Abstract
Several tephritid fruit flies have explosive population growth and a wide host range, resulting in some of the largest impacts on horticultural crops, reducing marketable produce, and limiting market access. For these pests, early detection and eradication are routinely implemented in vulnerable areas. However, social and consumer concerns can limit the types of population management tools available for fruit fly incursion responses. Deterministic population models were used to compare eradication tools used at typical densities alone and in combination against the Queensland fruit fly (‘Qfly’), Bactrocera tryoni. The models suggested that tools that prevent egg laying are likely to be most effective at reducing populations. Tools that induced mortality once Qfly was sexually mature only slowed population growth, as successful mating still occurred. Release of sterile Qfly when using the sterile insect technique (SIT) interferes with the successful mating of wild flies, and of the tools investigated here, SIT caused the greatest reduction in the population at the prescribed release rate. Used in tandem with SIT, protein baits slightly improved the rate of population reduction, but the male annihilation technique (MAT) almost nullified control by SIT due to the mortality induced on sterile flies. The model suggested that the most rapid decrease in population size would be achieved by SIT plus protein baits. However, the model predicted both the SIT and protein baits when used alone would result in population reduction. The MAT can be used prior to SIT release to increase overflooding ratios.
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References
Andrewartha HG, Monro J, Richardson NL (1967) The use of sterile males to control populations of Queensland fruit fly, Dacus tryoni (Frogg.) (Diptera. Tephritidae). II field experiments in New South Wales. Aust J Zool 15:475–499
Anon (1996) Code of practice for the management of Queensland fruit fly. In: standing committee on agriculture and resource management. Department of Primary Industries, Canberra
Balagawi S, Jackson K, Hamacek EL, Clark AR (2012) Spatial and temporal foraging patterns of Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), for protein and implications for management. Aust J Entomol 51:279–288
Balagawi S, Jackson K, Ul Haq I, Hood-Nowotny R, Resch C, Clarke AR (2014) Nutritional status and the foraging behaviour of Bactrocera tryoni with particular reference to protein bait spray. Physiol Entomol 39:33–43
Barclay HJ (1987) Combining methods of pest control: complementarity of methods and a guiding principle. Nat Resour Model 2:299–323
Barclay HJ (2005) Mathematical models for the use of sterile insects. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique. Principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 147–174
Barclay HJ, Chao L (1991) Combining methods of pest control: minimizing cost during the control program. Theor Popul Biol 40:105–123
Barclay HJ, Hendrichs J (2014a) Modeling trapping of fruit flies for detection, supression, or eradication. In: Trapping and the detection, control, and regulation of tephritid fruit flies: lures, area-wide programs, and trade implications. Springer, Dordrecht, pp 457–492, (e-Book)
Barclay HJ, Hendrichs J (2014b) Models for assessing the male annihilation of Bactrocera spp. with methyl eugenol baits. Ann Entomol Soc Am 107:81–96
Barton Browne L (1956) The effect of light on the fecundity of the Queensland fruit fly Strumeta tryoni (Frogg.). Aust J Zool 4:125–145
Bateman MA (1967) Adaptations to temperature in geographic races of the Queensland fruit fly Dacus (Strumeta) tryoni. Aust J Zool 15:1141–1161
Bateman MA, Sonleitner FJ (1967) The ecology of a natural population of the Queensland fruit fly, Dacus tryoni: I. the parameters of the pupal and adult populations during a single season. Aust J Zool 15:303–335
Berec L, Angulo E, Courchamp F (2007) Multiple Allee effects and population management. Trends Ecol Evol 22:185–191
Blackwood JC, Berec L, Yamanaka T, Epanchin-Niell RS, Hastings A, Liebhold AM (2012) Bioeconomic synergy between tactics for insect eradication in the presence of Allee effects. Proc R Soc Biol Sci Ser B 279:2807–2815
Brockerhoff EG, Liebhold AM, Richardson B, Suckling DM (2010) Eradication of invasive forest insects: concept, methods, costs and benefits. N Z J For 40:S117–S135
