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Yeast hydrolysate supplementation increases field abundance and persistence of sexually mature sterile Queensland fruit fly, Bactrocera tryoni (Froggatt)

Published online by Cambridge University Press:  23 January 2014

O.L. Reynolds ,
B.A. Orchard ,
S.R. Collins  and
P.W. Taylor
O.L. Reynolds*
Affiliation:
Graham Centre for Agricultural Innovation (NSW Department of Primary Industries and Charles Sturt University), Private Bag 4008, Narellan, NSW 2567, Australia
B.A. Orchard
Affiliation:
NSW Department of Primary Industries, Private Mail Bag, Wagga Wagga, NSW 2350, Australia
S.R. Collins
Affiliation:
Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia
P.W. Taylor
Affiliation:
Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia
*
*Author for correspondence Phone: +61 2 4640 6200 Fax: +61 2 4640 6300 E-mail: olivia.reynolds@dpi.nsw.gov.au
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Abstract

The sterile insect technique (SIT) is a non-chemical approach used to control major pests from several insect families, including Tephritidae, and entails the mass-release of sterile insects that reduce fertility of wild populations. For SIT to succeed, released sterile males must mature and compete with wild males to mate with wild females. To reach sexual maturity, the Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), must obtain adequate nutrition after adult emergence; however, in current SIT programs sterile B. tryoni receive a pre-release diet that lacks key nutrients required to sustain sexual development. The chief objective of this study was to determine whether pre-release yeast hydrolysate (YH) supplements affect the persistence and abundance of sexually mature sterile male B. tryoni under field conditions. Experiments were run in outdoor cages under conditions of low and high environmental stress that differed markedly in temperature and humidity, and in the field. Under low environmental stress conditions, survival of sterile B. tryoni was monitored in cages under three diet treatments: (i) sugar only, (ii) sugar plus YH or (iii) sugar plus YH for 48 h and sugar only thereafter. Under high environmental stress conditions survival of sterile B. tryoni was monitored in cages under four diet treatments: (i) white sugar only, (ii) brown sugar only, (iii) white sugar plus YH and (iv) brown sugar plus YH. In a replicated field study, we released colour-marked sterile B. tryoni from two diet regimes, YH-supplemented or YH-deprived, and monitored abundance of sexually mature males. In the low-stress cage study, there was no effect of diet, although overall females lived longer than males. In the high stress cage study, mortality was lower for YH-fed flies than YH-deprived flies and females lived longer than males. In the field, YH supplementation resulted in higher abundance of sexually mature sterile males, with 1.2 YH-fed flies trapped for every YH-deprived fly trapped. Under field conditions, YH supplementation can increase over-flooding ratios and hence may improve the effectiveness of SIT programmes.

Keywords

DipteraTephritidaeproteindietnutritionsterile insect technique
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 2 , April 2014 , pp. 251 - 261
Copyright
Copyright © Cambridge University Press 2014 

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References

Aluja, M., Jácome, I. & Maćias-Ordóñez, R. (2001) Effect of adult nutrition on male sexual performance in four tropical fruit fly species of the genus Anastrepha (Diptera: Tephritidae). Journal of Insect Behaviour 14, 759–775.CrossRefGoogle Scholar
Ben Ami, E., Yuval, B. & Jurkevitch, E. (2010) Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. ISME Journal 4, 28–37.Google Scholar
