak BC, Mapson R (2017) Revised distribution of Bactrocera tryoni in eastern Australia and effect on possible incursions of Mediterranean fruit fly: development of Australia’s eastern trading block. J Econ Entomol 110:2459–2465

    PubMed  Google Scholar 

  • Dominiak BC, Sundaralingam S, Jessup AJ, Barchia IM (2002) Pupal weight as a key indicator for quality of mass produced adult Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) in 1997/1998. Gen Appl Entomol 31:17–24

    Google Scholar 

  • Dominiak BC, Campbell AJ, Barchia IM (2007a) Changes in emergence parameters as a result of transporting sterile Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) pupae. Gen Appl Entomol 36:7–10

    Google Scholar 

  • Dominiak B, Sundaralingam S, Jiang L, Jessup A, Barchia I (2007b) Quality parameters of mass production adult Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) in 1998/1999. Plant Prot Q 22:59–61

    Google Scholar 

  • Dominiak BC, Sundaralingam S, Jiang L, Jessup AJ, Nicol HI (2010) Impact of marking dye, transport and irradiation on eclosion of mass produced Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Plant Prot Q 25:141–143

    Google Scholar 

  • Dominiak B, Sundaralingam S, Jiang L, Nicol H (2011) Effect of conditions in sealed plastic bags on eclosion of mass-reared Queensland fruit fly, Bactrocera tryoni. Entomol Exp Appl 141:123–128

    Google Scholar 

  • Dyck VA, Hendrichs J, Robinson AS (2005) Sterile insect technique: principles and practice in area-wide integrated pest management. Springer, Dordrecht

    Google Scholar 

  • Enkerlin WR (2005) Impact of fruit fly control programmes using the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide pest management. Springer, Dordrecht, pp 651–676

    Google Scholar 

  • Fanson BG, Sundaralingam S, Jiang L, Dominiak BC, D'arcy G (2014) A review of 16 years of quality control parameters at a mass-rearing facility producing Queensland fruit fly, Bactrocera tryoni. Entomol Exp Appl 151:152–159

    Google Scholar 

  • FAO/IAEA/USDA (2014) Product quality control for sterile mass-reared and released tephritid fruit flies, Version 6.0. International Atomic Energy Agency, Vienna

    Google Scholar 

  • Fisher K (1996) Queensland fruit fly (Bactrocera tryoni): eradication from Western Australia. In: McPheron BA, Steck GJ (eds) Fruit fly pests, a world assessment of their biology and management. St. Lucie Press, Delray Beach, pp 535–541

    Google Scholar 

  • Fisher K (1997) Irradiation effects in air and in nitrogen on Mediterranean fruit fly (Diptera: Tephritidae) pupae in Western Australia. J Econ Entomol 90:1609–1614

    Google Scholar 

  • Gallardo-Ortiz U, Pérez-Staples D, Liedo P, Toledo J (2018) Sexual competitiveness, field survival, and dispersal of Anastrepha obliqua (Diptera: Tephritidae) fruit flies irradiated at different doses. J Econ Entomol 111:761–769

    PubMed  Google Scholar 

  • Gilchrist AS, Sved JA, Meats A (2004) Genetic relations between outbreaks of the Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), in Adelaide in 2000 and 2002. Aust J Entomol 43:157–163

    Google Scholar 

  • Harrison JF, Greenlee KJ, Verberk WC (2018) Functional hypoxia in insects: definition, assessment, and consequences for physiology, ecology, and evolution. Annu Rev Entomol 63:303–325

    CAS  PubMed  Google Scholar 

  • Hooper GHS (1975) Sterilization of Dacus cucumis French (Diptera: Tephritidae) by gamma radiation: I. Effect of dose on fertility, survival and competitiveness. Aust J Entomol 14:81–87

    Google Scholar 

  • Klassen W (2005) Area-wide integrated pest management and the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide pest management. Springer, Dordrecht, pp 39–68

    Google Scholar 

  • Knipling EF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol 48:459–462

    Google Scholar 

  • Langley PA, Maly H, Ruhm F (1972) Application of the sterility principle for the control of the Mediterranean fruit fly (Ceratitis capitata): pupal metabolism in relation to mass-rearing techniques. Entomol Exp Appl 15:23–34

    Google Scholar 

  • López-Martínez G, 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. J Exp Biol 215:2150–2161

    PubMed  Google Scholar 

  • López-Martínez G, Carpenter JE, Hight SD, Hahn DA (2014) Low-oxygen atmospheric treatment improves the performance of irradiation-sterilized male cactus moths used in SIT. J Econ Entomol 107:185–197

    PubMed  Google Scholar 

  • Lux SA, Vilardi JC, Liedo P, Gaggl K, Calcagno GE, Munyiri FN, Vera MT, Manso F (2002) Effects of irradiation on the courtship behavior of medfly (Diptera, Tephritidae) mass reared for the sterile insect technique. Fla Entomol 85:102–113

    Google Scholar 

  • Moadeli T, Taylor PW, Ponton F (2017) High productivity gel diets for rearing of Queensland fruit fly, Bactrocera tryoni. J Pest Sci 90:507–520

    Google Scholar 

  • Nestel D, Nemny-Lavy E, Islam SM, Wornoayporn V, Cáceres C (2007) Effects of pre-irradiation conditioning of medfly pupae (Diptera: Tephritidae): hypoxia and quality of sterile males. Fla Entomol 90:80–87

    Google Scholar 

  • Ohinata K, Ashraf M, Harris EJ (1977) 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 70:165–168

    CAS  PubMed  Google Scholar 

  • Ozaki ET, Kobayashi RM (1981) Effects of pupal handling during laboratory rearing on adult eclosion and flight capability in three tephritid species. J Econ Entomol 74:520–525