Byers JA, Castle SJ (2005) Areawide models comparing synchronous versus asynchronous treatments for control of dispersing insect pests. J Econ Entomol 98:1763–1773
Cacho OJ, Hester S, Spring D (2007) Applying search theory to determine the feasibility of eradicating an invasive population in natural environments. Aust J Agric Resour Econ 51:425–443
Carpenter JE, Bloem S, Hofmeyr JH (2004) Acceptability and suitability of eggs of false codling moth (Lepidoptera: Tortricidae) from irradiated parents to parasitism by Trichogrammatoidea cryptophlebiae (Hymenoptera: Trichogrammatidae). Biol Control 30:351–359
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
Collins SR, Weldon CW, Banos C, Taylor PW (2008) Effects of irradiation dose rate on quality and sterility of Queensland fruit flies, Bactrocera tryoni (Froggatt). J Appl Entomol 132:398–405
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
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 58:1406–1412
Cossentine JE, Jensen LBM (2000) Releases of Trichogramma platneri (Hymenoptera: Trichogrammatidae) in apple orchards under a sterile codling moth release program. Biol Control 18:179–186
De Roos AM, Diekmann O, Metz JAJ (1992) Studying the dynamics of structured population models: a versatile technique and its application to Daphnia. Am Nat 139:123–147
Dominiak BC, Ekman JH (2013) The rise and demise of control options for fruit fly in Australia. Crop Protect 51:57–67
Dominiak BC, Nicol HI (2010) Field performance of Lynfield and McPhail traps for monitoring male and female sterile Bactrocera tryoni (Froggatt) and wild Dacus newmani (Perkins). Pest Manag Sci 66:741–744
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 23:131–135
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 107:1172–1178
Elkinton JS, Parry D, Boettner GH (2006) Implicating an introduced generalist parasitoid in the invasive browntail moth’s enigmatic demise. Ecology 87:2664–2672
El-Sayed AM, Suckling DM, Byers JA, Jang EB, Wearing CH (2009) Potential of “lure and kill” in long-term pest management and eradication of invasive species. J Econ Entomol 102:815–835
Epanchin-Niell RS, Haight RG, Berec L, Kean JM, Liebhold AM (2012) Optimal surveillance and eradication of invasive species in heterogeneous landscapes. Ecol Lett 15:803–812
Epsky ND, Espinoza HR, Kendra PE, Abernathy R, Midgarden D, Heath RR (2010) Effective sampling range of a synthetic protein-based attractant for Ceratitis capitata (Diptera: Tephritidae). J Econ Entomol 103:1886–1895
Ero MM, Hamacek E, Clarke AR (2011) Foraging behaviours of Diachasmimorpha kraussii (Fullaway) (Hymenoptera: Braconidae) and its host Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) in a nectarine (Prunus persica (L.) Batsch var. nectarina (Aiton) Maxim) orchard. Aust J Entomol 50:234–240
Fitt GP (1990) Comparative fecundity clutch size ovariole number and egg size of Dacus tryoni and D. jarvisi, and their relationship to body size. Entomol Exp Appl 55:11–21
Fletcher BS (1974) The ecology of a natural population of the Queensland fruit fly, Dacus tryoni. VI. seasonal changes in fruit fly numbers in the areas surrounding the orchard. Aust J Zool 22:353–363
Florec V, Sadler RJ, White B, Dominiak BC (2013) Choosing the battles: the economics of area wide pest management for Queensland fruit fly. Food Pol 38:203–213
Gamble JC, Payne T, Small B (2010) Interviews with New Zealand community stakeholders regarding acceptability of current or potential pest eradication technologies. N Z J Crop Hortic Sci 38:57–68
Gascoigne J, Berec L, Gregory S, Courchamp F (2009) Dangerously few liaisons: a review of mate-finding Allee effects. Popul Ecol 51:355–372
HIAL (2016) Horticulture Innovation Australia Limited. SITplus partnership. http://horticulture.com.au/how-we-invest-2/sitplus-partnership/. Accessed 28 May 2016
Jessup AJ, Dominiak B, Woods B, De Lima CPF, Thomkins A, Smallridge C (2007) Area wide management of fruit flies in Australia. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, Dordrecht, pp 685–697
Kagbadouno MS, Camara M, Bouyer J, Courtin F, Onikoyamou MF, Schofield CJ, Solano P (2011) Progress towards the eradication of Tsetse from the Loos islands, Guinea. Parasit Vectors 4: Article 18
