Next Article in Journal
Current Status of Omics Studies Elucidating the Features of Reproductive Biology in Blood-Feeding Insects
Previous Article in Journal
The Multifaceted Effects of Short-Term Acute Hypoxia Stress: Insights into the Tolerance Mechanism of Propsilocerus akamusi (Diptera: Chironomidae)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 14
Issue 10
10.3390/insects14100801
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Biosecurity and Management Strategies for Economically Important Exotic Tephritid Fruit Fly Species in Australia

by
Jessica L. Hoskins
1,*,
Polychronis Rempoulakis
2,
Mark M. Stevens
1 and
Bernard C. Dominiak
3
1
Yanco Agricultural Institute, New South Wales Department of Primary Industries, Private Mail Bag, Yanco, NSW 2703, Australia
2
Central Coast Primary Industries Centre, New South Wales Department of Primary Industries, Locked Bag 26, Gosford, NSW 2250, Australia
3
The Ian Armstrong Building, New South Wales Department of Primary Industries, 105 Prince Street, Orange, NSW 2280, Australia
*
Author to whom correspondence should be addressed.
Insects 2023, 14(10), 801; https://doi.org/10.3390/insects14100801
Submission received: 14 August 2023 / Revised: 22 September 2023 / Accepted: 28 September 2023 / Published: 4 October 2023
(This article belongs to the Section Insect Pest and Vector Management)
Versions Notes

Abstract

:

Simple Summary

Australian horticulture is at risk from incursions by exotic tephritid fruit fly species, particularly oriental fruit fly. An incursion by exotic fruit flies is likely to result in global trade restrictions and will cause significant economic losses. In this study, we investigated global management strategies for exotic fruit fly species and compared them with available local strategies in Australia to identify areas where Australian management practices could be improved. We identified that although Australia has a good understanding of the main exotic fruit fly threats, there remains no species-specific emergency response plan available to implement in the case of an incursion. Australia has effective tools for exotic fruit fly detection, an early warning surveillance network is in place across Australia and control measures used successfully for eradication elsewhere are available in Australia. However, the speed at which Australia could respond to an incursion is currently limited by the lack of a response plan, and this could have major implications for the effectiveness of management strategies for containment and eradication, likely leading to a more severe and costly incursion outcome.

Abstract

Exotic tephritid incursions are of high concern to Australia’s biosecurity and its horticultural industries. It is vital that Australia remains ready to respond to incursions as they arise, as an incursion of tephritid fruit fly species will result in significant economic losses. In this review, we compared Australian incursion management strategies for fruit flies with global management strategies and identified possible areas where improvements could be made in an Australian context. Overall, Australia has a good understanding of the main tephritid threats, of which Bactrocera species from across the Torres Strait (northern Australia) are of most concern. Effective tools for tephritid detection and early warning surveillance at points of entry are in place at ports and in horticultural areas Australia-wide and provide the basis for initiating biosecurity responses in the event of an incursion. Area-wide control measures used in successful eradication attempts globally are available for use in Australia. However, a specific tephritid emergency response plan identifying suitable response measures and control options for species of concern is not yet available. We have identified that Australia has the policies and management tools available to respond to an exotic tephritid incursion, but the speed at which this could be accomplished would be greatly improved by the development of species-specific emergency response plans.

1. Introduction

Tephritid fruit fly species are a serious threat to global food production. Fruit fly infestations cause significant economic losses, reduce commodity quality, and disrupt trade, which in turn affects livelihoods, food security and market access [1,2]. To date, Australia remains largely free of economically damaging exotic fruit fly species, such as the Oriental fruit fly (OFF; Bactrocera dorsalis (Hendel)). This freedom from most exotic tephritids means that Australian horticultural commodities can maintain premium prices and Australian horticultural industries are worth ~AUD 15 billion annually [3]. If an incursion by exotic fruit flies were to occur, even for a short time, market access for export produce would be challenged [4] and this would result in significant economic losses [5]. As such, it is vital that Australia has good biosecurity and management strategies in place to monitor for and respond to fruit fly incursions as they arise.
At present there are five exotic fruit fly species that have been identified as biosecurity priorities for Australian horticulture: Anastrepha ludens (Loew) (Mexican fruit fly), Bactrocera carambolae (Drew & Hancock) (carambola fruit fly), Bactrocera dorsalis (Hendel) (Oriental fruit fly (OFF)) (Note that Bactrocera dorsalis is considered the senior synonym of Bactrocera papayae Drew & Hancock, Bactrocera invadens Drew, Tsuruta & White, and Bactrocera philippinesis Drew & Hancock, with Bactrocera carambolae Drew & Hancock considered a separate species included in the B. dorsalis species complex [6].), Bactrocera trivialis (Drew) (New Guinea fruit fly) and Zeugodacus cucurbitae (Coquillett) (melon fly) (see Table 1) [7]. These species were identified during the development of the National Priority Plant Pests list by the Australian Government [7]. To be considered a priority pest, exotic species must be injurious to plants/plant products, have the potential to cause significant negative effects on the economy, environment or community, and have the potential to enter, establish and spread within Australia [7].
International horticultural trade and tourism from Australia’s nearest neighbours (predominantly countries in Asia) are the most probable pathways for an incursion by these tephritid species [8,9], although wind-assisted dispersal across the Torres Strait is also significant [10,11]. Except for the Mexican fruit fly [12,13], all the above species are present in Asia. Bactrocera species (particularly OFF) are of most concern to Australia, as species in this genus have a long history of invasion and establishment globally (e.g., [14]). OFF, regarded as the most damaging and aggressive fruit fly [15], has the highest incursion risk due to its presence throughout Asia [16], invasion and establishment in Indonesia [17] and Papua New Guinea [18], and because of the historical incursion and subsequent eradication of OFF (then B. papayae) in far north Queensland, Australia in the 1990′s [19].
Here, we aim to review Australia’s capacity for preventing and managing an incursion of exotic tephritid fruit flies. Observations of the history of incursions and subsequent eradication attempts, such as the incursion of OFF into Africa [14,20] or medfly (Mediterranean fruit fly, Ceratitis capitata (Wiedemann)) into almost every continent [21,22], can assist in developing best practice management strategies for control and damage mitigation. We provide a summary of national and international tephritid fruit fly incursion management practices, a summary of the history of economically damaging fruit flies in Australia and an outline of the potential of an incursion into Australia by exotic fruit fly. The aim of this study is not to provide an extensive review of exotic fruit fly management practices, as this has, to varying degrees, already been achieved (for examples see [13,23,24,25]. Rather, it is to examine if current Australian measures are adequate to manage an incursion by exotic fruit flies and, if not, to suggest modifications that will improve Australian management practices.
Table 1. The top five exotic tephritid fruit fly species of biosecurity concern to Australia, their distribution, hosts, ideal climate and known attractants.
Table 1. The top five exotic tephritid fruit fly species of biosecurity concern to Australia, their distribution, hosts, ideal climate and known attractants.
SpeciesDistributionCommercial Host/sClimateLure
NativeInvasive
Anastrepha ludens (Loew)
Mexican fruit fly		Mexico (other areas of North America possible)United States (transient-under eradication in California and Texas) and PanamaPolyphagous. Major commercial hosts citrus and mango Tropical and warm temperateNo para-pheromone lure known but captured in traps with ammonia based lures [26,27,28,29]
Bactrocera carambolae (Drew and Hancock)
carambola fruit fly		ASIA including Malaysia, Thailand, Indonesia, Timor-Leste, Vietnam, Singapore, Myanmar, India, CambodiaFrench Guyana, Guyana (eradicated 1994), Brazil, Suriname, Brunei, BangladeshPolyphagous >100 hosts [12]. Major commercial hosts carambola, mango, jackfruit, sapodilla, guava [30]Tropical and sub-tropical [31]Methyl eugenol [30]
Bactrocera dorsalis (Hendel)
Oriental fruit fly (OFF)		Southeast Asia>75 countries in Asia, North America, South America, Africa [32] and Oceania (Christmas Island, Papua New Guinea, Palau, Hawaii and Tahiti) Polyphagous >300 cultivated fruit and vegetable host species. Most edible fruit is susceptible [12,33]. Some major hosts include mango, stone fruit, apple, citrus, cherry, carambola, cashew, banana.Tropical and warm temperateMethyl eugenol [7]
Bactrocera trivialis (Drew)
New Guinea fruit fly		Papua New Guinea and Indonesia [34] Polyphagous, recorded on 17 host plants [33]. Major commercial hosts chilli, grapefruit, mango, peach, guava [33,34]TropicalCuelure [30]
Zeugodacus cucurbitae (Coquillett)
melon fly		India>40 countries including in Africa, Asia, Oceania (Papua New Guinea, Mariana Islands, Solomon Islands, Nauru, Kiribati, Guam, Hawaii [35]). Eradicated from Japan [36] North America (California) Polyphagous but predominantly cucurbits. Recorded on 44 hosts [12,33] Main commercial hosts include watermelon, rockmelon, cucumber, pumpkin, bitter melon, edible Luffa, ivy gourd, wax gourd, bean and tomato. Tropical and warm temperateCuelure group (melolure in Hawaii) [37]
Information summarised from CABI-Invasive species compendium www.cabi.org/isc/ (accessed on 15 January 2023) where correct and Plant Health Australia Fruit fly Identification website www.fruitflyidentification.org.au (accessed on 15 January 2023) and other identified sources, most up to date and correct information used.

2. Incursion and Environmental Suitability

2.1. Incursion and Dispersal Ability

The threat of incursion exists for all countries due to increasing global trade in fruit and vegetables [32,38,39]. Frequently, tephritid incursions follow a jump-diffusion model [40] where tourism (e.g., [9]) or trade provide the long-distance jump, followed by dispersal into the local environment, often with human assistance [11]. In Australia, local human movements appear responsible for Queensland fruit fly (Qfly, Bactrocera tryoni (Froggatt)) dispersal of up to several hundred kilometers (e.g., [41]). Internationally, human movements have contributed to the dispersal of medfly to most continents [21] and the spread of OFF through most of the Pacific Islands [42].
While trade and tourism represent the most likely incursion pathways for exotic fruit flies, wind is also thought to play a role, especially in Australia. In general, the influence of wind on fruit fly dispersal is not well understood and reports are contradictory. Some indicate wind does not redistribute tephritids across land (e.g., [43]), while others provide evidence for downwind dispersal [10,44]. Mark and recapture studies show that most fruit fly species do not move far from their release sites, being limited to distances of 2–4 km [43,45] although dispersal ability appears to be largely species-specific. There are a few instances where fruit flies, particularly Bactrocera species, have dispersed large distances. OFF and Qfly have been found at distances of 50 km and 94 km, respectively, from their release sites [43,46], although most reports indicate dispersal distances of less than 1 km. Conversely, other species such as melon fly and Mexican fruit fly do not disperse aerially over significant distances. Mark and recapture studies on the melon fly have demonstrated a dispersal distance of between 50 and 800 m from release sites [47,48], while Mexican fruit flies dispersed up to 9 km, but typically traveled less than 250 m [49].
For Australia, the influence of winds on dispersal may be more important across waterways, such as the Torres Strait [10,11]. There is strong evidence that prevailing wind patterns during the Australian northern wet season (November to April) facilitate the movement of exotic tephritids from southern areas of the Papua New Guinea (PNG) mainland onto the Torres Strait Islands [18]. The closest islands, Boigu and Saibai, lie less than 6 km from PNG, with the rest of the islands spread out over 150 km between Cape York on the Australian mainland and PNG. Trapping of fruit flies conducted as part of Australia’s surveillance network on the Torres Straight Islands frequently intercepts OFF, melon fly and New Guinea fruit fly [11,18]. It is possible that wind-assisted dispersal of exotic flies to the southerly Torres Strait Islands could lead to an incursion on the Australian mainland.

