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Journal of Pest Science

, Volume 93, Issue 1, pp 477–489 | Cite as

Dietary methoprene enhances sexual competitiveness of sterile male Queensland fruit flies in field cages

  • Saleh Mohammad AdnanEmail author
  • Iffat Farhana
  • Jess Inskeep
  • Polychronis Rempoulakis
  • Phillip W. Taylor
Original Paper

Abstract

Queensland fruit flies Bactrocera tryoni (Froggatt) have a long adult maturation phase which, together with high mortality rates, can substantially reduce number of released flies that survive to mature and contribute to sterile insect technique (SIT) programmes. This constraint on SIT can potentially be addressed by incorporating methoprene, a juvenile hormone analogue, into an adult diet of sugar and yeast hydrolysate for 2 days after emergence. Methoprene treatments have been found to accelerate sexual development of male Queensland fruit fly, resulting in increased mating propensity of 5–7-day-old males in no-choice laboratory trials. Before considering deployment of methoprene as a pre-release treatment in SIT, it is necessary to demonstrate mating competitiveness and compatibility of methoprene-treated flies under field-like conditions. In the present study, we assessed whether methoprene treatment increases ability of sterile males (5 and 7 days old) to compete with mature (wild or laboratory) males for matings with mature (wild or laboratory) females in field cages. We also investigated mating compatibility to test for sexual isolation between sterile flies and mature (wild or laboratory) fertile flies. In mating competitiveness tests, methoprene-treated males of either age outperformed mature wild or laboratory males for matings with mature wild or laboratory females, respectively. Untreated 5- and 7-day-old males were less competitive than mature wild or laboratory mature males and hence had lower relative sterility indexes. Methoprene-treated males mated earlier in the evening and continued mating for longer than untreated sterile males and mature wild or laboratory males. In mating compatibility trials, methoprene-treated males mated equally with methoprene-treated females and mature females, whereas methoprene-treated females tended to mate more often with mature males than with methoprene-treated males. However, untreated flies of both sexes exhibited substantial sexual isolation. Pairings that comprised methoprene-treated males and mature females had shorter mating latency and longer copulations than other pairings. Unlike males, methoprene-treated females did not exhibit changes in mating latency or duration. Overall, the present study supports the use of pre-release dietary methoprene treatment in Queensland fruit fly SIT.

Keywords

Juvenile hormone Mating Tephritidae Bactrocera tryoni Sterile insect technique 

Notes

Acknowledgements

This research was conducted as part of the SITplus collaborative fruit fly programme. 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. SMA and JI were supported by Macquarie University Research Excellence Scholarships.

