Journal of Pest Science

, Volume 91, Issue 4, pp 1441–1454 | Cite as

Dietary methoprene supplement promotes early sexual maturation of male Queensland fruit fly Bactrocera tryoni

  • Saleh Mohammad AdnanEmail author
  • Vivian Mendez
  • Renata Morelli
  • Humayra Akter
  • Iffat Farhana
  • Phillip W. Taylor
Original Paper


Sterile insect technique (SIT) is an environmentally benign pest management technique that relies on released sterile male insects mating with, and curtailing reproduction of, wild females. However, for species with high mortality rates and long adult maturation phases, a large proportion of the released insects can die before maturing and so fail to contribute to SIT. To counter this problem, inclusion of yeast hydrolysate in pre-release diets and treatment of pupae or adults with methoprene, a juvenile hormone analogue, have been investigated as means of accelerating development of some fruit flies, including Queensland fruit fly, Bactrocera tryoni (Froggatt) (‘Q-fly’). Methoprene has most often been administered topically in acetone solution, which is toxic, flammable, and impractical for operational settings. As a practical alternative, we incorporated methoprene (0, 0.05, 0.1, and 0.5%) into Q-fly adult diet of sugar only or sugar mixed with yeast hydrolysate for 2 days, and then provided sugar only for the rest of the trial period. Mating performance of males and females was tested from 4 to 30 days of age. Flies provided sugar mixed with yeast hydrolysate had increased mating propensity in comparison with flies that were provided sugar only. At all ages and for both diets, all methoprene doses increased male mating probability. Methoprene treatment did not affect copula latency of males that received yeast hydrolysate, but males that received only sugar mated earlier if they had received 0.05% methoprene. Methoprene treatment of males was also associated with longer copulations, which may affect fertility of females that later remate. Females differed from males in that methoprene treatment did not significantly affect mating probability or latency, but resembled males in that methoprene treatment resulted in longer copulations. Sex differences in response to methoprene may lead to male-biased operational sex ratio when bisex Q-fly strains are used in SIT. Yeast hydrolysate increased longevity of both males and females, but methoprene treatment did not affect longevity. Overall, findings of the present study indicate that Q-fly sexual maturation can be accelerated, and SIT might hence be enhanced, by incorporation of methoprene and yeast hydrolysate in pre-release diet.


Q-fly Tephritidae Yeast hydrolysate Sterile insect technique Development 



The authors gratefully acknowledge the assistance of staff at New South Wales Department of Primary Industries, especially Solomon Balagawi who generously provided the flies used in this study.


This study was funded by Project Raising Q-fly Sterile Insect Technique to World Standard (HG14033) 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.

Compliance with ethical standards

Conflict of interest

SMA and HA were supported by Macquarie University Research Excellence Scholarships. RM was supported by a Brazilian Government Scientists without Borders Fellowship. 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.

Supplementary material

10340_2018_1017_MOESM1_ESM.docx (987 kb)
Supplementary material 1 (DOCX 986 kb)