2.2. Climate, Fruit Fly Ecology, Hosts, and Incursions

Climate and host availability are the two most important factors governing the establishment and spread of fruit fly species during an incursion event. Understanding the response of fruit fly species to various climate scenarios in terms of their adaptability can allow for predictions of how incursions will develop for different species. For example, OFF has a reduced capacity (lower trait plasticity) to adapt to increasing temperatures when compared to medfly [50]. This difference in trait plasticity may indicate that high temperatures will favour medflies in some locations, even though thermal tolerance to high temperatures itself is greater in OFF (e.g., medfly [51]; OFF [2]) (see Table 2 for examples). These differences in trait characteristics have applications in models attempting to forecast distributions for exotic fruit fly species, such as CLIMEX [4,52], GARP [53] or MaxEnt [54,55]. These models can be used to predict climate-dependent limitations for survival and population growth, allowing incursion surveillance measures to be focused on regions with appropriate conditions for fly population establishment.
Models, such as those previously mentioned, suggest that with increasing global temperatures tropical areas are likely to become less suitable for many fruit fly species, as temperatures will exceed thermal limits for survival. Conversely, temperate areas will become more suitable due to a reduction in unfavourable winter conditions (e.g., extreme frost events) allowing for overwintering by adults [16,56] and consequently population establishment. Within Australia, most models of climate suitability for native tephritid fruit fly species (especially those of economic importance) indicate future temperature conditions will facilitate range expansion from Queensland and northern areas of NSW into southern NSW and Victoria along the eastern seaboard and to higher elevations along the Great Dividing Range [54,57,58]. Northern Queensland is predicted to become less acceptable to many local tephritids, but potentially more acceptable to the establishment of exotic species, particularly OFF (e.g., [53,54]).
Table 2. Examples of species traits that can be used in models predicting fruit fly establishment likelihood and distribution.
Table 2. Examples of species traits that can be used in models predicting fruit fly establishment likelihood and distribution.
TraitBactrocera dorsalis * (Hendel)
Oriental Fruit Fly (OFF)		Bactrocera tryoni (Froggatt)
Queensland Fruit Fly (Qfly)		Ceratitis capitata (Wiedemann)
Mediterranean Fruit Fly (medfly)
Critical thermal limitsmin7.3 °C (larvae) [2]
9.1 °C (adults) [2]		 6 °C (adults) [51,59]
max45.23 °C (larvae) [2]
46.16 °C (adults) [2]		 42 °C (adults) [51,59]
Lethal limitslower −8 °C (larvae) [2]
−6 to −6.5 (adults) [2,50]		 −7 to −3 °C all life stages [60]
upper42 to 45 °C (adults) [2,50]38–40 °C (all life stages) [61]37 °C all life stages [60]
Developmental temperature thresholdslower8.8 °C,11.8 °C, 12.1 °C, 12 °C (eggs) [62,63,64,65]
5.6 °C, 9.4 °C, 10.5 °C (larvae) [62,63,64]
8.7 °C, 9.3 °C, 10.9 °C (pupae) [62,63,64]		12 °C (all life stages) [65]10 to 11 °C (egg) [63,66]
5 °C, 10.2 °C (larvae) [63,66,67]
9 °C (pupae) [63]
upper30 to 35 °C (all life stages) [62] 37 °C (eggs) [61,65]
35 °C (larvae) [65]
34 °C (pupae) [65]		35 °C (larvae) [2]
optimum24–30 °C (all life stages) [62,68]25–30 °C (all life stages) [61]24–27 °C (all life stages) [62,68]
* Includes data from Bactrocera dorsalis synonymy.
Despite forecasts that an area is or will be climatically suitable for range expansion by native or exotic tephritids, establishment can be limited by host availability or by interspecific competition for hosts from local fruit fly species. In an Australian context host availability alone might not be a limiting factor for establishment as the exotic tephritids in our study are polyphagous (Table 1; Table 3), i.e., OFF affects more than 250 fruits and vegetables [32], and the most likely entry points for an incursion are airports and seaports which are typically in or near capital cities and which are generally surrounded by peri-urban and food production areas with a wide variety of hosts [69].
Competition for hosts between native and exotic fruit fly species has the potential to curb the establishment of exotic species. Research [70,71] suggests that the ability of an invading species to overwhelm resident species is partly based on their reproductive capacity, or the number of adult flies produced per kg of fruit (termed the host reproduction number (HRN) [72]). OFF has frequently become the dominant tephritid species after introduction to a new country or region [42], outcompeting resident fruit fly species [2,71,73]. OFF has a high HRN in many hosts (see Table 4 for examples) and a competitive advantage over other species, which is largely due to its ability to infest unripe fruit (e.g., [74,75]). Laying eggs in unripe fruit means that OFF can often claim resources before other species [71,76]. HRNs are available for other fruit fly species (see [72] for medfly HRN), but information is limited. For Australian incursion management, a comparison of Qfly (the most economically damaging and widespread endemic fruit fly species) and exotic fruit fly HRN values would be beneficial to increase the accuracy of determining the invasion and establishment potential of exotic fruit fly taxa [77]. A caveat to this is that in certain locations such as northern Australia, especially in island habitats, host type may be very limited. In these areas, the benefits of using HRN for optimising fruit fly management may also be limited, especially in areas where hosts are similar across fruit fly species.
Table 3. Australian pest species of tephritid fruit fly, their distribution, hosts, preferred climate and attractant (lure type). C. capitata and B. frauenfeldi are the only non-native species. Note B. aquilonis and B. neohumeralis are sibling species of Qfly [69,78] and B. aquilonis is genetically indistinct from Qfly [79].
Table 3. Australian pest species of tephritid fruit fly, their distribution, hosts, preferred climate and attractant (lure type). C. capitata and B. frauenfeldi are the only non-native species. Note B. aquilonis and B. neohumeralis are sibling species of Qfly [69,78] and B. aquilonis is genetically indistinct from Qfly [79].
SpeciesDistributionHost/sClimate †Attractant
NativeInvasive
Bactrocera aquilonis (May)
Northern Territory fruit fly		Northern areas of Western Australia and the Northern Territory Polyphagus [80], major host billy-goat plum (Terminalia ferdinandiana). Major commercial host bitter gourd and guavaTropicalCuelure
Bactrocera bryoniae (Tryon)West Papua, Papua New Guinea, Queensland, Northern Territory, New South Wales and northern Western Australia [81], and Torres Strait Islands [35] Polyphagous, recorded on 9 hosts [80], main host chilliTropical, sub-tropicalCuelure group (melolure in Queensland [82]) and Wilson’s lure [34]
Bactrocera frauenfeldi (Schiner)
mango fruit fly		Federated States of Micronesia, Kiribati, Marshall Islands, Palau, Nauru, Solomon Islands, Moluccas, Papua New Guinea. Invasive to Queensland and Torres Strait [83]Polyphagous, 109 known hosts. Commercial hosts mango, banana, citrus, carambola, guava, papaya, edible Syzygium, star apple, sapodilla and abiu [33,80]TropicalCuelure group (melolure [82])
Bactrocera jarvisi (Tryon)
Jarvis’ fruit fly		Queensland and northern tropics [84] including Western Australia, Northern Territory, Torres Strait Islands and NSW south to Sydney [80]. West Papua and Papua New Guinea [33] Polyphagous. Recorded on 84 hosts. Main host cockatoo apple (Planchonia careya). Commercial hosts include mango, guava, papaya, persimmon, soursop, avocado, banana, pomegranate, apple, peach, pear, coffee, citrus and edible Syzygium [80]Tropical, sub-tropical, warm temperateZingerone [85] and weakly to cuelure [84]
Bactrocera kraussi (Hardy)Torres Strait Islands and northeast Queensland south to Townsville [80] Polyphagous. Recorded on 106 hosts. Commercial hosts include mango, banana, grumichama, feijoa, carambola, peach, citrus and tamarind [80]TropicalIsoeugenol and weakly to cuelure [82]
Bactrocera musae (Tryon)
banana fruit fly 		Torres Strait Islands and northeast Queensland south to Townsville [80], Papua New Guinea and associated islands [34], West Papua [35] Polyphagous. Recorded on 16 hosts. Primary economic host banana, occasional hosts papaya and guava [80]TropicalMethyl eugenol
Bactrocera neohumeralis
(Hardy)
lesser Queensland fruit fly		Eastern seaboard [69,78] south to Coffs Harbour, Papua New Guinea Polyphagous recorded on 160 hosts. Commercial hosts include mango, custard apple, rollinia, date palm, persimmon, mulberry, banana, carambola, passionfruit, loquat, apple, plum, peach, pear, citrus, coffee, star apple, sapodilla, abiu, capsicum and tomato [34,80]Tropical, sub-tropicalCuelure group [34]
Bactrocera tryoni (Froggatt)
Queensland fruit fly (Qfly)		Queensland, New South Wales and Victoria [86], Northern Territory [87]. Invasive to New Caledonia, French Polynesia, Pitcairn Island [34]Polyphagous recorded on over 200 hosts. Major commercial crops include mango, custard apple, papaya, carambola, passionfruit, loquat, apple, peach, coffee, star apple, sapodilla, capsicum, chilli and tomato [34,80]Tropical, sub-tropical, warm temperateCuelure group [82]
Ceratitis capitata (Wiedemann)
Mediteranean fruit fly (medfly)		African sub-Saharan countries. Invasive to >60 countries- Middle East, Europe, Egypt, Americas, and Australia (Western Australia and incursions into South Australia [86]).Polyphagous (any type of fleshy fruit-location dependant), major commercial hosts cherimoya, bell pepper, citrus, coffee, fig, apple, stone fruit, Japanese plum, guava, cocoa.Mediterranean and warm temperate (elevated tropical regions)Trimedlure/capilure, EGO lure and terpinyl acetate [87], enriched ginger oil (EGO) [88]
Zeugodacus cucumis (French)
cucumber fruit fly		Northern Territory, Queensland, Torres Strait Islands, northeast New South Wales [80] Polyphagous recorded on 40 hosts. Major commercial hosts include papaya, cucumber, pumpkin, squash, zucchini, guada bean, passionfruit and tomatoTropical, sub-tropicalNot attracted to male lures, cucumber volatile blend attractive to both sexes [89,90]
Data obtained from the Australian Handbook for the Identification of Australia fruit fly [30] and associated website fruitflyidentification.org.au (accessed on 15 January 2023) unless otherwise stated. † Based on presence data.
Table 4. Examples of very good host plants for Bactrocera dorsalis and associated host reproduction number (HRN) from different regions. HRN is calculated as the number of adults who emerged per 1 kg of fruit and very good hosts have a HRN value exceeding 100 [91]. HRN is for affected fruit in the field.
Table 4. Examples of very good host plants for Bactrocera dorsalis and associated host reproduction number (HRN) from different regions. HRN is calculated as the number of adults who emerged per 1 kg of fruit and very good hosts have a HRN value exceeding 100 [91]. HRN is for affected fruit in the field.
HostAfricaAsia and the Pacific
Annona muricata—Soursop [92]454
Carica papaya—Pawpaw [93] 142
Chrysobalanus icaco—Icaco [94]125
Diospyros blancoi—Velvet apple [94]140
Eriobotrya japonica—Loquat [92]325
Mangifera indica—Mango [92]505
Musa sp.—Banana [12,95]130 247
Nephelium lappaceum—Rambutan [95] 370
Pometia pinnata—Pacific lychee [95] 195
Psidium guajava—Guava [42,96]156 247
Sclerocarya birrea—Marula [12]238
Syzygium jambos—Jambos, Rose-apple [94,95]141 225
Terminalia catappa—Tropical almond [12]653
Vaccinium corymbosum—Blueberry [95] 1228

3. Management Strategies for Tephritid Fruit Fly Incursions

3.1. Emergency Response Plans

Effective control of exotic fruit fly incursions starts with an emergency response plan, which many countries have in place to guide their response operations. Plans typically involve identification, trapping (to delimit the incursion), host sampling surveys to identify the incursion zone, the establishment of a quarantine zone (usually with several levels or buffer zones including an exclusion zone) and then eradication (e.g., [97,98]). Australia has a generic emergency response plan, the Australian Emergency Plant Pest Response Plan or PLANTPLAN [99]. PLANTPLAN sets out general guidelines to follow in the event of an incursion by a plant pest. In summary, this includes identification of the pest (initial and confirmatory morphological or molecular diagnostics), determining the geographic extent of the incident, establishing quarantine zones (restricted areas, control areas and pest-free areas), establishing movement restrictions (for vehicles/machinery/produce) and finally control strategies (see Table 5 for fruit fly control examples). To date, mainland Australia does not have a generic or species-specific emergency response plan for exotic fruit fly species. There is, however, a detailed response plan (not an emergency plan because it manages ongoing seasonal incursions) for exotic fruit flies called the National Exotic Fruit Fly in Torres Strait Eradication Program: Response Plan 2021–2026. This plan describes the response activity required for detection and control of OFF, melon fly and New Guinea fruit fly and is based upon historical detections and proven eradication activities refined over the last 25 years in this area. While the implementation of this plan is useful to prevent incursions into Australia and acts as an early warning system, it does not cover the response to any mainland incursions [18], and as such the addition of a specific emergency response plan (as part of a National Action Plan) for exotic fruit fly species is required for mainland Australia.