Kean JM (2015) The effective sampling area of traps: estimation and application. In: Beresford RM, Froud KJ, Kean JM, Worner SP (eds) The plant protection data toolbox. New Zealand Plant Protection Society Inc, Christchurch, pp 67–76
Kean JM, Suckling DM, Stringer LD, Woods B (2011) Modeling the sterile insect technique for suppression of the light brown apple moth (Lepidoptera: Tortricidae). J Econ Entomol 104:1462–1475
Kean JM, Suckling DM, Sullivan NJ, Tobin PC, Stringer LD, Smith GR, Lee DC, Flores Vargas R, Fletcher J, Macbeth F, McCullough DG, Herms DA, Kimber B (2017) Global eradication and response database http://b3.net.nz/gerda/index.php. Accessed 24 May 2017
Knipling EF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol 48:459–462
Kumaran N, Hayes RA, Clarke AR (2014) Cuelure but not zingerone make the sex pheromone of male Bactrocera tryoni (Tephritidae: Diptera) more attractive to females. J Insect Physiol 68:36–43
Kuno E (1978) Simple mathematical models to describe the rate of mating in insect populations. Res Popul Ecol 20:50–60
Kuris AM (2003) Did biological control cause extinction of the coconut moth, Levuana iridescens. Fiji? Biol Invasions 5:133–141
Lloyd A, Smith D, Hamacek E, Kopittke R, Pinese B, De Lima F, Broughton S, Jessup A, MacDonald J, Mangan B, Moreno D, Downard P, Cross S, Papacek D (2003) Improved protein bait formulations for fruit fly control. Report to HAL 00012. Horticultural Australia Ltd., Sydney
Lloyd AC, Hamacek EL, Kopittke RA, Peek T, Wyatt PM, Neale CJ, Eelkema M, Gu HN (2010) Area-wide management of fruit flies (Diptera: Tephritidae) in the Central Burnett district of Queensland, Australia. Crop Protect 29:462–469
Mahat K, Drew RAI (2015) Evaluation of protein bait laced with various insecticides on the Queensland fruit fly (Diptera: Tephritidae): attraction, feeding, mortality and bait persistence. In: Peña L, Sabater-Muñoz B, Navarro L, Morena P (eds) XII International Citrus Congress - International Society of Citriculture, 18–23 November 2012, Valencia, 2015. Acta Horticulturae, pp 1041–1048
Meats A (1984) Thermal constraints to successful development of the Queensland fruit-fly in regimes of constant and fluctuating temperature. Entomol Exp Appl 36:55–59
Meats A (1998) Predicting or interpreting trap catches resulting from natural propagules or releases of sterile fruit flies. An actuarial and dispersal model tested with data on Bactrocera tryoni. Gen Appl Entomol 28:29–38
Meats A, Edgerton JE (2008) Short- and long-range dispersal of the Queensland fruit fly, Bactrocera tryoni and its relevance to invasive potential, sterile insect technique and surveillance trapping. Aust J Exp Agric 48:1237–1245
Meats A, Clift AD, 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. Gen Appl Entomol 31:53–58
Meats AW, Duthie R, Clift AD, Dominiak BC (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 Exp Agric 43:389–395
Morrison SA, Macdonald N, Walker K, Lozier L, Shaw MR (2007) Facing the dilemma at eradication’s end: uncertainty of absence and the Lazarus effect. Front Ecol Environ 5:271–276
Myers K (1952) Oviposition and mating behaviour of the Queensland fruit-fly (Dacus (Strumeta) tryoni (Frogg.)) and the Solanum fruit-fly (Dacus (Strumeta) cacuminatus (Hering)). Aust J Sci Res B 5:264–281
Papadopoulos NT, Katsoyannos BI, Carey JR, Kouloussis NA (2001) Seasonal and annual occurrence of the Mediterranean fruit fly (Diptera: Tephritidae) in northern Greece. Ann Entomol Soc Am 94:41–50
Perez-Staples D, Harmer AMT, Taylor PW (2007a) Sperm storage and utilization in female Queensland fruit flies (Bactrocera tryoni). Physiol Entomol 32:127–135
Perez-Staples D, Prabhu V, Taylor PW (2007b) Post-teneral protein feeding enhances sexual performance of Queensland fruit flies. Physiol Entomol 32:225–232
Piñero JC, Enkerlin W, Epsky ND (2014) Recent developments and applications of bait stations for integrated pest management of tephritid fruit flies. In: Shelly T, Epsky N, Jang EB, Reyes-Flores J, Vargas R (eds) Trapping and the detection, control, and regulation of tephritid fruit flies: lures, area-wide programs, and trade implications. Springer, Dordrecht, pp 457–492, (e-book)
Radhakrishnan P, Taylor PW (2007) Seminal fluids mediate sexual inhibition and short copula duration in mated female Queensland fruit flies. J Insect Physiol 53:741–745
Radhakrishnan P, Taylor PW (2008) Ability of male Queensland fruit flies to inhibit receptivity in multiple mates, and the associated recovery of accessory glands. J Insect Physiol 54:421–428
Radhakrishnan P, Perez-Staples D, Weldon CW, Taylor PW (2009) Multiple mating and sperm depletion in male Queensland fruit flies: effects on female remating behaviour. Anim Behav 78:839–846
Reynolds OL, 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 Ltd., Sydney
Rolfe J, Windle J (2014) Public preferences for controlling an invasive species in public and private spaces. Land Use Policy 41:1–10
Shelly TE, Edu J, McInnis D (2010) 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 10:8
Suckling DM, Barrington AM, Chhagan A, Stephens AEA, Burnip GM, Charles JG, Wee SL (2007) Eradication of the Australian painted apple moth Teia anartoides in New Zealand: trapping, inherited sterility, and male competitiveness. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, Dordrecht, pp 603–615
Suckling DM, Woods B, Mitchell VJ, Twidle AM, Lacey I, Jang EB, Wallace AR (2011) Mobile mating disruption of light-brown apple moths using pheromone-treated sterile Mediterranean fruit flies. Pest Manag Sci 67:1004–1014
Suckling DM, Tobin PC, McCullough DG, Herms DA (2012) Combining tactics to exploit Allee effects for eradication of alien insect populations. J Econ Entomol 105:1–13
Suckling DM, Kean JM, Stringer LD, Cáceres-Barrios C, Hendrichs J, Reyes-Flores J, Dominiak BC (2016) Eradication of tephritid fruit fly pest populations: outcomes and prospects. Pest Manag Sci 72:456–465
Tobin PC (2015) Ecological consequences of pathogen and insect invasions. Curr For Rep 1:25–32
Tobin PC, Berec L, Liebhold AM (2011) Exploiting Allee effects for managing biological invasions. Ecol Lett 14:615–624
Turchin P, Odendaal FJ (1996) Measuring the effective sampling area of a pheromone trap for monitoring population density of southern pine beetle (Coleoptera: Scolytidae). Environ Entomol 25:582–588
Vargas RI, Piñero JC, Mau RFL, Jang EB, Klungness LM, McInnis DO, Harris EB, McQuate GT, Bautista RC, Wong L (2010) Area-wide suppression of the Mediterranean fruit fly, Ceratitis capitata, and the Oriental fruit fly, Bactrocera dorsalis, in Kamuela, Hawaii. J Insect Sci 10:Article 135
Weldon C, Meats A (2007) Short-range dispersal of recently emerged males and females of Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) monitored by sticky sphere traps baited with protein and Lynfield traps baited with cue-lure. Aust J Entomol 46:160–166
Weldon C, Meats A (2010) Dispersal of mass-reared sterile, laboratory-domesticated and wild male Queensland fruit flies. J Appl Entomol 134:16–25
Weldon CW, Perez-Staples D, Taylor PW (2008) Feeding on yeast hydrolysate enhances attraction to cue-lure in Queensland fruit flies, Bactrocera tryoni. Entomol Exp Appl 129:200–209
Yonow T, Zalucki MP, Sutherst RW, Dominiak BC, Maywald GF, Maelzer DA, Kriticos DJ (2004) Modelling the population dynamics of the Queensland fruit fly, Bactrocera (Dacus) tryoni: a cohort-based approach incorporating the effects of weather. Ecol Model 173:9–30
Zamek AL, Spinner JE, Micallef JL, Gurr GM, Reynolds OL (2012) Parasitoids of Queensland fruit fly Bactrocera tryoni in Australia and prospects for improved biological control. Insects 3:1056–1083
Acknowledgements
This project, HG13034, has been funded by Horticulture Innovation Australia Limited with co-investment from The New Zealand Institute for Plant and Food Research Limited and funds from the Australian Government. We thank the Better Border Biosecurity collaboration (http://www.b3nz.org), Andrew Jessup for providing unpublished reports, and Howard Wearing, Alistair Hall, Tony Clarke, Hazel Parry and two anonymous reviewers for greatly improving an earlier draft of the manuscript and model assumptions, Donna Gibson for enhancing figure 1 and Megan Gee for literature support.
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LDS, JMK, JRB and DMS conceived the research. LDS and JMK developed the model. LDS prepared the manuscript and JMK, JRB and DMS edited the manuscript. All authors read and approved the manuscript.
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Stringer, L.D., Kean, J.M., Beggs, J.R. et al. Management and eradication options for Queensland fruit fly. Popul Ecol 59, 259–273 (2017). https://doi.org/10.1007/s10144-017-0593-2
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DOI: https://doi.org/10.1007/s10144-017-0593-2