Compliance with ethical standards

Conflict of interest

There was no conflict of interest regarding the preparation and submission of this manuscript.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Abraham S, Liendo MC, Devescovi F, Peralta PA, Yusef V, Ruiz J, Cladera JL, Vera MT, Segura DF (2013) Remating behavior in Anastrepha fraterculus (Diptera: Tephritidae) females is affected by male juvenile hormone analogue treatment but not by male sterilization. Bull Entomol Res 103:310–317CrossRefPubMedGoogle Scholar
  2. Adnan SM, Mendez V, Morelli R, Akter H, Farhana I, Taylor PW (2018) Dietary methoprene supplement promotes early sexual maturation of male Queensland fruit fly Bactrocera tryoni. J Pest Sci 91:1441–1454CrossRefGoogle Scholar
  3. Akter H, Taylor PW (2018) Sexual inhibition of female Queensland fruit flies mated by males treated with raspberry ketone supplements as immature adults. J Appl Entomol 142:380–387CrossRefGoogle Scholar
  4. Akter H, Mendez V, Morelli R, Perez J, Taylor PW (2017) Raspberry ketone supplement promotes early sexual maturation in male Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Pest Manag Sci 73:1764–1770CrossRefPubMedGoogle Scholar
  5. Aluja M, Ordano M, Teal PE, Sivinski J, García-Medel D, Anzures-Dadda A (2009) Larval feeding substrate and species significantly influence the effect of a juvenile hormone analog on sexual development/performance in four tropical tephritid flies. J Insect Physiol 55:231–242CrossRefPubMedGoogle Scholar
  6. Barnes B, Hofmeyr J, Groenewald S, Conlong D, Wohlfarter M (2015) The sterile insect technique in agricultural crops in South Africa: a metamorphosis…. but will it fly? Afr Entomol 23:1–18CrossRefGoogle Scholar
  7. Barton-Browne L (1957) The effect of light on the mating behaviour of the Queensland fruit fly, Strumeta tryoni (Frogg.). Aust J Zool 5:145–158CrossRefGoogle Scholar
  8. Benelli G, Daane KM, Canale A, Niu CY, Messing RH, Vargas RI (2014a) Sexual communication and related behaviours in Tephritidae: current knowledge and potential applications for integrated pest management. J Pest Sci 87:385–405CrossRefGoogle Scholar
  9. Benelli G, Giunti G, Canale A, Messing RH (2014b) Lek dynamics and cues evoking mating behavior in tephritid flies infesting soft fruits: implications for behavior-based control tools. Appl Entomol Zool 49:363–373CrossRefGoogle Scholar
  10. Bourtzis K, Lees RS, Hendrichs J, Vreysen MJ (2016) More than one rabbit out of the hat: radiation, transgenic and symbiont-based approaches for sustainable management of mosquito and tsetse fly populations. Acta Trop 157:115–130CrossRefPubMedGoogle Scholar
  11. Briceño D, Eberhard W, Shelly T (2007) Male courtship behavior in Ceratitis capitata (Diptera: Tephritidae) that have received aromatherapy with ginger root oil. Fla Entomol 90:175–179CrossRefGoogle Scholar
  12. Calla B, Hall B, Hou S, Geib SM (2014) A genomic perspective to assessing quality of mass-reared SIT flies used in Mediterranean fruit fly (Ceratitis capitata) eradication in California. BMC Genom 15:98CrossRefGoogle Scholar
  13. 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 99:1191–1198CrossRefGoogle Scholar
  14. Clarke AR, Powell KS, Weldon CW, Taylor PW (2011) the ecology of Bactrocera tryoni (Froggatt) (Diptera: Tephritidae): what do we know to assist pest management? Ann Appl Biol 158:26–54CrossRefGoogle Scholar
  15. Collins SR, Weldon CW, Banos C, Taylor PW (2009) Optimizing irradiation dose for sterility induction and quality of Bactrocera tryoni. J Econ Entomol 102:1791–1800CrossRefPubMedGoogle Scholar
  16. Collins SR, Pérez-Staples D, Taylor PW (2012) A role for copula duration in fertility of Queensland fruit fly females mated by irradiated and unirradiated males. J Insect Physiol 58:1406–1412CrossRefPubMedGoogle Scholar
  17. Collins SR, Reynolds OL, Taylor PW (2014) Combined effects of dietary yeast supplementation and methoprene treatment on sexual maturation of Queensland fruit fly. J Insect Physiol 61:51–57CrossRefPubMedGoogle Scholar
  18. Díaz-Fleischer F, Arredondo J, Aluja M (2009) Enriching early adult environment affects the copulation behaviour of a tephritid fly. J Exp Biol 212:2120–2127CrossRefPubMedGoogle Scholar