3.2. Border Control and Surveillance

International border controls, entry restrictions, policies and treatment protocols are employed globally by countries to stop the entry of infested produce (fruit and vegetables) carried by travellers or in commercial consignments (e.g., [110,111]). Commercial fruit consignments are usually required to be treated using a recognised disinfestation technique to eliminate any live insects within the fruit. There are three main disinfestation techniques: irradiation [112], temperature treatments [113,114] and fumigation (e.g., methyl bromide) [115]. Methods used for disinfestation typically vary between crops due to associated damage, quality loss or acceptance of treatments by trading partners. Irradiation is highly effective against many tephritids with an internationally accepted dose of 150 Gy [112,116]. Temperature disinfestation is a non-polluting strategy but is time-consuming, may affect quality and typically has a large energy footprint. Methyl bromide is an ozone-depleting substance and is scheduled for phase-out under the Montreal Protocol. Despite quarantine treatments currently having a critical use exemption, the use of methyl bromide is likely to become increasingly restricted [115], and many countries including the European Union have banned its use for quarantine purposes on imported products.
Interceptions by border control are very successful in preventing incursions. Australia has some of the strictest biosecurity border controls in the world. The Department of Agriculture, Fisheries and Forestry (DAFF) and Australian Border Force manage pre-border checks of produce which involve declaration, manual inspection, X-ray inspection, inspection by detection dogs and destruction or treatment of seized goods [117]. In Australia, between 2012 and 2018, 1.9 million items of biosecurity concern were seized at airports. Between 2014 and 2017 there were over 37,000 border interceptions of pests (most of which were insects). Of these interceptions, most pests (45%) were brought into Australia by air cargo followed by sea cargo and containers (35%), the remainder a combination of interceptions from international air passengers and mail. Less than 1% of interceptions were for high-priority plant pests [117]. Border controls are vital in preventing incursions as propagule pressure (the initial population size) is linked to establishment success—the smaller the propagule the less likely a population will establish [77].
Should fruit flies bypass pre-border controls, targeted surveillance is used to detect flies or provide evidence of early establishment. Surveillance varies widely between countries. Australia, New Zealand and the USA (California and Florida) all have extensive surveillance networks in place (see [101] for a review; [118] for a map of the surveillance network in Australia). Typically, surveillance networks consist of grids interspersed with traps (e.g., McPhail, Lynfield, or Steiner traps) laced with a lure and an insecticide (e.g., malathion, fipronil, spinosad). Lures can be species or genus-specific, such as para-pheromone lures designed to attract males only or ammonia-based lures for non-lure-responsive species, which capture both sexes. Most if not all fruit flies are attracted to ammonia-based lures, and baits of ammonia laced with insecticides are commonly used for control or eradication of fruit fly populations (see Section 3.3 Eradication and control). However, para-pheromone lures are typically much more effective in terms of detecting target species for surveillance purposes. Ammonia-based lures are an old technology used before para-pheromones became available and are typically used where no para-pheromone lure has been developed for a particular species. The para-pheromone lures methyl eugenol, cuelure and trimedlure/capilure are widely used to attract OFF, Qfly and medfly males, respectively. In contrast, the Mexican fruit fly has no known para-pheromone lure, but ammonium acetate, hydrolysed protein, torula yeast and putrescine-based lures work as attractants [26,27,28,29]. Table 1 and Table 3 list the lures used for the species mentioned in this review.
Fruit fly trap and lure selection is influenced by the target fly species and by environmental conditions, leading to different trap/lure combinations being used in different countries or regions. USA surveillance programs (in California, Florida and Texas) use Jackson traps in combination with trimedlure and BioLure® (ammonia-based) for medfly, BioLure® for Anastrepa spp., cuelure and methyl eugenol for Bactrocera spp., and McPhail traps baited with torula yeast to monitor Mexican fruit fly [119]. The New Zealand Fruit Fly Detection Program uses Lynfield traps baited with cuelure to attract Qfly and melon fly, methyl eugenol to attract OFF, trimedlure/capilure to attract medfly, and ammonia-based lures as a general lure for species not attracted to para-pheromones [120,121] (see below for details of Australian trap/lure combinations).
Typically, surveillance networks employ grids of traps at densities of between one and eight traps per km2 at major ports of entry and in high-risk areas (i.e., urban areas and horticultural zones), depending on designated risk [101,122]. The effectiveness of a trapping grid in detecting incursions is dependent on the sensitivity of the grid, which in turn is determined by the type and combination of lures used (some combinations of lures can reduce efficacy (e.g., [123]), grid size, trap density, monitoring frequency, geography and climate [124]. Additionally, the use of any particular trap/lure combination in lure-based eradication designed for one fruit fly species may lead to an increase in the likelihood of the establishment of other species. The suppression of resident fruit fly populations may reduce competition for invading species [125], and the traps and lures in place may not be suitable for the control of the new invading species [126]. Trapping guidelines have been issued by the Food and Agriculture Organisation and International Atomic Energy Agency [124] and stipulate trap density for effective monitoring, control/suppression and eradication.
The fruit fly surveillance network in Australia is complex, as it is largely funded by the federal government but run independently by the Australian states and territories. The federal program is responsible for international border control and runs the National Plant Health Surveillance Program (NPHSP) (previously the Australian National Exotic Fruit Fly Surveillance Program), and the Northern Australia Quarantine Strategy (NAQS) (see [86,101]). The NPHSP was established after the 1995 incursion of OFF in Cairns and consists of a network of 4800 traps equally baited with a malathion toxicant and cuelure, capilure or methyl eugenol lures set up at one trap per 25 km2 within 20 km of major ports of entry around Australia [101] (see [127] for a location map).
NAQS became operational in 1989 and remains the key Australian program today to monitor incursions from non-regulated pathways into northern Australia [101]. The NAQS fruit fly monitoring network currently comprises 125 permanent traps spread out over 20 islands at 46 sites, as well as across 13 sites in the northern tip of Cape York Peninsula, Queensland [18,127]. Additional response traps are added in the event of an incursion.
Each state and territory in Australia additionally runs its own fruit fly surveillance programs, mostly to monitor the spread of existing but regionally restricted fruit fly populations (i.e., Qfly and medfly). These programs act as an early warning system for incursions and also demonstrate the absence of fruit fly species for international trade purposes [69]. In combination, the trapping surveillance networks of the Australian states and territories consist of more than 25,000 traps baited with a combination of methyl eugenol, cuelure and capilure, set up at a density of 6 traps per km2 in high-risk urban areas and at 1 trap per km2 in horticultural zones [69,100,115].
Surveillance trap architecture varies between locations due to local environmental conditions, predominantly rainfall frequency. The Lynfield trap is used throughout NSW [69], in most southern regions [128] and in many parts of southern and central Queensland [129]. In northern Australia, Lynfield traps are suboptimal due to heavy monsoon rain and Paton and Steiner traps are used instead [11]. Recently, Biotraps® were found to be equivalent to Lynfield traps in New Zealand and southern Australia in terms of efficacy [130] and cone traps were also found to be equivalent to Lynfield traps [131]. These trap designs may replace Lynfield traps as their availability declines [132]. Based on national guidelines, most states inspect their fruit fly traps fortnightly. Traps for the Torres Strait grid are checked monthly during the “dry” season (July to December) and fortnightly during the “wet” season (January to June) [18]. Data from programs (excluding NAQS trapping data) are sent to the federal government agency, the DAFF to include in a restricted-access national database called AUSPestCheck® run by Plant Health Australia (PHA), the national coordinator of the government-industry partnership for plant biosecurity in Australia.

3.3. Eradication and Control

According to the Global Eradication and Response Database (GERDA), [133] there have been approximately 189 incursion responses and eradication attempts for the exotic fruit flies mentioned in this study; nine for Mexican fruit fly in Mexico and the USA, eight for melon fly in the USA and Japan, approximately 55 for OFF (including synonyms) in USA, Japan, Australia, New Zealand and French Polynesia and 117 for medfly in New Zealand, USA, Australia and South America (for a summary see Table 6, for full information on successful eradications see http://b3.net.nz/gerda accessed on 15 March 2023). By summarising the methods used, we found that a combination of management technologies including cultural control (e.g., wrapping fruit, early harvesting, crop sanitation, soil raking), establishment of quarantine zones, the male annihilation technique (MAT), the bait application technique (BAT), the sterile insect technique (SIT) and biological control agents were used in an area-wide manner in successful eradication programs (see below and Table 5 for definitions). The most common eradication methods included various combinations of MAT, BAT and SIT.
MAT is a low-cost management strategy designed to attract and kill males so that mating is severely compromised [104]. MAT is used predominantly in orchards and urban control of fruit flies [19]. MAT uses para-pheromone lures (e.g., methyl eugenol or cuelure) in combination with an insecticide (e.g., malathion). The lure and insecticide are impregnated into caneite (compressed fibreboard), cordelitos (cotton wicks), coconut husks [18], compressed cardboard [18,137] or plastics [103]. The choice of material to be impregnated depends on rainfall, geography and local availability. Areas of high rainfall require more frequent replacement of MAT assemblies. Where access is difficult, MAT assemblies using cordelitos can be dropped from aircraft and remain active for several months. The Torres Strait Islands program in Australia uses caneite blocks impregnated with malathion and methyl eugenol or cuelure [18] for control of exotic fruit flies. Likewise, caneite blocks impregnated with malathion and methyl eugenol formed a very effective part of the Cairns eradication of OFF in the 1990s [19,102].
BAT or protein bait spays are another key component of fruit fly control, where a toxicant and attractant are applied to the foliage of host crops, usually only along the borders of the crop or in targeted areas. The toxicants and attractants used vary between countries, but toxicants may include malathion [105], spinosad [106,138] or fipronil [107]. Both male and female flies are attracted to protein sources emitting ammonia, so often the attractant used is a protein-based material. Either protein hydrolysate [103] or protein autolysate [139] is typically used, although protein hydrolysate may be phytotoxic due to its high acidity. In Australia, the type of protein used in BAT to control Qfly was changed from protein hydrolysate to protein autolysate for exactly this reason [108]. Malathion is the most frequently used BAT toxicant in Australia [11,18,127,140]. However, as the ability to use pesticides becomes more restricted by the Australian Pesticide and Veterinary Medicines Authority (APVMA) due to environmental and human health concerns, Australian chemical control of fruit fly is moving towards toxicants such as spinosad (a toxicant derived from the actinobacterium Saccharopolyspora spinosa Mertz and Yao (Pseudonocardiales: Pseudonocardiaceae) that is non-toxic to mammals but highly effective against arthropods (e.g., [18], for a review of chemical use against fruit fly in Australia see [141]).
SIT is the process of mass-rearing and releasing large numbers of sterile flies (preferably males only) into a wild population, the intended outcome being that wild females will mate with sterile males and then not produce fertile eggs, which in turn reduces the population [109]. SIT is an expensive and complex control method, but also a more environmentally sensitive option for fruit fly control. It requires specialised facilities and proven rearing, transportation and release techniques to minimise losses of sterile flies. This method of control has been used successfully for eradication as well as in reducing population size [136,142]. Australia has used SIT to suppress outbreaks of local fruit fly species since the 1960s [143,144] and currently has two SIT facilities available, one in South Australia and one in Western Australia, that produce sterile Qfly and medfly adults.

3.4. Economic Costs of Fruit Fly Incursion Management

The costs of fruit fly incursion management including preventative measures such as surveillance, eradication costs and loss of profits vary considerably but tend to range from millions to billions of dollars, depending on the location and the extent of the incursion. It is typically much less costly to invest in good incursion prevention measures than to initiate an eradication response. In Australia, an exotic fruit fly incursion would result in production disruptions, potential loss of domestic and international markets and income losses, together estimated at between AUD 269 million and AUD 2.1 billion, depending on the area affected and the success of the eradication attempt [18]. The cost of surveillance in mainland Australia in 2002 was estimated to be between AUD 1.3 and AUD 7 million per year [145] and the total cost of the NAQS surveillance program from 2021 to 2026 is estimated at AUD 4 million [18]. The eradication of OFF from Australia in the 1990s cost an estimated AUD 34 million [19], with a further AUD 100 million in costs incurred through increased production expenses, reduced productivity, and market access closures [18].

4. Fruit Fly in Australia

4.1. History of Economically Important Fruit Flies in Australia

Of the 301 tephritid species native to Australia [146] only eight are considered problematic to Australian horticultural industries [30] (Table 3). The most widespread and damaging of these tephritids is Qfly [140]. Qfly is thought to be native to Queensland and the north New South Wales coast. Historically, southern Australia was climatically suitable for Qfly establishment, however, range extension did not occur until after European settlement [40] brought the unregulated domestic trade of fruit and vegetables [86]. Qfly was first reported in NSW in 1819, but it was not considered a pest in NSW until 1852, with the first major outbreak occurring in 1884 [34]. Qfly is also present in the Northern Territory [140] and has been found periodically in (and eradicated from) South Australia, Western Australia [128,140] and Tasmania [147].
There have been two noteworthy incursions of exotic fruit flies into Australia. The first major incursion was by medfly. Medfly is considered the second most economically damaging fruit fly in Australia, after Qfly. Medfly was first introduced into Western Australia in 1896 and New South Wales in 1898 [148] and had spread to Victoria by 1909 [149]. It disappeared from the eastern states by the 1950s, probably due to a combination of control measures (most likely fruit destruction and soil drenches) and competition from Qfly [140]. Since that time there have been sporadic and swiftly eradicated outbreaks of medfly in South Australia (mostly around Adelaide) and in the Northern Territory [133,149]. In general, for national management and international trade purposes, Medfly is considered restricted to Western Australia, while Qfly is restricted to eastern areas of Australia (Northern Territory, Queensland, NSW, Victoria) and South Australia and Tasmania are free from both pests.
In the second major incursion, OFF (then B. papayae) was detected in papaya (Carica papaya) near Cairns in northern Queensland in October 1995, and again (as B. philippinensis) in the Northern Territory in November 1997 [19]. A national eradication response was mounted by state and federal government agencies and by 1999 OFF was eradicated from mainland Australia [19,146]. To date, mainland Australia remains free from OFF, however as mentioned previously interceptions and eradication of OFF (and other species) still occur yearly in the Torres Strait Islands [18,118].