Butler, D.G., Cullis, B.R., Gilmour, A.R. & Gogel, B.J. (2009) ASReml-R Reference Manual (Version3), Training Series QE02001. Queensland, Department of Primary Industries and Fisheries, pp. 32–33, 71.Google Scholar
Chang, C.L. (2009) Evaluation of yeasts and yeast products in larval and adult diets for the oriental fruit fly, Bactrocera dorsalis, and adult diets for the medfly, Ceratitis capitata, and the melon fly, Bactrocera curcurbitae . Journal of Insect Science 9, 9. Available online at http://insectscience.org/9.23.Google Scholar
Collins, S.R., Taylor, P.W. & Reynolds, O.L. (in press) Combined effects of dietary yeast supplementation and methoprene treatment on sexual maturation of Queensland fruit fly. Journal of Insect Physiology.Google Scholar
Collins, S.R., Weldon, C.W., Banos, C. & Taylor, P.W. (2009) Optimizing irradiation dose for sterility induction and quality of Bactrocera tryoni . Journal of Economic Entomology 102, 1791–1800.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 . Entomologia Experimentalis et Applicata 141, 123–128.Google Scholar
Dominiak, B.C., Sundaralingam, S., Jiang, L., Jessup, A.J. & Barchia, I.M. (2008) Production levels and life history traits of mass reared Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) during 1999/2002 in Australia. Plant Protection Quarterly 23, 131–135.Google Scholar
Drew, R.A.I. (1987) Behavioural strategies of fruit flies of the genus Dacus (Diptera: Tephritidae) significant in mating and host-plant relationships. Bulletin of Entomological Research 77, 73–81.Google Scholar
Drew, R.A.I. & Yuval, B. (2000) The evolution of fruit fly feeding behavior. pp. 731–750 in Aluja, M. & Norrbom, A.L. (Eds) Fruit flies (Tephritidae): Phylogeny and Evolution of Behaviour. Boca Raton, Florida, CRC Press.Google Scholar
Drew, R.A.I., Courtice, A.C. & Teakle, D.S. (1983) Bacteria as a natural source of food for adult fruit-flies (Diptera, Tephritidae). Oecologia 60, 279–284.CrossRefGoogle Scholar
Enkerlin, W.R. (2005) Impact of fruit fly control programmes using the sterile insect technique. pp. 651–676 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.Google Scholar
Fanson, B.G. & Taylor, P.W. (2012) Additive and interactive effects of nutrient classes on longevity, reproduction, and diet consumption in the Queensland fruit fly (Bactrocera tryoni). Journal of Insect Physiology 58, 327–334.Google Scholar
Faria, M.J., Pereira, R., Dellinger, T. & Teal, P.E.A. (2008) Influence of methoprene and protein on survival, maturation and sexual performance of male Ceratitis capitata (Diptera: Tephritidae). Journal of Applied Entomology 132, 812–819.Google Scholar
Fletcher, B.S. (1975) Temperature regulated changes in the ovaries of overwintering females of the Queensland fruit fly, Dacus tryoni . Australian Journal of Zoology 23, 91–102.Google Scholar
Food and Agriculture Organisation of the United Nations (FAO)/International Atomic Energy Agency (IAEA)/United States Department of Agriculture (USDA) (2003) Product Quality Control and Shipping Procedures for Sterile Mass-Reared Tephritid Fruit Flies. Version 5. Vienna, Austria, IAEA.Google Scholar
Gavriel, S., Gazit, Y. & Yuval, B. (2010) Effect of diet on survival, in the laboratory and the field, of sterile male Mediterranean fruit flies. Entomologia Experimentalis et Applicata 135, 96–104.Google Scholar
Gilchrist, S., Cameron, E.C., Sved, J.A. & Meats, A.W. (2012) Genetic consequences of domestication and mass rearing of pest fruit fly Bactrocera tryoni (Diptera: Tephritidae). Journal of Economic Entomology 105, 1051–1056.CrossRefGoogle Scholar
Hancock, D.L., Hamacek, E.L., Lloyd, A.C. & Elson-Harris, M.M. (2000) The Distribution and Host Plants of Fruit Flies (Diptera: Tephritidae) in Australia. Brisbane, Australia, DPI Publications.Google Scholar