  19. Dominiak BC, Daniels D (2012) Review of the past and present distribution of Mediterranean fruit fly (Ceratitis capitata Wiedemann) and Queensland fruit fly (Bactrocera tryoni Froggatt) in Australia. Aust J Entomol 51:104–115CrossRefGoogle Scholar
  20. Dominiak BC, Sundaralingam S, Jiang L, Fanson BG, Collins SR, Banos C, Davies JB, Taylor PW (2014) Evaluating irradiation dose for sterility induction and quality control of mass-produced fruit fly Bactrocera tryoni (Diptera: Tephritidae). J Econ Entomol 107:1172–1178CrossRefPubMedGoogle Scholar
  21. Dyck V, Hendrichs J, Robinson A (2005) The sterile insect technique: principles and practice in area-wide integrated pest management. Springer, DordrectCrossRefGoogle Scholar
  22. Enkerlin W (2007) Guidance for packing, shipping, holding and release of sterile flies in area-wide fruit fly control programmes. FAO Plant Production and Protection. Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture. Paper 190, Rome, p 134Google Scholar
  23. Fanson BG, Taylor PW (2012) Additive and interactive effects of nutrient classes on longevity, reproduction, and diet consumption in the Queensland fruit fly (Bactrocera tryoni). J Insect Physiol 58:327–334CrossRefPubMedGoogle Scholar
  24. FAO/IAEA/USDA (2014) Product quality control for sterile mass-reared and released tephritid fruit flies, version 6.0. International Atomic Energy Agency, Vienna, pp 88–92Google Scholar
  25. Gaskin T, Futerman P, Chapman T (2002) Increased density and male–male interactions reduce male longevity in the medfly, Ceratitis capitata. Anim Behav 63:121–129CrossRefGoogle Scholar
  26. Gómez Y, Teal PEA, Pereira R (2013) Enhancing efficacy of Mexican fruit fly SIT programmes by large-scale incorporation of methoprene into pre-release diet. J Appl Entomol 137:252–259CrossRefGoogle Scholar
  27. Gómez-Simuta Y, Díaz-Fleisher F, Arredondo J, Díaz-Santiz E, Pérez-Staples D (2017) Precocious Mexican fruit fly methoprene-fed males inhibit female receptivity and perform sexually as mature males. J Appl Entomol 141:266–273CrossRefGoogle Scholar
  28. Hancock DL, Hamacek EL, Lloyd AC, Elson-Harris MM (2000) The distribution and host plants of fruit flies (Diptera: Tephritidae) in Australia. Department of Primary Industries, Queensland, Australia. Information Series Q 199067, pp 1–75Google Scholar
  29. Haq I, Cáceres C, Hendrichs J, Teal P, Wornoayporn V, Stauffer C, Robinson AS (2010a) Effects of the juvenile hormone analogue methoprene and dietary protein on male melon fly Bactrocera cucurbitae (Diptera: Tephritidae) mating success. J Insect Physiol 56:1503–1509CrossRefGoogle Scholar
  30. Haq I, Cáceres C, Hendrichs J, Teal PEA, Stauffer C, Robinson AS (2010b) Methoprene modulates the effect of diet on male melon fly, Bactrocera cucurbitae, performance at mating aggregations. Entomol Exp Appl 136:21–30CrossRefGoogle Scholar
  31. Haq I, Vreysen MJ, Cacéres C, Shelly TE, Hendrichs J (2015) Optimizing methyl-eugenol aromatherapy to maximize post treatment effects to enhance mating competitiveness of male Bactrocera carambolae (Diptera: Tephritidae). Insect Sci 22:661–669CrossRefPubMedGoogle Scholar
  32. Haq I, Cáceres C, Meza JS, Hendrichs J, Vreysen MJ (2018) Different methods of methyl eugenol application enhance the mating success of male Oriental fruit fly (Dipera: Tephritidae). Sci Rep 8:6033CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hendrichs J, Robinson A, Cayol J, Enkerlin W (2002) Medfly areawide sterile insect technique programmes for prevention, suppression or eradication: the importance of mating behavior studies. Fla Entomol 85:1–13CrossRefGoogle Scholar
  34. Itô Y, Kakinohana H, Yamagishi M, Kohama T (2003) Eradication of the melon fly, Bactrocera cucurbitae, from Okinawa, Japan, by means of the sterile insect technique, with special emphasis on the role of basic studies. J Asia Pac Entomol 6:119–129CrossRefGoogle Scholar
  35. Ji Q, Chen J, McInnis D, Guo Q (2013) The effect of methyl eugenol exposure on subsequent mating performance of sterile males of Bactrocera dorsalis. J Appl Entomol 137:238–243CrossRefGoogle Scholar