4.2. National Fruit Fly Programs and Policy

The Australian Plant Health Committee (PHC) is the peak government plant biosecurity policy and decision-making forum. It provides strategic policy, technical and regulatory advice and national leadership on all plant biosecurity matters to protect Australia’s plant health and economic benefits derived from fruit and vegetable exports. In 2011, at the request of the National Biosecurity Committee (NBC), PHC assumed responsibility for managing policy for endemic fruit flies and the Australian Fruit Fly Technical Advisory Subcommittee (AFFTAC) was commissioned to develop Australia’s National Fruit Fly Management Protocol (ANFFMP). AFFTAC provides the necessary technical support for a nationally coordinated approach to surveillance and management of fruit flies, in line with Australia’s international import and export market access conditions and policies.
To manage ongoing fruit fly concerns in Australia a National Fruit Fly Council (NFFC) jointly funded by government and industry through their Research and Development Corporation (Hort Innovation) was established in 2015. The NFFC connects growers and fruit fly management groups across states and territories to control fruit flies in Australia on a national scale. The NFFC has produced a National Fruit Fly Strategy (NFFS) [150] to provide a framework for the cost-effective and coordinated management of fruit flies in Australia. It is designed to maintain Australia’s freedom from exotic fruit fly species, minimise the incidence and spread of local fruit fly species, support market access and facilitate a national approach to fruit fly management and research [150]. Other relevant plant protection organisations, such as Plant Health Australia (PHA), are responsible for developing and publishing important documents on the identification of native species of fruit fly (i.e., the Australian Handbook for Identification of Fruit Flies) and factsheets on the control measures that can be used against them.
In the event of an incursion of fruit flies Australia relies on a committee of experts called the Consultative Committee for Emergency Plant Pests (CCEPP) [151]. The CCEPP was developed as a response to the 1995 incursion of OFF to support a national response to fruit fly incursions. Before this time fruit fly management by the Australian states and territories was managed independently [19]. The CCEPP is designed to make recommendations for incursion management and oversees the preparation of a response plan (post-incursion) based on the general emergency response plan for plant pests (PLANTPLAN, [99]. This strategy is informed by a National Management Group (NMG) of Australian and international experts who will guide the incursion response based on the latest scientific information. The NMG usually stays engaged with the response and assists in the declaration of successful eradication if this is achieved.

4.3. Fruit Fly Incursion in Australia

Exact invasion pathways often remain unknown when an incursion occurs (e.g., [19]). As mentioned previously tourists, visitors and returning Australians from the Torres Strait Islands and Asia into northern Queensland are considered the most likely sources of an incursion [118]. Darwin (Northern Territory) and Cairns (Queensland) have international airports that service both tourism and airfreight and in addition to various potential incursion pathways, northern Australia also has excellent environmental conditions for fruit fly establishment and spread. Northern Australia has a tropical climate that is preferred by most exotic tephritids (see Table 1 and Table 3), and a wide range of hostplants are readily available. This area is particularly suitable for OFF establishment and additionally, the proximity to the Torres Strait Islands offers a potential stepping stone for OFF from PNG [18].
Surveillance traps are in place across Australia and contain fly-specific lures suitable for most species of concern, such as methyl eugenol which is attractive to OFF [11,115]. Mainland Australia seems well placed to detect any incursion, provided the surveillance trapping grid is maintained. Part of a good surveillance system is predicting where entry is most likely to occur to target priority areas for surveillance. There are several older models available that predict environmental suitability for OFF in Australia (e.g., [53,54]), however, models of environmental suitability are lacking for other species of concern and these types of models require frequent updating with the latest data to improve accuracy. Predictions for OFF indicate that the northern coastline of Australia is currently the most suitable [53], however, most of the eastern seaboard of Australia will be suitable for OFF establishment within the next 50 years [54,152].
Host availability is a key factor for fruit fly colonisation and establishment [153,154]. In most climatically suitable areas of Australia, there are no host limitations. However, there may be competition for hosts for invading fruit fly species. Qfly is established in most Australian horticultural areas and there are at least seven other endemic pest tephritids in northern Australia (Table 3; [55]), all of which currently compete for host resources [125]. An indication of the likelihood of establishment success might be gained by comparing the HRN of species of concern (e.g., OFF) with the HRN of native Australian tephritids [91]. Comparisons of OFF and Qfly on the more common and preferred host species such as mango would be of particular value. Unfortunately, HRN values for most fruit fly species present in Australia (other than Qfly and Medfly) are yet to be determined even for major hosts, and the competitive potential of these species cannot be easily assessed. This is important as it is thought that competition from native tephritid species masked the detection of the 1997 incursion of OFF in Cairns, which is estimated to have occurred 2.5 years prior to discovery [19].
Limiting factors to the spread of OFF in Australia are likely to be related to water availability, host availability and temperature. Areas of lower humidity cause moisture stress in tephritids and this would hypothetically restrict most exotic fruit flies to coastal areas of Australia since inland Australia is mostly arid. Lower temperatures that occur in southern Australia (which currently has a more temperate climate) would typically cause cold stress [154], with temperatures in large areas of southern Australia falling below the minimum requirements for development and survival (see Table 2). However, the availability of irrigation in the drier areas of southern Australia, both in towns and on farming land, climate change, the heat island effect of urban areas and host availability in backyard gardens may aid in survival and establishment in areas where natural conditions would have previously made this unlikely [152,153,154]. Anthropogenic environments (particularly in rural locations) need to be considered when attempting to model the establishment and spread of exotic fruit fly species in Australia. Models incorporating anthropogenically modified environments (e.g., [155]) show the establishment of fruit fly populations to be possible in areas where models incorporating only general climate data predict low or no establishment potential. Likewise, consideration of areas where the establishment is known to not occur, despite modelling predictions to the contrary, needs to occur. During the 1995 incursion OFF demonstrated an apparent inability to establish in natural rainforest habitats in far north Queensland, despite the large number of fruiting trees available in rainforest areas adjacent to horticultural crops. OFF establishment was restricted to areas of human habitation [19,156], which aided significantly in its successful eradication.
Australia has been successful in managing outbreaks of local fruit flies (Qfly and medfly) across state borders [115]. To control or locally eradicate Qfly and medfly, Australia uses various combinations of MAT, BAT [18], SIT [157], quarantine zones [19,140], surveillance, fruit removal and destruction [133], community awareness and engagement and, where necessary, financial penalties for transporting unauthorised produce into or out of quarantine zones [19]. These methods are all used in the control and eradication of exotic fruit fly species in global locations (Table 6) and could be used in the management of an incursion into Australia by exotic fruit fly species.

5. Conclusions

The high risk of a new incursion by OFF or by other exotic fruit fly species remains one of the primary drivers for continued targeted surveillance and quarantine measures at ports of entry into Australia [69,100]. Australia relies heavily on surveillance grids and border controls to prevent incursions of exotic tephritids. The maintenance of an effective surveillance and early warning system remains the best way to optimise Australia’s ongoing freedom from exotic fruit flies. The current surveillance system was established in the 1990s with reference to earlier environmental conditions, tephritid species and trapping methods. To be effective, the surveillance system in Australia needs to be utilising the latest and most effective lure types [158], best trap architecture, optimal grid spacing, appropriate pesticides [141,159], and trap locations based on detailed species distribution models and climate forecasts, with emphasis on busy ports of entry. A review of the national trapping grid was completed in 2018 by the DAFF, however, the results of this review, along with up-to-date information on the surveillance grid and its effectiveness, are not yet publicly available. Notwithstanding the above, we acknowledge that the current surveillance system seems to be effective, as there have been no serious incursions since the grid was established.
Specific areas of improvement other than those already mentioned, include a better understanding of the effect of interspecific competition between exotic and native species of fruit fly through the generation of additional HRN data. These data may help us better understand the establishment, detection and spread of exotic fruit fly species, as well as facilitate more closely targeted lure use. Lure type is particularly important for those species not attracted to the para-pheromone lures that are used in the Australian surveillance grid, such as Mexican fruit fly. Although Mexican fruit fly is not as high a biosecurity risk as OFF, Australia seems less prepared for Mexican fruit fly than for other priority species. This reflects the fact that whilst this species is listed as one of those of most concern to Australia, it is not present in Asia from where the greatest incursion risks are likely to originate. Additionally, the Mexican fruit fly is low on the ‘tephritid hierarchy’ [160] and is likely to have difficulty establishing in an environment saturated with Bactrocera spp. Surveillance for Mexican fruit fly (and other non-lure responsive species) could potentially be improved with the addition of ammonia-based lures that attract a wide range of fruit fly species to the Australian surveillance grid. This approach is being used by New Zealand in their fruit fly surveillance program [120,121].
Australia has a robust set of management strategies and policies available for the surveillance, containment, and eradication of local fruit fly species. To some degree, this has been extended to exotic fruit fly species. Australia-wide management protocols, strategies and plans for exotic fruit fly species, such as those discussed here, have benefited from the experience gained in implementing control measures directed towards preventing the internal spread of Qfly and medfly in Australia. Measures that have been used to successfully eradicate exotic tephritids (including OFF) globally also provide a sound basis for future incursion responses. National participation in management programs, the development of policy and collaboration by industry and government mean that Australia is reasonably well placed to deal with an incursion by exotic fruit fly. However, the lack of a specific emergency response plan means that the reaction to a post-border detection of exotic fruit flies will likely be delayed while research is conducted into the best management strategies for containment and eradication, potentially leading to a more severe and costly incursion outcome. A targeted emergency response plan would be relatively easy to develop and established management strategies for pest tephritids currently present in Australia would provide it with a strong foundation.

Author Contributions

J.L.H. coordinated the literature review, wrote the manuscript, and prepared the revision; B.C.D. contributed to the initial draft and revisions; P.R. secured the funding, initiated the review, and coordinated the project of which this review is a part; M.M.S. contributed to early drafts and the revision. All authors have read and agreed to the published version of the manuscript.

Funding

This paper forms part of the research conducted under the project Biosecurity preparedness for Oriental fruit fly (FF18001) 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, New South Wales Department of Primary Industries, South Australia Research Development Institute, and contributions from the Australian Government. Hort Innovation is the grower-owned, not-for-profit research and development corporation for Australian horticulture.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Acknowledgments

Thanks go to Andrew Elliot for suggestions and comments on first drafts of the manuscript and David Britton, Peter Gillespie and Greg Chandler for suggestions and comments on the final draft of the manuscript.

Conflicts of Interest

The authors declare there are no conflict of interest.