Haq, I., Caceres, C., Hendrichs, J., Teal, P., Wornoayporn, V., Stauffer, C. & Robinson, A.S. (2010) Effects of the juvenile hormone analogue methoprene and dietary protein on male melon fly Bactrocera cucurbitae (Diptera: Tephritidae) mating success. Journal of Insect Physiology 56, 1503–1509.CrossRefGoogle Scholar
Haq, I., Ca´ceres, C., Liedo, P., Soriano, D., Jessup, A., Hendrichs, J., Teal, P.E.A. & Robinson, A.S. (2013) Effect of methoprene application, adult food and feeding duration on male melon fly starvation survival. Journal of Applied Entomology 137, 61–68.Google Scholar
Hoffmann, A.A., Hallas, R., Sinclair, C. & Partridge, L. (2001) Rapid loss of stress resistance in Drosophila melanogaster under adaptation to laboratory culture. Evolution 55, 436–438.Google Scholar
Jackman, D.J., Bailey, P., Milton-Hine, B., Perepelicia, N., Jessup, A. & Brewer, W. (1996) The Integrated Chemical and Sterile Insect Technique to Eradicate Queensland Fruit Fly at Glenside and Moana, Adelaide, South Australia. South Australia, Australia, Primary Industries, pp. 1–28.Google Scholar
Kaspi, R. & Yuval, B. (2000) Post-teneral protein feeding improves sexual competitiveness but reduces longevity of mass-reared sterile male Mediterranean fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 93, 949–955.Google Scholar
Knipling, E.F. (1955) Possibilities of insect control or eradication thought the use of sexually sterile males. Journal of Economic Entomology 48, 459–462.Google Scholar
Maor, M., Kamensky, B., Shloush, S. & Yuval, B. (2004) Effects of post-teneral diet on foraging success of sterile male Mediterranean fruit flies. Entomolgia Experimentalis et Applicata 110, 225–230.Google Scholar
Meats, A. & Khoo, K.C. (1976) The dynamics of ovarian maturation and oocyte resorption in the Queensland fruit fly, Dacus tryoni, in daily-rhythmic and constant temperature regimes. Physiological Entomology 1, 213–221.Google Scholar
Meats, A. & Leighton, S.M. (2004) Protein consumption by mated, unmated, sterile and fertile adults of the Queensland fruit fly, Bactrocera tryoni and its relation to egg production. Physiological Entomology 29, 179–182.Google Scholar
Meats, A., Clift, A.D. & Perepelicia, N. (2002) Performance of permanent and supplementary traps for Mediterranean and Queensland fruit flies in South Australia 1975–2001: comparison of male lure and food lure traps. General and Applied Entomology 31, 53–58.Google Scholar
Meats, A., Holmes, H.M. & Kelly, G.L. (2004) Laboratory application of Bactrocera tryoni (Diptera: Tephritidae) decreases mating age and increases protein consumption and number of eggs produced per milligram of protein. Bulletin of Entomological Research 94, 517–524.Google Scholar
Meats, A.W., Duthie, R., Clift, A.D. & Dominiak, B.C. (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. Australian Journal of Experimental Agriculture 43, 389–395.Google Scholar
McCullagh, P. & Nelder, J.A. (1989) Generalized Linear Models. 2nd edn. London, Chapman and Hall, pp. 106–107, 124–125.Google Scholar
McInnis, D., 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. Annals of the Entomological Society of America 87, 231–240.Google Scholar
Miyatake, T. (1997) Genetic trade-off between early fecundity and longevity in Bactrocera cucurbitae (Diptera: Tephritidae). Heredity 78, 93–100.Google Scholar
Nagel, P. & Peveling, R. (2005) Environment and the sterile insect technique. pp. 499–524 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.Google Scholar
Obra, G.B. & Resilva, S.S. (2013) Influence of adult diet and exposure to methyl eugenol in the mating performance of Bactrocera philippinensis . Journal of Applied Entomology 137, 210–216.Google Scholar
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. Journal of Applied Entomology 137, 200–209.Google Scholar