  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. 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
  3. 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
  4. 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
  5. 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
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. Dominiak BC, Ekman JH (2013) The rise and demise of control options for fruit fly in Australia. Crop Prot 51:57–67CrossRefGoogle Scholar
  12. Dominiak BC, McLeod LJ, Cagnacci M (2000) Review of suppression program using three ground release methods of sterile Queensland fruit fly Bactrocera tryoni (Froggatt) at Wagga Wagga, NSW, in 1996/97. Gen Appl Entomol 29:49–57Google Scholar
  13. Dominiak BC, Sundaralingam S, Jiang L, Jessup AJ, Barchia IM (2008) Production levels and life history traits of mass reared Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) during 1999/2002 in Australia. Plant Prot Q 23:131–135Google Scholar
  14. 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
  15. Dong YC, Wang ZJ, Chen ZZ, Clarke AR, Niu CY (2016) Bactrocera dorsalis male sterilization by targeted RNA interference of spermatogenesis: empowering sterile insect technique programs. Sci Rep 6:35750CrossRefPubMedPubMedCentralGoogle Scholar
  16. Drew RAI, Yuval BI (2000) The evolution of fruit fly feeding behavior. In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behaviour. CRC Press, Boca Raton, pp 731–749Google Scholar
  17. 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
  18. Fanson BG, Weldon CW, Pérez-Staples D, Simpson SJ, Taylor PW (2009) Nutrients, not caloric restriction, extend lifespan in Queensland fruit flies (Bactrocera tryoni). Aging Cell 8:514–523CrossRefPubMedGoogle Scholar
  19. 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 151:152–159CrossRefGoogle Scholar
  20. Faria M, Pereira R, Dellinger T, Teal P (2008) Influence of methoprene and protein on survival, maturation and sexual performance of male Ceratitis capitata (Diptera: Tephritidae). J Appl Entomol 132:812–819CrossRefGoogle Scholar
  21. Flatt T, Tu MP, Tatar M (2005) Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. BioEssays 27:999–1010CrossRefPubMedGoogle Scholar
  22. Gomez 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
  23. Gomez-Simuta Y, Díaz-Fleisher F, Arredondo J, Díaz-Santiz E, Perez-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
  24. 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, BrisbaneGoogle Scholar
  25. Happ GM (1992) Maturation of the male reproductive system and its endocrine regulation. Ann Rev Entomol 37:303–320CrossRefGoogle Scholar
  26. Haq I, Hendrichs J (2013) Pre-release feeding on hydrolysed yeast and methoprene treatment enhances male Bactrocera cucurbitae Coquillett (Diptera: Tephritidae) longevity. J Appl Entomol 137:99–102CrossRefGoogle Scholar
  27. 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
  28. 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
  29. Harmer AMT, Radhakrishnan P, Taylor PW (2006) Remating inhibition in female Queensland fruit flies: effects and correlates of sperm storage. J Insect Physiol 52:179–186CrossRefPubMedGoogle Scholar
  30. Hendrichs J, Prokopy RJ (1994) Food foraging behavior of frugivorous fruit flies. In: Calkins CO, Klassen W, Liedo P (eds) Fruit flies and the sterile insect technique. CRC Press, Boca Raton, pp 37–56Google Scholar
  31. 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
  32. Jacome I, Aluja M, Liedo P, Nestel D (1995) The influence of adult diet and age on lipid reserves in the tropical fruit fly Anastrepha serpentina (Diptera: Tephritidae). J Insect Physiol 41:1079–1086CrossRefGoogle Scholar
  33. 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 Raton, pp 223–236Google Scholar
  34. Kelly TJ, Adams TS, Schwartz MB, Birnbaum MJ, Rubenstein EC, Imberski RB (1987) Juvenile hormone andovarian maturation in the Diptera: a review of recent results. Insect Biochem 17:1089–1093CrossRefGoogle Scholar
  35. Knipling RF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol 48:459–462CrossRefGoogle Scholar
  36. Krafsur ES (1998) Sterile insect technique for suppressing and eradicating insect populations: 55 years and counting. J Agric Entomol 15:303–317Google Scholar
  37. Leftwich PT, Koukidou M, Rempoulakis P, Gong HF, Zacharopoulou A, Fu G, Chapman T, Economopoulos A, Vontas J, Alphey L (2014) Genetic elimination of field-cage populations of Mediterranean fruit flies. Proc R Soc B 281:20141372CrossRefPubMedGoogle Scholar
  38. Liedo P, Orozco D, Cruz-Lopez L, Quintero JL, Becerra-Perez C, del Refugio-Hernandez M, Oropeza A, Toledo J (2013) Effect of post-teneral diets on the performance of sterile Anastrepha ludens and Anastrepha obliqua fruit flies. J Appl Entomol 137:49–60CrossRefGoogle Scholar
  39. 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
  40. McInnis DO, Tam S, Grace C, Miyashita D (1994) Population suppression and sterility rates induced by variable sex ratio, sterile insect releases of Ceratitis capitata (Diptera: Tephritidae) in Hawaii. Ann Entomol Soc Am 87:231–240CrossRefGoogle Scholar
  41. 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
  42. Meats A, Leighton SM (2004) Protein consumption by mated, unmated, sterile and fertile adults of the Queensland fruit fly, Bactrocera tryoni and its relation to egg production. Physiol Entomol 29:176–182CrossRefGoogle Scholar