References

  1. STDF. A Coordinated Multi-Stakeholder Approach to Control Fruit Fly in West Africa; Food and Agriculture Organization: Rome, Italy, 2010. [Google Scholar]
  2. Motswagole, R.; Gotcha, N.; Nyamukondiwa, C. Thermal biology and seasonal population abundance of Bactrocera dorsalis Hendel (Diptera: Tephritidae): Implications on pest management. Int. J. Insect Sci. 2019, 11, 1179543319863417. [Google Scholar] [CrossRef]
  3. Hort Innovation. Australian Horticulture Statistics Handbook; Hort Innovation: Sydney, NSW, Australia, 2021. [Google Scholar]
  4. Kriticos, D.; Stephens, A.; Leriche, A. Effect of climate change on oriental fruit fly in New Zealand and the Pacific. N. Z. Plant Prot. 2007, 60, 271–278. [Google Scholar] [CrossRef]
  5. Ormsby, M.D. Establishing criteria for the management of tephritid fruit fly outbreaks. CABI Agric. Biosci. 2021, 2, 23. [Google Scholar] [CrossRef]
  6. Schutze, M.K.; Aketarawong, N.; Amornsak, W.; Armstrong, K.F.; Augustinos, A.A.; Barr, N.; Bo, W.; Bourtzis, K.; Boykin, L.M.; Caceres, C. Synonymization of key pest species within the Bactrocera dorsalis species complex (Diptera: Tephritidae): Taxonomic changes based on a review of 20 years of integrative morphological, molecular, cytogenetic, behavioural and chemoecological data. Syst. Entomol. 2015, 40, 456–471. [Google Scholar] [CrossRef]
  7. Plant Health Australia. National Plant Biosecurity Status Report; Plant Health Australia: Canberra, ACT, Australia, 2019. [Google Scholar]
  8. Early, R.; Bradley, B.A.; Dukes, J.S.; Lawler, J.J.; Olden, J.D.; Blumenthal, D.M.; Gonzalez, P.; Grosholz, E.D.; Ibañez, I.; Miller, L.P. Global threats from invasive alien species in the twenty-first century and national response capacities. Nat. Commun. 2016, 7, 12485. [Google Scholar] [CrossRef]
  9. Robinson, A.P.; McNeill, M.R. Biosecurity and post-arrival pathways in New Zealand: Relating alien organism detections to tourism indicators. NeoBiota 2022, 71, 51–69. [Google Scholar] [CrossRef]
  10. Steiner, L.; Hart, W.; Harris, E.; Cunningham, R.; Ohinata, K.; Kamakahi, D. Eradication of the oriental fruit fly from the Mariana Islands by the methods of male annihilation and sterile insect release. J. Econ. Entomol. 1970, 63, 131–135. [Google Scholar] [CrossRef]
  11. Huxham, K. A unique fruit fly monitoring and control system—Australia’s frontline of northern defence. In Proceedings of the 6th International Fruit Fly Symposium of Fruit Flies of Economic Importance, Stellenbosch, South Africa, 6–10 May 2002; Isteg Scientific Publications: Irene, South Africa, 2002; pp. 331–334. [Google Scholar]
  12. Allwood, A.; Chinajariyawong, A.; Kritsaneepaiboon, S.; Drew, R.; Hamacek, E.; Hancock, D.; Hengsawad, C.; Jipanin, J.; Jirasurat, M.; Krong, C.K. Host plant records for fruit flies (Diptera: Tephritidae) in Southeast Asia. Raffles Bull. Zool. 1999, 47, 1–92. [Google Scholar]
  13. Vargas, R.I.; Piñero, J.C.; Leblanc, L. 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 2015, 6, 297–318. [Google Scholar] [CrossRef] [PubMed]
  14. Mutamiswa, R.; Nyamukondiwa, C.; Chikowore, G.; Chidawanyika, F. Overview of oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) in Africa: From invasion, bio-ecology to sustainable management. Crop Prot. 2021, 141, 105492. [Google Scholar] [CrossRef]
  15. Leblanc, L.; Putoa, R. Fruit flies in French Polynesia and Pitcairn Islands; P.P. Service, Ed. Secretariat of the Pacific Community: Suva, Fiji, 2000; Volume 29. [Google Scholar]
  16. Clarke, A.R. Biology and Management of Bactrocera and Related Fruit Flies; CABI: Boston, MA, USA, 2019. [Google Scholar]
  17. Tarno, H.; Octavia, E.; Himawan, T.; Setiawan, Y. Diversity and abundance of fruit flies (Diptera: Tephritidae) on different host plants in Depok and Bogor Districts, West Java, Indonesia. Biodiversitas 2022, 23, 4202–4208. [Google Scholar] [CrossRef]
  18. Queensland Department of Agriculture and Fisheries (QDAF). National Exotic Fruit Flies in the Torres Strait Eradication Program Response Plan; QDAF: Brisbane, Australia, 2021. [Google Scholar]
  19. Cantrell, B.; Chadwick, B.; Cahill, A. Fruit Fly Fighters: Eradication of the Papaya Fruit Fly; CSIRO Publishing: Collingwood, VIC, Australia, 2002. [Google Scholar]
  20. Ekesi, S.; De Meyer, M.; Mohamed, S.A.; Virgilio, M.; Borgemeister, C. Taxonomy, ecology, and management of native and exotic fruit fly species in Africa. Annu. Rev. Entomol. 2016, 61, 219–238. [Google Scholar] [CrossRef] [PubMed]
  21. Bonizzoni, M.; Guglielmino, C.; Smallridge, C.; Gomulski, M.; Malacrida, A.; Gasperi, G. On the origins of medfly invasion and expansion in Australia. Mol. Ecol. 2004, 13, 3845–3855. [Google Scholar] [CrossRef] [PubMed]
  22. Arias, M.B.; Hartle-Mougiou, K.; Taboada, S.; Vogler, A.; Riesgo, A.; Elfekih, S. Unveiling biogeographic patterns in the worldwide distributed Ceratitis capitata (medfly) using population genomics and microbiome composition. Mol. Ecol. 2022, 31, 4866–4883. [Google Scholar] [CrossRef] [PubMed]
  23. Dias, N.P.; Zotti, M.J.; Montoya, P.; Carvalho, I.R.; Nava, D.E. Fruit fly management research: A systematic review of monitoring and control tactics in the world. Crop Prot. 2018, 112, 187–200. [Google Scholar] [CrossRef]
  24. Clarke, A.R.; Li, Z.h.; Qin, Y.j.; Zhao, Z.H.; Liu, L.j.; Schutze, M.K. Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) is not invasive through Asia: It’s been there all along. J. Appl. Entomol. 2019, 143, 797–801. [Google Scholar] [CrossRef]
  25. Dias, N.P.; Montoya, P.; Nava, D.E. A 30-year systematic review reveals success in tephritid fruit fly biological control research. Entomol. Exp. Appl. 2022, 170, 370–384. [Google Scholar] [CrossRef]
  26. Bateman, M.A. Chemical methods for suppression or eradication of fruit fly populations. In Economic Fruit Flies of the South Pacific Region; Drew, R.A.I., Hooper, G.H.S., Bateman, M.A., Eds.; Queensland Department of Primary Industries: Brisbane, QLD, Australia, 1982; pp. 115–128. [Google Scholar]
  27. Hedström, I.; Jimenez, J. Field evaluation of attractants in the capture of Anastrepha spp. (Diptera, Tephritidae), pests of fruit trees in tropical America. II. Ammonium acetate and torula with sodium borate. Rev. Bras. Entomol. 1988, 32, 319–322. [Google Scholar]
  28. Sharp, J.L. Laboratory and field experiments to improve enzymatic casein hydrolysate as an arrestant and attractant for Caribbean fruit fly, Anastrepha suspensa (Diptera: Tephritidae). Fla. Entomol. 1987, 70, 225–233. [Google Scholar] [CrossRef]
  29. Hedström, I.; Jirón, L. Field evaluation of attractants in the trapping of Anastrepha spp. (Diptera, Tephritidae), pests of fruit trees in tropical America. I. Molasses and torula yeast. Rev. Bras. Entomol. 1985, 29, 515–520. [Google Scholar]
  30. Plant Health Australia. The Australian Handbook for the Identification of Fruit Flies; Plant Health Australia: Canberra, ACT, Australia, 2018; Volume 3.1. [Google Scholar]
  31. Marchioro, C.A. Global potential distribution of Bactrocera carambolae and the risks for fruit production in Brazil. PLoS ONE 2016, 11, e0166142. [Google Scholar] [CrossRef]
  32. Zeng, Y.; Reddy, G.V.; Li, Z.; Qin, Y.; Wang, Y.; Pan, X.; Jiang, F.; Gao, F.; Zhao, Z.H. Global distribution and invasion pattern of oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). J. Appl. Entomol. 2019, 143, 165–176. [Google Scholar] [CrossRef]
  33. Leblanc, L.; Vueti, E.T.; Drew, R.A.; Allwood, A.J. Host plant records for fruit flies (Diptera: Tephritidae: Dacini) in the Pacific Islands. Proc. Hawaii. Entomol. Soc. 2012, 44, 11–53. [Google Scholar]
  34. Drew, R.A. The tropical fruit flies (Diptera: Tephritidae: Dacinae) of the Australasian and Oceanian regions. Mem. Qld. Mus. 1989, 26, 521. [Google Scholar]
  35. Drew, R.A.; Romig, M.C. Tropical Fruit Flies (Tephritidae Dacinae) of South-East Asia: Indomalaya to North-West Australasia; CABI: Oxfordshire, UK, 2013. [Google Scholar]
  36. Shiga, M.; Robinson, A.; Hooper, G. Current programme in Japan. In Fruit Flies: Their biology, Natural Enemies and Control; Robinson, A.S., Hooper, G., Eds.; Elsevier: Amsterdam, The Netherlands, 1989; pp. 365–374. [Google Scholar]
  37. Casaña-Giner, V.; Oliver, J.; Jang, E.; Carvalho, L. Syntheses and behavioral evaluations of fluorinated and silylated analogs of raspberry ketone as attractants for the melon fly, Bactrocera cucurbitae (Coquillett). J. Entomol. Sci. 2003, 38, 111–119. [Google Scholar] [CrossRef]
  38. Kriticos, D.J.; Leriche, A.; Palmer, D.J.; Cook, D.C.; Brockerhoff, E.G.; Stephens, A.E.; Watt, M.S. Linking climate suitability, spread rates and host-impact when estimating the potential costs of invasive pests. PLoS ONE. 2013, 8, e54861. [Google Scholar] [CrossRef]
  39. Bebber, D.P.; Holmes, T.; Smith, D.; Gurr, S.J. Economic and physical determinants of the global distributions of crop pests and pathogens. New Phytol. 2014, 202, 901–910. [Google Scholar] [CrossRef]
  40. Sadler, R.; Florec, V.; White, B.; Dominiak, B. Calibrating a jump-diffusion model of an endemic invasive: Metamodels, statistics and Qfly. In Proceedings of the 19th International Congress on Modelling and Simulation MODSIM2011, Perth, Australia, 12–16 December 2011; Chan, F., Marinova, D., Anderssen, R.S., Eds.; 2011; pp. 2549–2555. [Google Scholar]
  41. Gilchrist, A.; Dominiak, B.; Gillespie, P.; Sved, J. Variation in population structure across the ecological range of the Queensland fruit fly, Bactrocera tryoni. Aust. J. Zool. 2006, 54, 87–95. [Google Scholar] [CrossRef]
  42. Leblanc, L.; Vargas, R.I.; Putoa, R. From eradication to containment: Invasion of French Polynesia by Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) and releases of two natural enemies: A 17-year case study. Proc. Hawaii. Entomol. Soc. 2013, 45, 31–43. [Google Scholar]
  43. Hicks, C.B.; Bloem, K.; Pallipparambil, G.R.; Hartzog, H.M. Reported long-distance flight of the invasive Oriental fruit fly and its trade implications. In Area-Wide Management of Fruit Fly Pests; Hicks, C.B., Bloem, K., Godshen, R., Eds.; CRC Press: Boca Raton, FL, USA, 2019; pp. 9–25. [Google Scholar] [CrossRef]
  44. Fletcher, B. The ecology of a natural population of the Queensland fruit fly, Dacus tryoni. IV. The immigration and emigration of adults. Aust. J. Zool. 1973, 21, 541–565. [Google Scholar] [CrossRef]
  45. Weldon, C.W.; Schutze, M.K.; Karsten, M. Trapping to monitor tephritid movement: Results, best practice, and assessment of alternatives. In Trapping and the Detection, Control, and Regulation of Tephritid Fruit Flies; Shelly, T., Epsky, N., Jang, E., Reyes-Flores, J., Vargas, R., Eds.; Springer: Dordrecht, The Netherlands, 2014; pp. 175–217. [Google Scholar] [CrossRef]
  46. Froerer, K.; Peck, S.; McQuate, G.; Vargas, R.; Jang, E.; McInnis, D. Long-distance movement of Bactrocera dorsalis (Diptera: Tephritidae) in Puna, Hawaii: How far can they go? Am. Entomol. 2010, 56, 88–95. [Google Scholar] [CrossRef]
  47. Nakamori, H.; Soemori, H. Comparison of dispersal ability and longevity for wild and mass-reared melon flies: Dacus cucurbitae Coquillett (Diptera: Tephritidae), under field conditions. Appl. Entomol. Zool. 1981, 16, 321–327. [Google Scholar] [CrossRef]
  48. Fezza, T.J.; Shelly, T.E. Comparative lure response, dispersal, and survival of male melon flies (Diptera: Tephritidae) from wild and genetic sexing strains in Hawaii. Fla. Entomol. 2020, 103, 253–258. [Google Scholar] [CrossRef]
  49. Thomas, D.B.; Loera-Gallardo, J. Dispersal and longevity of mass-released, sterilized Mexican fruit flies (Diptera: Tephritidae). Environ. Entomol. 1998, 27, 1045–1052. [Google Scholar] [CrossRef]
  50. Pieterse, W.; Terblanche, J.S.; Addison, P. Do thermal tolerances and rapid thermal responses contribute to the invasion potential of Bactrocera dorsalis (Diptera: Tephritidae)? J. Insect Physiol. 2016, 98, 1–6. [Google Scholar] [CrossRef] [PubMed]