  36. Juan-Blasco M, San Andrés V, Martínez-Utrillas M, Argilés R, Pla I, Urbaneja A, Sabater-Muñoz B (2013) Alternatives to ginger root oil aromatherapy for improved mating performance of sterile Ceratitis capitata (Diptera: Tephritidae) males. J Appl Entomol 137:244–251CrossRefGoogle Scholar
  37. Kakinohana H (1994) The melon fly eradication program in Japan. In: Calkins CO, Klassen W, Liedo P (eds) Fruit flies and the sterile insect technique. CRC Press, Boca Ratoon, pp 223–236Google Scholar
  38. Khan MAM, Shuttleworth LA, Osborne T, Collins D, Gurr GM, Reynolds OL (2018) Raspberry ketone accelerates sexual maturation and improves mating performance of sterile male Queensland fruit fly, Bactrocera tryoni (Froggatt). Pest Manag Sci.  https://doi.org/10.1002/ps.5307 CrossRefGoogle Scholar
  39. Knipling RF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol 48:459–462CrossRefGoogle Scholar
  40. Krafsur ES (1998) Sterile insect technique for suppressing and eradicating insect populations: 55 years and counting. J Agric Entomol 15:303–317Google Scholar
  41. Lees RS, Gilles JR, Hendrichs J, Vreysen MJ, Bourtzis K (2015) Back to the future: the sterile insect technique against mosquito disease vectors. Curr Opin Insect Sci 10:156–162CrossRefPubMedGoogle Scholar
  42. Liendo MC, Devescovi F, Bachmann GE, Utgés ME, Abraham S, Vera MT, Lanzavecchia SB, Bouvet JP, Gómez-Cendra P, Hendrichs J, Teal PE, Cladera JL, Segura DF (2013) Precocious sexual signalling and mating in Anastrepha fraterculus (Diptera: Tephritidae) sterile males achieved through juvenile hormone treatment and protein supplements. Bull Entomol Res 103:1–13CrossRefPubMedGoogle Scholar
  43. Meats A (1998) A quality assurance measure for field survival rates of released sterile flies based on recapture rates. Gen Appl Entomol 28:39–46Google Scholar
  44. Moadeli T, Taylor PW, Ponton F (2017) High productivity gel diets for rearing of Queensland fruit fly, Bactrocera tryoni. J Pest Sci 90:507–520CrossRefGoogle Scholar
  45. Morató S, Shelly T, Rull J, Aluja M (2015) Sexual competitiveness of Anastrepha ludens (Diptera: Tephritidae) males exposed to Citrus aurantium and Citrus paradisi essential oils. J Econ Entomol 108:621–628CrossRefPubMedGoogle Scholar
  46. Munhenga G, Brooke BD, Gilles JRL, Slabbert K, Kemp A, Dandalo LC, Wood OR, Lobb LN, Govender D, Renke M, Koekemoer LL (2016) Mating competitiveness of sterile genetic sexing strain males (GAMA) under laboratory and semi-field conditions: steps towards the use of the sterile insect technique to control the major malaria vector Anopheles arabiensis in South Africa. Parasit Vectors 9:122CrossRefPubMedPubMedCentralGoogle Scholar
  47. Orankanok W, Chinvinijkul S, Thanaphum S, Sitilob P, Enkerlin WR (2007) Area-wide integrated control of oriental fruit fly Bactrocera dorsalis and guava fruit fly Bactrocera correcta in Thailand. In: Vreyson MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, Berlin, pp 517–526CrossRefGoogle Scholar
  48. Orankanok W, Chinvinijkul S, Sawatwangkhoung A, Pinkaew S, Orankanok S (2013) Methyl eugenol and pre-release diet improve mating performance of young Bactrocera dorsalis and Bactrocera correcta males. J Appl Entomol 137:200–209CrossRefGoogle Scholar
  49. Orozco-Dávila D, de Lourdes Adriano-Anaya M, Quintero-Fong L, Salvador-Figueroa M (2015) Sterility and sexual competitiveness of Tapachula-7 Anastrepha ludens males irradiated at different doses. PLoS ONE 10(8):e0135759CrossRefPubMedPubMedCentralGoogle Scholar
  50. Papadopoulos NT, Shelly TE, Niyazi N, Jang E (2006) Olfactory and behavioral mechanisms underlying enhanced mating competitiveness following exposure to ginger root oil and orange oil in males of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). J Insect Behav 19:403CrossRefGoogle Scholar
  51. Paranhos B, McInnis D, Morelli R, Castro R, Garziera L, Paranhos L, Costa K, Gava C, Costa M, Walder J (2013) Optimum dose of ginger root oil to treat sterile Mediterranean fruit fly males (Diptera: Tephritidae). J Appl Entomol 137:83–90CrossRefGoogle Scholar