Orozco, D., Hernandez, M.R., Meza, J.S. & Quintero, J.L. (2013) Do sterile females affect the sexual performance of sterile males of Anastrepha ludens (Diptera: Tephritidae)? Journal of Applied Entomology 137, 321–326.Google Scholar
Pereira, R., Sivinski, J. & Teal, P.E.A. (2009) Influence of methoprene and dietary protein on male Anastrepha suspensa (Diptera:Tephritidae) mating aggregations. Journal of Insect Physiology 55, 328–335.CrossRefGoogle Scholar
Perepelicia, N., Black, K., Bailey, P.T., Terras, M.A., Schinagl, L. & Dominiak, B.C. (1997) The Integrated Chemical and Sterile Insect Technique to Eradicate Queensland Fruit Fly at Linden Park, Adelaide, South Australia. South Australia, Primary Industries, pp. 1–26.Google Scholar
Pérez-Staples, D., Prabhu, V. & Taylor, P.W. (2007) Post-teneral protein feeding enhances sexual performance of Queensland fruit flies. Physiological Entomology 32, 225–232.Google Scholar
Pérez-Staples, D., Harmer, A.M.T., Collins, S.R. & Taylor, P.W. (2008) Potential for pre-release diet supplements to increase the sexual performance and longevity of male Queensland fruit flies. Agricultural and Forest Entomology 10, 255–262.Google Scholar
Pérez-Staples, D., Weldon, C.W., Smallridge, C. & Taylor, P.W. (2009) Pre-release feeding on yeast hydrolysate enhances sexual competitiveness of sterile male Queensland fruit flies in field cages. Entomologia Experimentalis et Applicata 131, 159–166.Google Scholar
Pérez-Staples, D., Weldon, C.W. & Taylor, P.W. (2011) Sex differences in developmental response to yeast hydrolysate supplements in adult Queensland fruit fly. Entomologia Experimentalis et Applicata 141, 103–113.Google Scholar
Prabhu, V., Perez-Staples, D. & Taylor, P.W. (2008) Protein:carbohydrate ratios promoting sexual activity and longevity of male Queensland fruit flies. Journal of Applied Entomology 132, 575–582.Google Scholar
Pritchard, G. (1969) The ecology of a natural population of Queensland fruit fly, Dacus tryoni. II The distribution of eggs and its relation to behaviour. Australian Journal of Zoology 17, 293–311.Google Scholar
Prokopy, R.J. & Roitberg, B.D. (1989) Fruit fly foraging behaviour. pp. 293–306 in Robinson, A. & Hooper, G. (Eds) Fruit Flies: Their Biology, Natural Enemies and Control (World Crop Pests). Amsterdam, Netherlands, Elsevier Science Publishers B.V. Google Scholar
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. Journal of Economic Entomology 97, 1547–1553.Google Scholar
Reynolds, O. & van der Rijt, V. (2011). Queensland Fruit Fly – Adult Sterile Insect Technique. Standard Operating Procedure PRO 2011/01, Australia, NSW Department of Primary Industries.Google Scholar
Reynolds, O.L. & Orchard, B.A. (2011) Effect of adult chill treatments on recovery, longevity and flight ability of Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Bulletin of Entomological Research 101, 63–71.Google Scholar
Reynolds, O.L., Smallridge, C., Cockington, V. & Penrose, L.D.D. (2012) Field release of adult sterile Queensland fruit fly, Bactrocera tryoni (Froggatt): the effect of release method and location on trap recapture rates. Australian Journal of Entomology 51, 116–126.Google Scholar
Schwarz, A.J., Zambada, A., Orozco, D.H.S. & Zavala, J.L. (1985) Mass production of the Mediterranean fruit fly at Metapa, Mexico. Florida Entomologist 68, 467–477.Google Scholar
Segura, D.F., Caceres, C., Vera, M.T., Wornoayporn, V., Islam, A., Teal, P.E.A., Cladera, J.L., Hendrichs, J. & Robinson, A.S. (2009) Enhancing mating performance after juvenile hormone treatment in Anastrepha fraterculus: a differential response in males and females acts as a physiological sexing system. Entomologia Experimentalis et Applicata 131, 75–84.Google Scholar