  51. Nyamukondiwa, C.; Terblanche, J.S. Thermal tolerance in adult Mediterranean and Natal fruit flies (Ceratitis capitata and Ceratitis rosa): Effects of age, gender and feeding status. J. Therm. Biol. 2009, 34, 406–414. [Google Scholar] [CrossRef]
  52. Sutherst, R.W.; Collyer, B.S.; Yonow, T. The vulnerability of Australian horticulture to the Queensland fruit fly, Bactrocera (Dacus) tryoni, under climate change. Aust. J Agric. Res. 2000, 51, 467–480. [Google Scholar] [CrossRef]
  53. De Meyer, M.; Robertson, M.P.; Mansell, M.W.; Ekesi, S.; Tsuruta, K.; Mwaiko, W.; Vayssières, J.-F.; Peterson, A.T. Ecological niche and potential geographic distribution of the invasive fruit fly Bactrocera invadens (Diptera, Tephritidae). Bull. Entomol. Res. 2010, 100, 35–48. [Google Scholar] [CrossRef]
  54. Qin, Y.; Wang, C.; Zhao, Z.; Pan, X.; Li, Z. Climate change impacts on the global potential geographical distribution of the agricultural invasive pest, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Clim. Chang. 2019, 155, 145–156. [Google Scholar] [CrossRef]
  55. Sultana, S.; Baumgartner, J.B.; Dominiak, B.C.; Royer, J.E.; Beaumont, L.J. Impacts of climate change on high priority fruit fly species in Australia. PLoS ONE 2020, 15, e0213820. [Google Scholar] [CrossRef]
  56. Han, P.; Wang, X.; Niu, C.-Y.; Dong, Y.-C.; Zhu, J.-Q.; Desneux, N. Population dynamics, phenology, and overwintering of Bactrocera dorsalis (Diptera: Tephritidae) in Hubei Province, China. J. Pest. Sci. 2011, 84, 289–295. [Google Scholar] [CrossRef]
  57. Sultana, S.; Baumgartner, J.B.; Dominiak, B.C.; Royer, J.E.; Beaumont, L.J. Potential impacts of climate change on habitat suitability for the Queensland fruit fly. Sci. Rep. 2017, 7, 13025. [Google Scholar] [CrossRef] [PubMed]
  58. Simpson, M.; Dominiak, B.C.; McGowen, I.J.; Crean, J.J.; Sides, T.J. Bioclimatic niche modelling projects a potential shift in distribution and abundance of Queensland fruit fly Bactrocera tryoni vs Australia. Gen. Appl. Entomol. 2020, 48, 61–74. [Google Scholar]
  59. Nyamukondiwa, C.; Terblanche, J.S. Within-generation variation of critical thermal limits in adult Mediterranean and Natal fruit flies Ceratitis capitata and Ceratitis rosa: Thermal history affects short-term responses to temperature. Physiol. Entomol. 2010, 35, 255–264. [Google Scholar] [CrossRef]
  60. Nyamukondiwa, C.; Weldon, C.W.; Chown, S.L.; le Roux, P.C.; Terblanche, J.S. Thermal biology, population fluctuations and implications of temperature extremes for the management of two globally significant insect pests. J. Insect Physiol. 2013, 59, 1199–1211. [Google Scholar] [CrossRef]
  61. Meats, A. Thermal constraints to successful development of the Queensland fruit fly in regimes of constant and fluctuating temperature. Entomol. Exp. Appl. 1984, 36, 55–59. [Google Scholar] [CrossRef]
  62. Rwomushana, I.; Ekesi, S.; Ogol, C.; Gordon, I. Effect of temperature on development and survival of immature stages of Bactrocera invadens (Diptera: Tephritidae). J. Appl. Entomol. 2008, 132, 832–839. [Google Scholar] [CrossRef]
  63. Vargas, R.I.; Walsh, W.A.; Jang, E.B.; Armstrong, J.W.; Kanehisa, D.T. Survival and development of immature stages of four Hawaiian fruit flies (Diptera: Tephritidae) reared at five constant temperatures. Ann. Entomol. Soc. Am. 1996, 89, 64–69. [Google Scholar] [CrossRef]
  64. Danjuma, S.; Thaochan, N.; Permkam, S.; Satasook, C. Effect of temperature on the development and survival of immature stages of the carambola fruit fly, Bactrocera carambolae, and the Asian papaya fruit fly, Bactrocera papayae, reared on guava diet. J. Insect Sci. 2014, 14, 126. [Google Scholar] [CrossRef]
  65. Meats, A. Abiotic mortality factors: Temperature. In Fruit Flies: Biology, Natural Enemies and Control; Robinson, A.S., Hooper, G.H.S., Eds.; Elsevier: Amsterdam, The Netherlands, 1989; pp. 229–239. [Google Scholar]
  66. Shoukry, A.; Hafez, M. Studies on the biology of the Mediterranean fruit fly Ceratitis capitata. Entomol. Exp. Appl. 1979, 26, 33–39. [Google Scholar] [CrossRef]
  67. Duyck, P.F.; David, P.; Quilici, S. A review of relationships between interspecific competition and invasions in fruit flies (Diptera: Tephritidae). Ecol. Entomol. 2004, 29, 511–520. [Google Scholar] [CrossRef]
  68. Vargas, R.I.; Walsh, W.A.; Kanehisa, D.; Jang, E.B.; Armstrong, J.W. Demography of four Hawaiian fruit flies (Diptera: Tephritidae) reared at five constant temperatures. Ann. Entomol. Soc. Am. 1997, 90, 162–168. [Google Scholar] [CrossRef]
  69. Dominiak, B.C. Surveillance for exotic fruit fly of the subfamily Dacinae (Insecta, Diptera, Tephrididae) and a review of the Dacinae established in Sydney, Australia, between 2010 and 2019. N. Z. Entomol. 2021, 43, 114–121. [Google Scholar] [CrossRef]
  70. Ekesi, S.; Nderitu, P.; Rwomushana, I. Field infestation, life history and demographic parameters of the fruit fly Bactrocera invadens (Diptera: Tephritidae) in Africa. Bull. Entomol. Res. 2006, 96, 379–386. [Google Scholar] [CrossRef] [PubMed]
  71. Ekesi, S.; Billah, M.K.; Nderitu, P.W.; Lux, S.A.; Rwomushana, I., IV. Evidence for competitive displacement of Ceratitis cosyra by the invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) on mango and mechanisms contributing to the displacement. J. Econ. Entomol. 2009, 102, 981–991. [Google Scholar] [CrossRef] [PubMed]
  72. Dominiak, B.; Taylor-Hukins, R. Priority host plants for Ceratitis capitata, Mediterranean fruit fly, based on the host reproduction number for surveillance, trade and eradication programs. Int. J. Trop. Insect Sci. 2022, 42, 3721–3727. [Google Scholar] [CrossRef]
  73. Ndiaye, M.; Dieng, E.O.; Delhove, G. Population dynamics and on-farm fruit fly integrated pest management in mango orchards in the natural area of Niayes in Senegal. Pest Manag. Hortic. Ecosyst. 2008, 14, 1–8. [Google Scholar]
  74. Jang, E.B.; Light, D.M. Behavioral responses of female oriental fruit flies to the odor of papayas at three ripeness stages in a laboratory flight tunnel (Diptera: Tephritidae). J. Insect Behav. 1991, 4, 751–762. [Google Scholar] [CrossRef]
  75. Rattanapun, W.; Amornsak, W.; Clarke, A.R. Bactrocera dorsalis preference for and performance on two mango varieties at three stages of ripeness. Entomol. Exp. Appl. 2009, 131, 243–253. [Google Scholar] [CrossRef]
  76. Rwomushana, I.; Ekesi, S.; Ogol, C.K.; Gordon, I. Mechanisms contributing to the competitive success of the invasive fruit fly Bactrocera invadens over the indigenous mango fruit fly, Ceratitis cosyra: The role of temperature and resource pre-emption. Entomol. Exp. Appl. 2009, 133, 27–37. [Google Scholar] [CrossRef]
  77. Dominiak, B.C.; Fanson, B.G. Predicting point-source invasion success in the Queensland fruit fly (Bactrocera tryoni): An individual-based modelling approach. Crop Prot. 2023, 164, 106121. [Google Scholar] [CrossRef]
  78. Dominiak, B.C.; Worsley, P. Lesser Queensland fruit fly Bactrocera neohumeralis (Hardy) (Diptera: Tephritidae: Dacinae) not detected in inland New South Wales or south of Sydney. Gen. Appl. Entomol. 2016, 44, 9–15. [Google Scholar]
  79. Cameron, E.; Sved, J.; Gilchrist, A. Pest fruit fly (Diptera: Tephritidae) in northwestern Australia: One species or two? Bull. Entomol. Res. 2010, 100, 197–206. [Google Scholar] [CrossRef]
  80. Hancock, D.; Hamacek, E.; Lloyd, A.; Elson-Harris, M. The Distribution and Host Plants of Fruit Flies (Diptera: Tephritidae) in Australia; Information Series (Queensland Dept. of Primary Industries) (Q19906); Queensland Department of Primary Industries: Brisbane, Australia, 2000. [Google Scholar]
  81. Dominiak, B.C.; Millyn, B. A review of Bactrocera bryoniae (Tryon) and revised distribution in Asia and Australia, with a focus on New South Wales. Gen. Appl. Entomol. 2022, 50, 1–9. [Google Scholar]
  82. Royer, J.E. Responses of fruit flies (Tephritidae: Dacinae) to novel male attractants in north Queensland, Australia, and improved lures for some pest species. Austral Entomol. 2015, 54, 411–426. [Google Scholar] [CrossRef]
  83. Royer, J.E.; Wright, C.L.; Hancock, D.L. Bactrocera frauenfeldi (Diptera: Tephritidae), an invasive fruit fly in Australia that may have reached the extent of its spread due to environmental variables. Austral Entomol. 2016, 55, 100–111. [Google Scholar] [CrossRef]
  84. Dominiak, B.C.; Worsley, P. Review of the southern boundary of Jarvis fruit fly Bactrocera jarvisi (Tryon) (Diptera: Tephritidae: Dacinae) and its likley southern distribution in Australia. Gen. Appl. Entomol. 2017, 45, 1–7. [Google Scholar]
  85. Fay, H.A. A highly effective and selective male lure for Bactrocera jarvisi (Tryon) (Diptera: Tephritidae). Aust. J. Entomol. 2012, 51, 189–197. [Google Scholar] [CrossRef]
  86. Dominiak, B.C.; Nicol, H.I. Chemical analysis of male annihilation blocks used in the control of Queensland fruit fly Bactrocera tryoni (Froggatt) in New South Wales. Plant Prot. Q. 2012, 27, 31–35. [Google Scholar]
  87. Cunningham, R. Biology and physiology, parapheromones. In Fruit Flies: Their Biology, Natural Enemies and Control; Robinson, A.S., Hooper, G., Eds.; Elsevier: Amsterdam, The Netherlands, 1989. [Google Scholar]
  88. Mwatawala, M.; Virgilio, M.; Quilici, S.; Dominic, M.; De Meyer, M. Field evaluation of the relative attractiveness of enriched ginger root oil (EGO) lure and trimedlure for African Ceratitis species (Diptera: Tephritidae). J. Appl. Entomol. 2012, 137, 392–397. [Google Scholar] [CrossRef]
  89. Royer, J.E.; De Faveri, S.G.; Lowe, G.E.; Wright, C.L. Cucumber volatile blend, a promising female-biased lure for Bactrocera cucumis (French 1907) (Diptera: Tephritidae: Dacinae), a pest fruit fly that does not respond to male attractants. Austral Entomol. 2014, 53, 347–352. [Google Scholar] [CrossRef]
  90. Dominiak, B.C.; Worsley, P. Review of cucumber fruit fly, Bactrocera cucumis (French) (Diptera: Tephritidae: Dacinae) in Australia: Part 1, host range, surveillance and distribution. Crop Prot. 2018, 106, 79–85. [Google Scholar] [CrossRef]
  91. Follett, P.A.; Haynes, F.E.; Dominiak, B.C. Host suitability index for polyphagous tephritid fruit flies. J. Econ. Entomol. 2021, 114, 1021–1034. [Google Scholar] [CrossRef]
  92. Moquet, L.; Payet, J.; Glenac, S.; Delatte, H. Niche shift of tephritid species after the Oriental fruit fly (Bactrocera dorsalis) invasion in La Réunion. Divers. Distrib. 2021, 27, 109–129. [Google Scholar] [CrossRef]
  93. Follett, P.A.; Jamieson, L.; Hamilton, L.; Wall, M. New associations and host status: Infestability of kiwifruit by the fruit fly species Bactrocera dorsalis, Zeugodacus cucurbitae, and Ceratitis capitata (Diptera: Tephritidae). Crop Prot. 2019, 115, 113–121. [Google Scholar] [CrossRef]
  94. Grové, T.; de Jager, K.; Theledi, M.L. Fruit flies (Diptera: Tephritidae) and Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae) associated with fruit of the family Myrtaceae Juss. in South Africa. Crop Prot. 2019, 116, 24–32. [Google Scholar] [CrossRef]
  95. Follett, P.A.; Zee, F.T. Host status of Vaccinium reticulatum (Ericaceae) to invasive tephritid fruit flies in Hawaii. J. Econ. Entomol. 2011, 104, 571–573. [Google Scholar] [CrossRef]
  96. Leblanc, L.; Vueti, E.T.; Allwood, A.J. Host plant records for fruit flies (Diptera: Tephritidae: Dacini) in the Pacific Islands: 2. Infestation statistics on economic hosts. Proc. Hawaii. Entomol. Soc. 2013, 45, 83–117. [Google Scholar]
  97. Gonzalez, J.; Troncoso, P. The Fruit Fly Exclusion Programme in Chile. In Area-Wide Control of Insect Pests; Vreysen, M.J.B., Robinson, A.S., Hendrichs, J., Eds.; Springer: Dordrecht, The Netherlands, 2007. [Google Scholar] [CrossRef]
  98. Stewart, T.P.; Johanson, D.S. The SPS Agreement of the World Trade Organization and Plant Pest Infestations: A Case Study of the 1997 Mediterranean Fruit Fly Outbreak in Florida. Am. Univ. Int. Law Rev. 1999, 14, 1107. [Google Scholar]