  52. Pereira R, Sivinski J, Teal PEA (2009) Influence of methoprene and dietary protein on male Anastrepha suspensa (DipteraTephritidae) mating aggregations. J Insect Physiol 55:328–335CrossRefPubMedGoogle Scholar
  53. Pereira R, Sivinski J, Teal PEA (2010) Influence of a juvenile hormone analog and dietary protein on male Anastrepha suspensa (Diptera: Tephritidae) sexual success. J Econ Entomol 103:40–46CrossRefPubMedGoogle Scholar
  54. Pereira R, Teal P, Conway H, Worley J, Sivinski J (2013) Influence of methoprene and dietary protein on maturation and sexual performance of sterile Anastrepha ludens (Diptera: Tephritidae). J Appl Entomol 137:191–199CrossRefGoogle Scholar
  55. Pérez-Staples D, Prabhu V, Taylor PW (2007) Post-teneral protein feeding enhances sexual performance of Queensland fruit flies. Physiol Entomol 32:225–232CrossRefGoogle Scholar
  56. Pérez-Staples D, Harmer AMT, Collins SR, Taylor PW (2008) Potential for pre-release diet supplements to increase the sexual performance and longevity of male Queensland fruit flies. Agric For Entomol 10:255–262CrossRefGoogle Scholar
  57. Pérez-Staples D, Weldon CW, Smallridge C, Taylor PW (2009) Pre-release feeding on yeast hydrolysate enhances sexual competitiveness of sterile male Queensland fruit flies in field cages. Entomol Exp Appl 131:159–166CrossRefGoogle Scholar
  58. Pérez-Staples D, Weldon CW, Taylor PW (2011) Sex differences in developmental response to yeast hydrolysate supplements in adult Queensland fruit fly. Entomol Exp Appl 141:103–113CrossRefGoogle Scholar
  59. Qin Y, Paini DR, Wang C, Fang Y, Li Z (2015) Global establishment risk of economically important fruit fly species (Tephritidae). PLoS ONE 10:e0116424CrossRefPubMedPubMedCentralGoogle Scholar
  60. Reyes J, Carro X, Hernandez J, Méndez W, Campo C, Esquivel H, Salgado E, Enkerlin W (2007) A multi-institutional approach to create fruit fly-low prevalence and fly-free areas in Central America. In: Vreyson MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, Berlin, pp 627–640CrossRefGoogle Scholar
  61. Reynolds O, Jessup A, Dominiak B, Smallridge C, Cockington V, Penrose L, Taylor P, Collins S (2012) Enhancing emergence and release methods of the sterile insect technique (SIT) to improve market access. Report to Horticulture Australia Limited MT06049, Horticultural Australia LtdGoogle Scholar
  62. Segura DF, Cáceres C, Vera MT, Wornoayporn V, Islam A, Teal PEA, Cladera JL, Hendrichs J, Robinson AS (2009) Enhancing mating performance after juvenile hormone treatment in Anastrepha fraterculus: a differential response in males and females acts as a physiological sexing system. Entomol Exp Appl 131:75–84CrossRefGoogle Scholar
  63. Segura DF, Utges ME, Liendo MC, Rodriguez MF, Devescovi F, Vera MT, Teal PEA, Cladera JL (2013) Methoprene treatment reduces the pre-copulatory period in Anastrepha fraterculus (Diptera: Tephritidae) sterile males. J Appl Entomol 137:19–29CrossRefGoogle Scholar
  64. Shelly TE, Edu J (2008) Do methyl eugenol-fed males of the oriental fruit fly (Diptera: Tephritidae) induce female re-mating? Fla Entomol 91:388–393CrossRefGoogle Scholar
  65. Shelly TE, McInnis D, Edu J, Pahio E (2004) Aromatherapy in the Mediterranean fruit fly (Diptera: Tephritidae): sterile males exposed to ginger root oil in prerelease storage boxes display increased mating competitiveness in field-cage trials. J Econ Entomol 97:846–853CrossRefPubMedGoogle Scholar
  66. Shelly TE, Edu J, Pahio E (2005) Influence of diet and methyl eugenol on the mating success of males of the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Fla Entomol 88:307–313CrossRefGoogle Scholar
  67. Shelly TE, Edu J, Pahio E (2007) Exposure to ginger root oil decreases capture of male Mediterranean fruit flies (Diptera: Tephritidae) in trimedlure-baited traps. Proc Hawaii Entomol Soc 39:27–32Google Scholar
  68. Shelly TE, Edu J, Pahio E, Wee SL, Nishida R (2008) Re-examining the relationship between sexual maturation and age of response to methyl eugenol in males of the oriental fruit fly. Entomol Exp Appl 128:380–388CrossRefGoogle Scholar