Shelly, T.E. (2001) Exposure to alpha-copaene and alpha-copaene-containing oils enhances mating success of male Mediterranean fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 94, 497–502.CrossRefGoogle Scholar
Shelly, T.E. & Dewire, A.-L.M. (1994) Chemically mediated mating success in male Oriental fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 87, 375–382.Google Scholar
Shelly, T.E. & Edu, J. (2008) Effect of nitrogen-containing dietary supplements on the mating success of sterile males of the Mediterranean fruit fly (Diptera : Tephritidae). Florida Entomologist 91, 394–399.Google Scholar
Shelly, T.E. & Kennelly, S. (2002) Influence of male diet on male mating success and longevity and female remating in the Mediterranean fruit fly (Diptera: Tephritidae) under laboratory conditions. Florida Entomologist 85, 572–579.Google Scholar
Shelly, T.E. & McInnis, D.O. (2003) Influence of adult diet on the mating success and survival of male Mediterranean fruit flies (Diptera: Tephritidae) from two mass-rearing strains on field-caged host trees. Florida Entomologist 86, 340–344.Google Scholar
Shelly, T.E., McInnis, D.O., Pahio, E. & Edu, J. (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. Journal of Economic Entomology 97, 846–853.Google Scholar
Tan, K.H. & Nishida, R. (1995) Incorporation of raspberry ketone in the rectal glands of males of the Queensland fruit-fly, Bactrocera-tryoni Froggatt (Diptera, Tephritidae). Applied Entomology and Zoology 30, 494–497.Google Scholar
Taylor, P.W., Khan, M., Collins, S.R. & Reynolds, O.L. (2013 a) Yeast hydrolysate supplement increases starvation vulnerability of Queensland fruit fly. Physiological Entomology 38, 337–343.CrossRefGoogle Scholar
Taylor, P.W., Perez-Staples, D., Weldon, C.W., Collins, S.R., Fanson, B.G., Yap, S. & Smallridge, C. (2013 b) Post-teneral nutrition as an influence on reproductive development, sexual performance and longevity of Queensland fruit flies. Journal of Applied Entomology 137 (Suppl), 113–125.Google Scholar
Thoday, J.M., and Read, J. (1947) Effect of oxygen on the frequency of chromosome aberralions produced by X-rays. Nature 160, 608.Google Scholar
Utgés, M.E., Vilardi, J.C., Oropeza, A., Toledo, J. & Liedo, P. (2013) Pre-release diet effect on field survival and dispersal of Anastrepha ludens and Anastrepha obliqua (Diptera: Tephritidae). Journal of Applied Entomology 137, 163–177.CrossRefGoogle Scholar
Vijaysegaran, S., Walter, G.H. & Drew, R.A.I. (2002) Influence of adult diet on the development of the reproductive system and mating ability of Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Journal of Tropical Agriculture and Food Science 30, 119–136.Google Scholar
Wee, S.L., Tan, K.H. & Nishida, R. (2007) Pharmacophagy of methyl eugenol by males enhances sexual selection of Bactrocera carambolae (Diptera: Tephritidae). Journal of Chemical Ecology 33, 1272–1282.Google Scholar
Weldon, C. & Meats, A. (2010) Dispersal of mass-reared sterile, laboratory domesticated and wild male Queensland fruit flies. Journal of Applied Entomology 134, 16–25.Google Scholar
Weldon, C.W. & Taylor, P.W. (2011) Sexual development of wild and mass-reared male Queensland fruit flies in response to natural food sources. Entomologia Experimentalis et Applicata 139, 17–24.Google Scholar
Weldon, C.W., Pérez-Staples, D. & Taylor, P.W. (2008) Feeding on yeast hydrolysate enhances attraction to cue-lure in Queensland fruit flies, Bactrocera tryoni . Entomologia Experimentalis et Applicata 129, 200–209.Google Scholar
Yonow, T. & Sutherst, R.W. (1998) The geographical distribution of the Queensland fruit fly, Bactrocera (Dacus) tryoni, in relation to climate. Australian Journal of Agricultural Research 49, 935–953.Google Scholar
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