  43. Meats A, Duthie R, Clift A, Dominiak B (2003) Trials on variants of the Sterile Insect Technique (SIT) for suppression of populations of the Queensland fruit fly in small towns neighbouring a quarantine (exclusion) zone. Aust J of Exp Agric 4:389–395CrossRefGoogle Scholar
  44. Monro J, Osborn AW (1967) the use of sterile males to control populations of Queensland fruit fly, Dacus tryoni (Frogg) (Diptera: Tephritidae) 1. Methods of mass-rearing, transporting, irradiating and releasing sterile flies. Aust J Zool 15:461–473CrossRefGoogle Scholar
  45. Nestel D, Nemny-Lavy E, Chang CL (2004) Lipid and protein loads in pupating larvae and emerging adults as affected by the composition of Mediterranean fruit fly (Ceratitis capitata) meridic larval diets. Arch Insect Biochem Physiol 3:97–109CrossRefGoogle Scholar
  46. 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
  47. 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
  48. Papadopoulos NT, Carey JR, Katsoyannos BI, Kouloussis NA, Muller HG, Liu X (2002) Supine behaviour predicts the time to death in male Mediterranean fruitflies (Ceratitis capitata). Proc R Soc B 269:1633–1637CrossRefPubMedGoogle Scholar
  49. 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
  50. 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
  51. Pereira R, Teal P, Conway H, Worley J, Sivinski J (2013a) Influence of methoprene and dietary protein on maturation and sexual performance of sterile Anastrepha ludens (Diptera: Tephritidae). J Appl Entomol 137:191–199CrossRefGoogle Scholar
  52. Pereira R, Yuval B, Liedo P, Teal PEA, Shelly TE, McInnis DO, Hendrichs J (2013b) Improving sterile male performance in support of programmes integrating the sterile insect technique against fruit flies. J Appl Entomol 137:178–190CrossRefGoogle Scholar
  53. 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
  54. 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
  55. 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
  56. 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
  57. Prabhu V, Pérez-Staples D, Taylor PW (2008) Protein: carbohydrate ratios promoting sexual activity and longevity of male Queensland fruit flies. J Appl Entomol 132:575–582CrossRefGoogle Scholar
  58. Radhakrishnan P, Pérez-Staples D, Weldon CW, Taylor PW (2009) Multiple mating and sperm depletion in male Queensland fruit flies: effects on female remating behaviour. Anim Behav 78:839–846CrossRefGoogle Scholar
  59. Rendón P, McInnis D, Lance D, Stewart J (2004) Medfly (Diptera:Tephritidae) genetic sexing: large-scale field comparison of males-only and bisexual sterile fly releases in Guatemala. J Econ Entomol 97:1547–1553CrossRefPubMedGoogle 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 OL, van der Rijt V (2011) Sterile insect technique strategic release for the Queensland fruit fly in Australia. A manual for operations personnel. NSW Department of Primary Industries and Horticulture Australia Ltd, Sydney, p 32Google Scholar
  62. Reynolds OL, Smallridge CJ, Cockington VG, Penrose LD (2012) The effect of release method and trial site on recapture rates of adult sterile Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Aust J Entomol 51:116–126CrossRefGoogle Scholar
  63. Reynolds OL, Orchard BA, Collins SR, Taylor PW (2014) Yeast hydrolysate supplementation increases field abundance and persistence of sexually mature sterile Queensland fruit fly, Bactrocera tryoni (Froggatt). Bull Entomol Res 104:251–261CrossRefPubMedGoogle Scholar
  64. Riddiford LM (2012) How does juvenile hormone control insect metamorphosis and reproduction? Gen Comp Endocrinol 179:477–484CrossRefPubMedGoogle Scholar
  65. Ringo JM (2002) Hormonal regulation of sexual behavior in insects. Horm Brain Behav 3:93–114CrossRefGoogle Scholar
  66. 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
  67. 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
  68. 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 137:113–125CrossRefGoogle Scholar
  69. Teal PEA, Gómez-Simuta Y, Proveaux AT (2000) Mating experience and juvenile hormone enhance sexual signaling and mating in male Caribbean fruit flies. Proc Natl Acad Sci USA 97:3708–3712CrossRefPubMedGoogle Scholar
  70. 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
  71. Teal PEA, Pereira R, Segura DF, Haq I, Gómez-Simuta Y, Robinson AS, Hendrichs J (2013) Methoprene and protein supplements accelerate reproductive development and improve mating success of male tephritid flies. J Appl Entomol 137:91–98CrossRefGoogle Scholar
  72. 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
  73. Weldon CW, Meats AW (2010) Dispersal of mass-reared sterile, laboratory-domesticated and wild male Queensland fruit flies. J Appl Entomol 134:16–25CrossRefGoogle Scholar
  74. 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
  75. 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
  76. Yap S, Fanson BG, Taylor PW (2015) Mating reverses actuarial aging in female Queensland fruit flies. PLoS ONE 10(7):e0132486CrossRefPubMedPubMedCentralGoogle Scholar
  77. Yee W (2003) Effects of cherries, honeydew, and bird feces on longevity and fecundity of Rhagoletis indifferens (Diptera: Tephritidae). Environ Entomol 32:726–735CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesMacquarie UniversitySydneyAustralia

Personalised recommendations