  69. Shelly T, Rendon P, Moscoso F, Menendez R (2010a) Testing the efficacy of aromatherapy at the world’s largest eclosion facility for sterile males of the Mediterranean fruit fly (Diptera: Tephritidae). Proc Hawaii Entomol Soc 42:33–40Google Scholar
  70. Shelly TE, Edu J, McInnis D (2010b) Pre-release consumption of methyl eugenol increases the mating competitiveness of sterile males of the oriental fruit fly, Bactrocera dorsalis, in large field enclosures. J Insect Sci 10:8CrossRefPubMedPubMedCentralGoogle Scholar
  71. Shelly TE, Edu J, Nishimoto J (2013) Chilling and flight ability and mating competitiveness of sterile males of the Mediterranean fruit fly. J Appl Entomol 137(S1):11–18CrossRefGoogle Scholar
  72. Steiner E, Woods W, McInnis D, Lindsey J, Fogliani R, Soopaya R (2013) Ginger root oil increases mating competitiveness of sterile Mediterranean fruit fly (Diptera: Tephritidae) in Western Australia. J Appl Entomol 137:103–112CrossRefGoogle Scholar
  73. Taylor PW, Pérez-Staples D, Weldon CW, Collins SR, Fanson BG, Yap S, Smallridge C (2013) Post-teneral nutrition as an influence on reproductive development, sexual performance, and longevity of Queensland fruit flies. J Appl Entomol 137(S1):113–125CrossRefGoogle Scholar
  74. Teal PEA, Gómez-Simuta Y, Dueben BD, Holler TC, Olsen SR (2007) Improving the efficacy of the sterile insect technique for fruit flies by incorporation of hormone and dietary supplements into adult holding protocols. In: Vreyson MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Spinger, Dordrecht, pp 163–173CrossRefGoogle Scholar
  75. Tyschen PH, Fletcher BS (1971) Studies on the rhythm of mating in the Queensland fruit fly, Dacus tryoni. J Insect Physiol 17:2139–2156CrossRefGoogle Scholar
  76. Vera MT, Ruiz MJ, Oviedo A, Abraham S, Mendoza M, Segura DF, Kouloussis N, Willink E (2013) Fruit compounds affect male sexual success in the South American fruit fly, Anastrepha fraterculus (Diptera: Tephritidae). J Appl Entomol 137:2–10CrossRefGoogle Scholar
  77. Vijaysegaran S, Walter G, Drew R (2002) Influence of adult diet on the development of the reproductive system and mating ability of Queensland fruit fly Bactrocera tryoni (Frogratt) (Diptera: Tephritidae). J Trop Agric Food Sci 30:119–136Google Scholar
  78. Vreysen MJ, Saleh K, Mramba F, Parker A, Feldmann U, Dyck VA, Msangi A, Bouyer J (2014) Sterile insects to enhance agricultural development: the case of sustainable tsetse eradication on Unguja Island, Zanzibar, using an area-wide integrated pest management approach. PLoS Negl Trop Dis 8:e2857CrossRefPubMedPubMedCentralGoogle Scholar
  79. Weldon CW, Taylor PW (2011) Sexual development of wild and mass-reared male Queensland fruit flies in response to natural food sources. Entomol Exp Appl 139:17–24CrossRefGoogle Scholar
  80. Weldon CW, Pérez-Staples D, Taylor PW (2008) Feeding on yeast hydrolysate enhances attraction to cue-lure in Queensland fruit flies, Bactrocera tryoni. Entomol Exp Appl 129:200–209CrossRefGoogle Scholar
  81. White IM, Elson-Harris MM (1992) Fruit flies of economic significance: their identification and bionomics. CAB International, WallingfordGoogle Scholar
  82. Yuval B, Maor M, Levy K, Kaspi R, Taylor P, Shelly T (2007) Breakfast of champions or kiss of death? Survival and sexual performance of protein-fed, sterile Mediterranean fruit flies (Diptera: Tephritidae). Fla Entomol 90:115–122CrossRefGoogle Scholar
  83. Zervas GA, Economopoulos AP (1982) Mating frequency in caged populations of wild and artificially reared (normal or gamma-sterilized) olive fruit flies, Dacus oleae (Gmelin) (Diptera:Tepritidae). Environ Entomol 11:17–20CrossRefGoogle Scholar
  84. Zhang D, Lees RS, Xi Z, Gilles JR, Bourtzis K (2015) Combining the sterile insect technique with Wolbachia-based approaches: II-a safer approach to Aedes albopictus population suppression programmes, designed to minimize the consequences of inadvertent female release. PLoS ONE 10:e0135194CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesMacquarie UniversityNorth Ryde, SydneyAustralia
  2. 2.Biosecurity and Food SafetyNSW Department of Primary IndustriesGosfordAustralia

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