    Google Scholar 

  • Ozaki ET, Kobayashi RM (1982) Effects of duration and intensity of sifting pupae of various ages on adult eclosion and flight capability of the Mediterranean fruit fly (Diptera: Tephritidae). J Econ Entomol 75:773–776

    Google Scholar 

  • PBCRC (2015) National fruit fly research, development and extension plan. Biosecurity Cooperative Research Centre, Bruce

    Google Scholar 

  • Pérez-Staples D, Prabhu V, Taylor PW (2007) Post-teneral protein feeding enhances sexual performance of Queensland fruit flies. Physiol Entomol 32:225–232

    Google Scholar 

  • Rathnayake DN, Lowe EC, Rempoulakis P, Herberstein ME (2019) Effect of natural predators on Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) control by Sterile Insect Technique (SIT). Pest Manag Sci. https://doi.org/10.1002/ps.5477

    Article  PubMed  Google Scholar 

  • Resilva SS, Hernández E, Obra GB (2019) Radiation sterilization of Mexican fruit fly Anastrepha ludens (Leow) based on pupal eye color. Philipp J Sci 148:45–50

    Google Scholar 

  • Rull J, Brunel O, Mendez ME (2005) Mass rearing history negatively affects mating success of male Anastrepha ludens (Diptera: Tephritidae) reared for sterile insect technique programs. J Econ Entomol 98:1510–1516

    PubMed  Google Scholar 

  • Rull J, Diaz-Fleischer F, Arredondo J (2007) Irradiation of Anastrepha ludens (Diptera: Tephritidae) revisited: optimizing sterility induction. J Econ Entomol 100:1153–1159

    PubMed  Google Scholar 

  • Rull J, Birke A, Ortega R, Montoya P, López L (2012) Quantity and safety vs. quality and performance: conflicting interests during mass rearing and transport affect the efficiency of sterile insect technique programs. Entomol Exp Appl 142:78–86

    Google Scholar 

  • Shelly T (2019) Ability of sterile males to inhibit female remating in the melon fly Zeugodacus cucurbitae (Diptera: Tephritidae). Fla Entomol 102:278–280

    Google Scholar 

  • Sutherst RW, Collyer BS, Yonow T (2000) The vulnerability of Australian horticulture to the Queensland fruit fly, Bactrocera (Dacus) tryoni, under climate change. Aust J Agric Res 51:467–480

    Google Scholar 

  • Toledo J, Rull J, Oropeza A, Hernández E, Liedo P (2004) Irradiation of Anastrepha obliqua (Diptera: Tephritidae) revisited: optimizing sterility induction. J Econ Entomol 97:383–389

    PubMed  Google Scholar 

  • ul Haq I, Abd-Alla A, Tomas US, Meza JS, Bourtzis K, Cáceres C (2019) Cryopreservation of the Mediterranean fruit fly (Diptera: Tephritidae) VIENNA 8 genetic sexing strain: no effect on large scale production of high quality sterile males for SIT applications. PLoS ONE. https://doi.org/10.1371/journal.pone.0211259

    Article  Google Scholar 

  • Vargas R, Piñero J, Leblanc L (2015) An overview of pest species of Bactrocera fruit flies (Diptera: Tephritidae) and the integration of biopesticides with other biological approaches for their management with a focus on the Pacific Region. Insects 6:297–318

    PubMed  PubMed Central  Google Scholar 

  • Vreysen MJ, Hendrichs J, Enkerlin WR (2006) The sterile insect technique as a component of sustainable area-wide integrated pest management of selected horticultural insect pests. J Fruit Ornam Plant Res 14:107–131

    Google Scholar 

  • Walder JMM, Calkins CO (1993) Effects of gamma radiation on the sterility and behavioral quality of the Caribbean fruit fly, Anastrepha suspensa (Loew) (Diptera: Tephritidae). Sci Agric 50:157–165

    Google Scholar 

  • Wimmer EA (2005) Eco-friendly insect management. Nat Biotechnol 23:432–433

    CAS  PubMed  Google Scholar 

  • Worsley PM, Dominiak BC, Gilmour AR, James DG (2008) Pilot study at Cowra of intra-town dynamics of Queensland Fruit Fly (Bactrocera tryoni (Froggatt)) populations based on trap catch data. Plant Prot Q 23:86–89

    Google Scholar 

  • Zavala-López JL, Enkerlin WR (2017) Guideline for packing, shipping, holding and release of sterile flies in area-wide fruit fly control programmes. FAO/IAEA, Rome

    Google Scholar 

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Funding

This research was conducted as part of the SIT-plus collaborative fruit fly program. Project Raising Q-fly sterile insect technique to World Standard (HG14033) is funded by the Hort Frontiers Fruit Fly Fund, part of the Hort Frontiers strategic partnership initiative developed by Hort Innovation, with co-investment from Macquarie University and contributions from the Australian Government.

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MB, BM, PWT and PR conceived and designed the experiments. MB conducted the experiments. MB and BM analyzed data. MB, BM and PWT wrote the manuscript, and all authors read and approved the manuscript.

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Correspondence to M. Benelli.

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Author Maurizio Benelli declares that he has no conflict of interest. Author Bishwo Mainali declares that he has no conflict of interest. Author Phillip W Taylor declares that he has no conflict of interest. Author Polychronis Rempoulakis declares that he has no conflict of interest.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

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Communicated by Tim Haye.

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Benelli, M., Mainali, B., Taylor, P.W. et al. Reduced quality of sterile Queensland fruit fly following post-production stress from hypoxia, irradiation and vibration. J Pest Sci 94, 473–485 (2021). https://doi.org/10.1007/s10340-020-01269-9

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  • DOI: https://doi.org/10.1007/s10340-020-01269-9

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