  99. Plant Health Australia. PLANTPLAN: Australian Emergency Plant Pest Response Plan; Plant Health Australia: Canberra, ACT, Australia, 2022. [Google Scholar]
  100. Gillespie, P. Observations on fruit flies (Diptera: Tephritidae) in New South Wales. Gen. Appl. Entomol. 2003, 32, 41–47. [Google Scholar]
  101. Quilici, S.; Donner, P. Analysis of exotic fruit fly trapping networks. EPPO Bull. 2012, 42, 102–108. [Google Scholar] [CrossRef]
  102. Lloyd, A.; Leach, P.; Kopittke, R. Effects of exposure on chemical content and efficacy of male annihilation blocks used in the eradication of Bactrocera papayae in north Queensland. Gen. Appl. Entomol. J. Entomol. 1998, 28, 2–8. [Google Scholar]
  103. Bhagat, G.; Shankar, U.; Singh, A.K. Refinement of male annihilation technique (Mat) and bait attractant technique (Bat) for fruit flies. Pharma Innov. 2022, 11, 1182–1185. [Google Scholar]
  104. Shelly, T.E.; Kaneshiro, K.Y. Lek behavior of the oriental fruit fly, Dacus dorsalis, in Hawaii (Diptera: Tephritidae). J. Insect Behav. 1991, 4, 235–241. [Google Scholar] [CrossRef]
  105. Prokopy, R.; Papaj, D.; Hendrichs, J.; Wong, T. Behavioral responses of Ceratitis capitata flies to bait spray droplets and natural food. Entomol. Exp. Appl. 1992, 64, 247–257. [Google Scholar] [CrossRef]
  106. Prokopy, R.J.; Miller, N.W.; Piñero, J.C.; Barry, J.D.; Tran, L.C.; Oride, L.; Vargas, R.I. Effectiveness of GF-120 fruit fly bait spray applied to border area plants for control of melon flies (Diptera: Tephritidae). J. Econ. Entomol. 2003, 96, 1485–1493. [Google Scholar] [CrossRef]
  107. Allwood, A.; Vueti, E.; Leblanc, L.; Bull, R. Eradication of introduced Bactrocera species (Diptera: Tephritidae) in Nauru using male annihilation and protein bait application techniques. In Turning the Tide: The Eradication of Invasive Species. Proceedings of the International Conference on Eradication of Island Invasives; Veitch, C.R., Clout, M.N., Eds.; IUCN SSC Invasive Species Specialist Group. IUCN: Gland, Switzerland; Cambridge, UK, 2002. [Google Scholar]
  108. Dominiak, B. Review of the use of protein food based lures in McPhail traps for monitoring Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephhtidae). Gen. Appl. Entomol. 2006, 35, 7–12. [Google Scholar]
  109. Gilmore, J. Sterile insect technique (SIT). In Fruit Flies: Their biology, Natural Enemies and Control; Robinson, A.S., Hooper, G., Eds.; Elsevier: Amsterdam, The Netherlands, 1989; pp. 353–363. [Google Scholar]
  110. Putulan, D.; Sar, S.; Drew, R.A.; Raghu, S.; Clarke, A.R. Fruit and vegetable movement on domestic flights in Papua New Guinea and the risk of spreading pest fruit-flies (Diptera: Tephritidae). Int. J. Pest Manag. 2004, 50, 17–22. [Google Scholar] [CrossRef]
  111. Nugnes, F.; Russo, E.; Viggiani, G.; Bernardo, U. First record of an invasive fruit fly belonging to Bactrocera dorsalis complex (Diptera: Tephritidae) in Europe. Insects 2018, 9, 182. [Google Scholar] [CrossRef]
  112. Haynes, F.E.; Dominiak, B.C. Irradiation for phytosanitary treatment of the Queensland fruit fly Bactrocera tryoni Froggatt benefits international trade. Crop Prot. 2018, 112, 125–132. [Google Scholar] [CrossRef]
  113. Jessup, A.J. Response of ‘Lambert’ and ‘Ron’s Seedling’ sweet cherries to fumigation with methyl bromide plus cold storage. Aust. J. Exp. Agric. 1988, 28, 431–434. [Google Scholar] [CrossRef]
  114. Jang, E.B.; Chan, H.T. Thermal Death Kinetics: Importance in development of heat-based quarantine treatments. In Fruit Flies; Aluja, M., Liedo, P., Eds.; Springer: New York, NY, USA, 1993. [Google Scholar] [CrossRef]
  115. Jessup, A.; Dominiak, B.; Woods, B.; De Lima, C.; Tomkins, A.; Smallridge, C. Area-wide management of fruit flies in Australia. In Area-Wide Control of Insect Pests; Vreysen, M.J.B., Robinson, A.S., Hendrichs, J., Eds.; Springer: Dordrecht, The Netherlands, 2007; pp. 685–697. [Google Scholar] [CrossRef]
  116. Akter, H.; Cunningham, N.; Rempoulakis, P.; Bluml, M. An overview of phytosanitary irradiation requirements for Australian pests of quarantine concern. Agriculture 2023, 13, 771. [Google Scholar] [CrossRef]
  117. Inspector-General of Biosecurity. Pest and Disease Interceptions and Incursions in Australia; Inspector-General of Biosecurity: Canberra, Australia.
  118. Camac, J.; Baumgartner, J.; Robinson, A.; Elith, J.; Subasinghe, R.; Stanaway, M.; Collins, S.; Gibert, A.; Hill, M.; Caley, P. Developing Pragmatic Maps of Establishment Likelihood for Plant Pests; Technical Report for CEBRA Project 170607; CEBRA: Melbourne, Australia, 2020. [Google Scholar]
  119. Burnett, W.; Enkerlin, W.; Gilmore, J.; Rendon, P.; Smith, C.; Zavala, J. International Panel for Review of the Fruit Fly Surveillance Programs in the United States; United States Department of Agriculture/APHIS/PPQ/Fruit Fly Program: Riverdale, MD, USA, 2006. [Google Scholar]
  120. Cowley, J. A new system of fruit fly surveillance trapping in New Zealand. N. Z. Entomol. 1990, 13, 81–84. [Google Scholar] [CrossRef]
  121. Frampton, E. An overview of quarantine for fruit flies. In Proceedings of the Area-Wide Control of Fruit Flies and Other Insect Pests. Joint Proceedings of the International Conference on Area-Wide Control of Insect Pests, 28 May–2 June 1998 and the Fifth International Symposium on Fruit Flies of Economic Importance, Penang, Ma-laysia, 1–5 June 1998; Penerbit Universiti Sains Malaysia: Gelugor, Malaysia, 2000; pp. 475–479. [Google Scholar]
  122. Steck, G.J.; Fox, A.J.; Carrillo, D.; Dean, D.; Roda, A.; Epsky, N.D.; Smith, T.R. Oriental fruit fly eradication in Florida 2015–2016 program implementation, unique aspects, and lessons learned. Am. Entomol. 2019, 65, 108–121. [Google Scholar] [CrossRef]
  123. Stringer, L.D.; Soopaya, R.; Butler, R.C.; Vargas, R.I.; Souder, S.K.; Jessup, A.J.; Woods, B.; Cook, P.J.; Suckling, D.M. Effect of lure combination on fruit fly surveillance sensitivity. Sci. Rep. 2019, 9, 2653. [Google Scholar] [CrossRef]
  124. FAO-IAEA (Ed.) Trapping Guidelines for Area-Wide Fruit Fly Programmes, 2nd ed.; FAO/IAEA: Rome, Italy, 2018. [Google Scholar]
  125. Kay, B.J. The complexity of competition between three native Australian fruit fly species, Bactrocera tryoni, B. neohumeralis and B. jarvisi in a Changing Environment. Ph.D. Thesis, Queensland University of Technology: Brisbane, Australia, 2023. [Google Scholar] [CrossRef]
  126. Biasazin, T.D.; Wondimu, T.W.; Herrera, S.L.; Larsson, M.; Mafra-Neto, A.; Gessese, Y.W.; Dekker, T. Dispersal and competitive release affect the management of native and invasive tephritid fruit flies in large and smallholder farms in Ethiopia. Sci. Rep. 2021, 11, 2690. [Google Scholar] [CrossRef]
  127. Smith, E. Internal and external fruit fly quarantine in Australia. In Proceedings of the Indian Ocean Commission, Regional Fruit Fly Symposium, Flic en Flac, Mauritius, 5–9 June 2000; Indian Ocean Commission: Quatre Bornes, Mauritius, 2000; pp. 171–177. [Google Scholar]
  128. Maelzer, D.; Bailey, P.T.; Perepelicia, N. Factors supporting the non-persistence of fruit fly populations in South Australia. Aust. J. Exp. Agric. 2004, 44, 109–126. [Google Scholar] [CrossRef]
  129. Fay, H.; Drew, R.; Lloyd, A. Eradication program for papaya fruit fly (Bactrocera papayae Drew and Hancock) in north Queensland. In Management of Fruit Flies in the Pacific, Proceedings of the A Regional Symposium, Nadi, Fiji, 28–31 October 1996; ACIAR Proceedings No. 76; Allwood, A.J., Drew, R.A.I., Eds.; ACIAR: Canberra, Australia, 1997. [Google Scholar]
  130. Bain, C.; Dominiak, B.C. Evaluating a new trap design for the surveillance of Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera:Tephritidae) in southern Australia. Gen. Appl. Entomol. 2022, 50, 21–24. [Google Scholar]
  131. Dominiak, B.; Galvin, T.; Deane, D.; Fanson, B. Evaluation of Probodelt cone traps for surveillance of Dacinae in New South Wales, Australia. Crop Prot. 2019, 126, 104940. [Google Scholar] [CrossRef]
  132. Voice, D.; MacLellan, R. Alternative Insecticides for Fruit Fly Traps in New Zealand; Ministry for Primary Industries: Wellington, New Zealand, 2020. [Google Scholar]
  133. Kean, J.M.; Suckling, S.D.; Sullivan, N.J.; Tobin, P.C.; Stringer, L.D.; Smith, G.R.; Kimber, B.; Lee, D.C.; Flores Vargas, R.; Fletcher, J.; et al. Global Eradication and Response Database. 2023. Available online: http://b3.net.nz/gerda (accessed on 18 April 2023).
  134. Seewooruthun, S.; Sookar, P.; Permalloo, S.; Joomaye, A.; Alleck, M.; Gungah, B.; Soonnoo, A. An attempt to the eradication of the Oriental fruit fly, Bactrocera dorsalis (Hendel) from Mauritius. In Proceedings of the Second Annual Meeting of Agricultural Scientists, Reduit, Mauritius, 12–13 August 1997; Lalouette, J.A., Bachraz, D.Y., Sukurdeep, N., Seebaluck, B.D., Eds.; Food and Agricultural Research Council: Redult, Mauritius, 1997; pp. 181–187. [Google Scholar]
  135. Pather, V.; MacLellan, R.; King, K. National Fruit Fly Surveillance Programme Annual Report. Surveillance 2019, 46, 83–86. [Google Scholar]
  136. Koyama, J.; Kakinohana, H.; Miyatake, T. Eradication of the melon fly, Bactrocera cucurbitae, in Japan: Importance of behavior, ecology, genetics, and evolution. Annu. Rev. Entomol. 2004, 49, 331–349. [Google Scholar] [CrossRef]
  137. Vargas, R.I.; Stark, J.D.; Mackey, B.; Bull, R. Weathering trials of Amulet cue-lure and Amulet methyl eugenol “attract-and-kill” stations with male melon flies and oriental fruit flies (Diptera: Tephritidae) in Hawaii. J. Econ. Entomol. 2005, 98, 1551–1559. [Google Scholar] [CrossRef]
  138. Pinero, J.; Mau, R.; Vargas, R. Managing oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae), using spinosad-based protein bait sprays in papaya orchards in Hawaii. J. Econ. Entomol 2009, 102, 1123–1132. [Google Scholar] [CrossRef] [PubMed]
  139. Smith, D.; Nannan, L. Yeast autolysate bait sprays for control of Queensland fruit fly on passionfruit in Queensland. Qld. J. Agric. Anim. Sci. 1988, 45, 169–177. [Google Scholar]
  140. Dominiak, B.C.; Mapson, R. 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. 2017, 110, 2459–2465. [Google Scholar] [CrossRef]
  141. Dominiak, B.C.; Ekman, J.H. The rise and demise of control options for fruit fly in Australia. Crop Prot. 2013, 51, 57–67. [Google Scholar] [CrossRef]
  142. Klassen, W.; Curtis, C.; Hendrichs, J. History of the sterile insect technique. In Sterile Insect Technique; Dyck, D.A., Hendrichs, J., Robinson, A.S., Eds.; CRC Press: Boca Raton, FL, USA, 2021; pp. 1–44. [Google Scholar]
  143. Monro, J.; Osborn, A. The use of sterile males to control populations of Queensland fruit fly Dacus tryoni (Frogg) (Diptera: Tephritidae) I. methods of mass rearing, transporting, irradiating and releasing sterile flies. Aust. J. Zool. 1967, 15, 461–473. [Google Scholar] [CrossRef]
  144. Andrewartha, H.; Monro, J.; Richardson, N. 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. 1967, 15, 475–499. [Google Scholar] [CrossRef]
  145. Kompas, T.; Che, T. A Practical Optimal Surveillance Measure: The Case of Papaya Fruit Fly in Australia; Australian Centre for Biosecurity and Environmental Economics, ANU: Canberra, ACT, Australia, 2009. [Google Scholar]
  146. Hancock, D.L. A revised checklist of Australian fruit flies (Diptera: Tephritidae). Aust. Entomol. 2013, 40, 219–236. [Google Scholar]
  147. Popa-Báez, Á.-D.; Lee, S.F.; Yeap, H.L.; Westmore, G.; Crisp, P.; Li, D.; Catullo, R.; Cameron, E.C.; Edwards, O.R.; Taylor, P.W. Tracing the origins of recent Queensland fruit fly incursions into South Australia, Tasmania and New Zealand. Biol. Invasions 2021, 23, 1117–1130. [Google Scholar] [CrossRef]
  148. Froggatt, W. Report on Parasitic and Injurious Insects 1907–08. Part III. Fruit Flies. Official Report On Fruit Fly and Other Pests in Various Countries; W.A. Gullick, Government Printer: Sydney, Australia, 1909. [Google Scholar]
  149. Permkam, S.; Hancock, D. Australian Ceratitinae (Diptera: Tephritidae). Invertebr. Taxon. 1994, 8, 1325–1341. [Google Scholar] [CrossRef]
  150. National Fruit Fly Council. National Fruit Fly Strategy; Plant Health Australia: Canberra, ACT, Australia, 2020. [Google Scholar]
  151. Anderson, C.; Low-Choy, S.; Whittle, P.; Taylor, S.; Gambley, C.; Smith, L.; Gillespie, P.; Löcker, H.; Davis, R.; Dominiak, B. Australian plant biosecurity surveillance systems. Crop Prot. 2017, 100, 8–20. [Google Scholar] [CrossRef]
  152. Stephens, A.; Kriticos, D.J.; Leriche, A. The current and future potential geographical distribution of the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Bull. Entomol. Res. 2007, 97, 369–378. [Google Scholar] [CrossRef]
  153. Raghu, S.; Clarke, A.R.; Drew, R.A.; Hulsman, K. Impact of habitat modification on the distribution and abundance of fruit flies (Diptera: Tephritidae) in Southeast Queensland. Popul. Ecol. 2000, 42, 153–160. [Google Scholar] [CrossRef]
  154. De Villiers, M.; Hattingh, V.; Kriticos, D.J.; Brunel, S.; Vayssières, J.-F.; Sinzogan, A.; Billah, M.; Mohamed, S.; Mwatawala, M.; Abdelgader, H. The potential distribution of Bactrocera dorsalis: Considering phenology and irrigation patterns. Bull. Entomol. Res. 2016, 106, 19–33. [Google Scholar] [CrossRef]
  155. Dominiak, B.; McLeod, L.; Landon, R.; Nicol, H. Development of a low-cost pupal release strategy for Sterile Insect Technique (SIT) with Queensland fruit fly and assessment of climatic constraints for SIT in rural New South Wales. Aust. J. Exp. Agric. 2000, 40, 1021–1032. [Google Scholar] [CrossRef]
  156. Hadwen, W.; Small, A.; Kitching, R.; Drew, R. Potential suitability of North Queensland rainforest sites as habitat for the Asian papaya fruit fly, Bactrocera papayae Drew and Hancock (Diptera: Tephritidae). Aust. J. Entomol. 1998, 37, 219–227. [Google Scholar] [CrossRef]
  157. Reynolds, O.L.; Collins, D.; Dominiak, B.C.; Osborne, T. No sting in the tail for sterile bisex Queensland fruit fly (Bactrocera tryoni Froggatt) release programs. Insects 2022, 13, 269. [Google Scholar] [CrossRef] [PubMed]
  158. Kimbokota, F.; Hassanali, A.; Njagi, P.G.N. Potential attractants from three host plants of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Int. J. Trop. Insect Sci. 2022, 43, 107–114. [Google Scholar] [CrossRef]
  159. Reynolds, O.L.; Osborne, T.J.; Barchia, I. Efficacy of chemicals for the potential management of the Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Insects 2017, 8, 49. [Google Scholar] [CrossRef]
  160. Duyck, P.F.; Quilici, S. Survival and development of different life stages of three Ceratitis spp. (Diptera: Tephritidae) reared at five constant temperatures. Bull. Entomol. Res. 2002, 92, 461–469. [Google Scholar] [CrossRef] [PubMed]
Table 5. List of area-wide control options for fruit flies.
Table 5. List of area-wide control options for fruit flies.
Control Strategy/TypeDescription
SurveillanceLure-based traps (para-pheromone or ammonia-based) used to monitor areas of concern (i.e., ports of entry, horticultural areas [100] for an incursion. Usually set up in a grid pattern [101].
Quarantine zonesAreas that restrict the movement of potentially infected fruit and vegetables to create “fly free” zones, this could be a country, an area of high horticultural value or an incursion area within a country [86].
Cultural controlThe use of physical control techniques, such as crop sanitation and hygiene e.g., wrapping fruit, removal, and destruction of fallen fruits, digging up the ground to destroy pupae.
Cover spraysSpraying pesticides directly onto affected crops.
Male annihilation technique (MAT)Para-pheromone lures (e.g., methyl eugenol) and an insecticide (e.g., malathion) are impregnated into caneite (compressed fibreboard) [102], cordelitos (cotton wicks), coconut husks, compressed cardboard [18] or plastics [103] to lure and kill males so that mating is compromised [104].
Bait application technique (BAT) or protein bait spraysAn insecticide (malathion [105], spinosad [106], fipronil [107]) and protein source (protein hydrolysate [103] or protein autolysate [108]) is applied to the foliage of host crops, usually only along the borders of the crop or in targeted areas.
Sterile insect technique (SIT)Mass-rearing and releasing millions of sterile flies into a wild population of flies, the intended outcome that females will mate with sterile males and not produce fertile eggs which in turn reduces the population [109].
Biological control agents (BCAs)Natural control agents such as predators, parasitoids (wasps and flies), fungi, nematodes, bacteria and viruses to reduce populations [25].
Table 6. Successful eradication programs for the five tephritid fruit fly species of biosecurity concern to Australia and methods used in the eradication process.
Table 6. Successful eradication programs for the five tephritid fruit fly species of biosecurity concern to Australia and methods used in the eradication process.
SpeciesLocationIncursion/sEradication Program/sMethod/s of Eradication
Anastrepha ludens
Mexican fruit fly		California, USA (multiple locations)2000sMultiple programs 1990–2009BAT (spinosad), quarantine and movement control and SIT
Mexico (multiple locations)1980s1992–1994Natural enemies (parasitoids), BAT, host removal
and destruction, quarantine and movement control, and SIT
Texas, United States (multiple locations)2008, 2011, 20132008–2013BAT (spinosad or malathion), host removal or destruction, and SIT
Bactocera carambolae
carambola fruit fly		Guyanaunknown1988–2002BAT, MAT, quarantine and movement control
Brazil19961998–1998BAT
Bactrocera dorsalis
Oriental fruit fly *		Rota Island, USAunknown1962–1963MAT (methyl eugenol and naled impregnated cane fibre squares)
Guamunknown1963–1965SIT
Mariana Islands, USAunknown1964–1964MAT and SIT
Kikajima Island, Japan19291968–1978MAT
Amami Islands, Japan19461974–1978MAT
San Diego, California, USA19741974–1975MAT, BAT, quarantine and movement control,
Okinawa Islands, Japan19191977–1985SIT
Mauritius19961996–1998Destruction of infested fruit, MAT, BAT, cover sprays, soil drenching [134]
Nauru19921998–1999MAT (fipronil and methyl eugenol)
Queensland, Australia (Cairns (primary incursion site), Mt Isa, Humpty Do and Darwin)1995–19971995–1999Quarantine and movement control, MAT (fibreboard blocks with methyl eugenol and malathion), BAT (malathion)
Torres Strait Islands, AustraliaOngoing seasonal incursions [18]Multiple programs 1996–ongoing [18]MAT (caneite blocks laced with malathion), BAT (malathion or spinosad) [18]
Florida, USA1964 ongoing (multiple minor incursions) [122] Multiple programs 1995–2016MAT (methyl eugenol and naled), soil drench (diazinon and later lambda-cyhalothrin), host removal and destruction, BAT (spinosad), quarantine and movement control [122]
California, USA (multiple locations in Los Angeles and Sacramento)2006–2013Multiple programs 2006–2013MAT, quarantine, and movement control
Easter Island20102010–2011BAT (spinosad), MAT, destruction of infested fruit
South Africa (multiple locations)20102010–2011MAT (fibreboard blocks with methyl eugenol and malathion), BAT (GF-120 and LokLure with malathion), orchard sanitation
Bactrocera tryoni
Queensland fruit fly		Easter Island, Chile19711972BAT (hydrolysed protein and malathion), MAT (cuelure and malathion impregnated cordelito)
South Australia, Australia (multiple urban sites–re-occurring minor incursions from NSW)1987–1994Multiple programs 1987–1994BAT (maldison with protein attractant), removal and destruction of fruit, cover spray (fenthion)
Perth, Western Australia, Australia1989, 20111989–1990, 2011BAT (spinosad, Naturalure), MAT and SIT
Cook Islands20012001–2003Destruction of infested fruit, quarantine and movement control, BAT
Ti Tree, Northern Territory (re-occurring minor incursions)2000–2009Multiple programs 2000–2009BAT (spinosad and malathion baits), cover sprays, removal and destruction of infested fruits
South Australia, Australia (multiple urban sites–re-occurring minor incursions from NSW)2002–2014Multiple programs 2002–2014Removal and destruction of fruit, BAT (maldison with protein attractant) and SIT, black plastic on soil under trees to break lifecycle
Auckland, New Zealand2015, 20192015, 2019Quarantine and movement control, host collection and disposal, MAT (methyl eugenol and dichlorvos) and BAT (fipronil or spinetoram) [135]
Ceratitis capitata
Mediterranean fruit fly		New Zealand (multiple sites)1906, 1907 and 1996Multiple programs 1906–1907, 1996Presumed to be fruit destruction and soil drenches of kerosene (early eradications). BAT (malathion), host removal and destruction.
Bermuda19071907–1963BAT (malathion and protein attractant), ground application of dieldrin, MAT baits with trimedlure and dichlorvos
Florida (multiple locations), USA1929 ongoing (re-occurring minor incursions)Multiple programs 1930–2011Ground application of arsenical molasses followed by copper carbonate, host removal and destruction, BAT (malathion and later spinosad), soil drench of dieldrin and later on diazinon and spinosad, quarantine and movement control
Texas, USA19661966BAT (malathion and protein attractant)
South Australia, Australia (multiple locations)1968 ongoing (re-occurring minor incursions)Multiple programs 1968–2019BAT (malathion and later spinosad), SIT, cover spray (fenthion) and ground drench (chlorpyrifos and later lambda-cyhalothrin), quarantine zone, removal and destruction of fruit (treatment with malathion)
California, USA (multiple locations)1975 ongoing (re-occurring minor incursions)Multiple programs 1975–2006BAT (malathion and later spinosad), SIT, host removal and destruction, quarantine, and movement control
Alice Springs, Northern Territory, Australia1976, 1981 & 1986Multiple programs 1976–1986BAT (malathion), host removal and destruction, cover sprays of trichlorfon, fenthion (for destroyed fruit) and dimethoate, MAT (trimedlure and dichlorvos)
Guatemala (multiple locations)19771977–2013BAT (malathion and later spinosad), SIT
Chile (multiple locations)1963 ongoing (re-occurring minor incursions)Multiple programs 1990–2013BAT (malathion and spinosad), SIT, host removal and destruction, quarantine and movement control, soil drench
Tacna, Peru19571990–2007SIT
Argentina (multiple locations)1992 and 1997Multiple programs 1992–2012BAT, host removal and destruction, SIT, cover spray, quarantine and movement control
Belize19871997–2001BAT (malathion and later spinosad)
Managua, Nicaragua19942004–2012BAT, quarantine and host removal
Dominican Republic20152015–2017SIT
Zeugodacus cucurbitae
melon fly		Rota Island, United Statesunknown1962–1963SIT
Southwestern Islands, Japan19721972–1993SIT [136]
Nauru1992, 20011998–2001MAT (caneite blocks with methyl eugenol/fipronil) and BAT (fipronil)
Kern County, California, United Statesunknown2010–2011MAT
All data are summarised from the Global eradication and response database (GERDA) [133] unless otherwise stated. * Includes data from Bactrocera dorsalis synonymy.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Hoskins, J.L.; Rempoulakis, P.; Stevens, M.M.; Dominiak, B.C. Biosecurity and Management Strategies for Economically Important Exotic Tephritid Fruit Fly Species in Australia. Insects 2023, 14, 801. https://doi.org/10.3390/insects14100801

AMA Style

Hoskins JL, Rempoulakis P, Stevens MM, Dominiak BC. Biosecurity and Management Strategies for Economically Important Exotic Tephritid Fruit Fly Species in Australia. Insects. 2023; 14(10):801. https://doi.org/10.3390/insects14100801

Chicago/Turabian Style

Hoskins, Jessica L., Polychronis Rempoulakis, Mark M. Stevens, and Bernard C. Dominiak. 2023. "Biosecurity and Management Strategies for Economically Important Exotic Tephritid Fruit Fly Species in Australia" Insects 14, no. 10: 801. https://doi.org/10.3390/insects14100801

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop