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Review of cucumber fruit fly, Bactrocera cucumis (French) (Diptera: Tephritidae: Dacinae): Part 2, biology, ecology and control in Australia
Crop Protection 104 (2018) 35–40
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Crop Protection journal homepage: www.elsevier.com/locate/cropro
Review of cucumber fruit fly, Bactrocera cucumis (French) (Diptera: Tephritidae: Dacinae): Part 2, biology, ecology and control in Australia
MARK
Bernard C. Dominiak New South Wales Department of Primary Industries, 161 Kite Street, Orange, New South Wales 2800, Australia
A R T I C L E I N F O
A B S T R A C T
Keywords: Cucurbit Reproduction Rearing Disinfestation
Bactrocera cucumis is one of many fruit fly species of concern for Australia's international trade partners. This species is one of the lesser known native fruit flies in Australia and its distribution and hosts have been reviewed. Eggs are larger than in most other species with a short hatching period. The adults and larvae are also larger than most other Australian fruit flies. Adults are long lived and have a high rate of reproduction. Stridulation and pheromones appear not to be used in the mating process. Adults can be managed using a range of measures including chemosterilants, the sterile insect technique and chemical sprays. Produce can be disinfested using a range of post-harvest treatments. Current export protocols include hot air and chilling treatments, irradiation, methyl bromide fumigation and winter window.
1. Introduction In Asia and the Pacific regions, Dacine fruit flies (Diptera: Tephritidae: Dacinae) are key pests, adversely impacting food production and international trade. Larval stages feed on a broad range of fruit and vegetables causing direct damage, fruit drop and loss of export markets (Dominiak et al., 2015). In the last century, fruit fly research in Australia has concentrated on the major economic species such as Queensland fruit fly Bactrocera tryoni (Froggatt) (Qfly) and Mediterranean fruit fly Ceratitis capitata (Weidemann) (Medfly) (Dominiak and Daniels, 2012). As knowledge on these species improves, other fruit fly species are now being increasingly studied. Cucumber fruit fly Bactrocera cucumis (French) is the main pest of cucurbits in Australia and is a species that has been less well studied (Anon, 2014a). The hosts, lures and distribution of this species were reviewed by Dominiak and Worsley (Submitted). In this manuscript review, the published reports covering biology, ecology and controls of B. cucumis are reviewed, and research gaps identified.
(Austrodacus) cucumis and B. (Papuodacus) neopallescentis were nested in the B. (Zeugodacus) clade that seems to have diverged from the Dacus clade in the early Paleogene period. Zeugodacus and Bactrocera groups appear to have experienced increased speciation rates in the last 25–50 million years. Zeugodacus is an almost entirely monophyletic sister group to Dacus. Krosch et al. (2012) noted that it is important for applied workers to recognise that significant pest taxa of the Zeudodacus group, such as Zeugodacus cucurbitae (Coquillet), B. cucumis and B. tau (Walker), are more closely related to African Dacus species than they are to Asian pest species such as B. dorsalis (Hendel). Using mitochondrial analysis, Nakahara and Muraji (2008) also found that B. cucumis, B. tau and B. cucurbitae all had a common origin. Bactrocera cucurbitae and B. tau are attracted to cuelure; B. dorsalis is attracted to methyl eugenol and B. cucumis is not attracted to cuelure or methyl eugenol. Virgilio et al. (2015) have inferred higher phylogeny of frugivorous fruit flies (Diptera, Tephritidae, Dacini) from mitochondrial and nuclear gene fragments.
2. Phylogenetic placement
3. Taxonomy
Krosch et al. (2012) undertook a detailed genetic analysis of the tribe Dacini. While the analysis may have been directed at more economically important fruit flies, the evolution of B. cucumis was also identified. Bactrocera cucumis falls under the Zeugodacus group. All but two members of the Zeugodacus group of subgenera (including B. (Zeugodacus)) formed a clade that was more closely related to Dacus than Bactrocera. The species B. (Sinodacus) abdopallescens, B.
French (1907) originally described some morphology of Dacus cucumis and indicated it was a variant of Dacus tryoni var. cucumis. Froggatt (1910) described more adult morphology and supported the formation of a new species due to the differences to Dacus tryoni. Tryon (1926) provided a detailed key of all life stages and identified D. cucumis as a new species but noted that this insect was an exceptional species of Dacus due to the presence of four scutellar bristles,
E-mail address: [email protected]. http://dx.doi.org/10.1016/j.cropro.2017.10.005 Received 21 April 2017; Received in revised form 26 September 2017; Accepted 4 October 2017 0261-2194/ © 2017 Elsevier Ltd. All rights reserved.
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Queensland and females enter the fields to lay eggs (Allwood 1997; Balagawi et al., 2014). Numerous samples of adult B. cucumis were collected from the leaves of Ficus racemosa L. to start a laboratory culture in Northern Territory because B. cucumis was not known to infest commercial fruit (Smith et al., 1988). Senior et al. (2017) reported that bait sprays were best placed on vegetation surrounding crops as these roosting sites were preferred by B. cucumis. Bactrocera tryoni also rest in non-crop areas near host crops (Balagawi et al., 2014) and these plants, such as Ficus, may offer features such as resting sites, protection from predators, food not found elsewhere or other attributes to support life.
uncommon in other fruit flies at that time. Perkins (1937) also claimed it was necessary to create a new genus for cucumis as it was so different from the other Dacinae. Perkins placed the species in Dacus in the new Austrodacus genus. It was very easily distinguished from other genera with four bristles by the absence of both a.sa and pr.sc bristles (Perkins, 1937). The species was described in detail by Hardy (1951) and Hardy claimed that Dacus (Zeugodacus) was a group close to Dacus (Strumeta) differing only by possessing four scutellar bristles rather than two. Drew (1972) reviewed many species and noted that morphologically the supernumerary lobe is present in the male wing and was very strong in most species of Zeugodacus. In B. cucumis, the posterior lobe of the surstylus was extremely long and more so than in other species of Dacus group of the subgenera. Bactrocera cucurbitae possesses a long posterior lobe on surstylus and abdominal sternite (Drew, 1972). Drew (1989) placed B. cucumis in the Zeugodacus subgenera under the subgenus Austrodacus.
4.3. Chemical spiroketals Male tephritids store pheromones in a reservoir and secrete it from a sac: both organs are located in the lower rectal area. The release of pheromone is generally associated with courting behaviour, but females may respond to other stimuli (Fletcher and Kitching, 1995). Some species such as B. tryoni use stridulation combs to disperse these pheromones, however B. cucumis do not have these combs (Tychen, 1977). Kitching et al. (1989) found 14 compounds in rectal glands of male B. cucumis. Fletcher and Kitching (1995) reported that extracts of male B. cucumis rectal glands showed the presence of one major component (about 60%) ((E,E)- (E,E)-2,8-dimethyl-1, 7-dioxapiro [5.5]undecane) and several minor components. Kitching et al. (1989) also reported on the E,Z, and Z,Z diastereomers of (E,E)-2,8-dimethyl-1, 7dioxapiro [5.5]undecane making up 5% and 8% respectively. Perkins et al. (1992) reported minor amounts of Z, E isomers. The other two main components were 3-hydroxy-2, 8-dimethyl-1,7-dioxaspiro[5.5] (15%) and (R)-(-)-1,3-nonanediol (10%) (Kitching et al., 1989). Some of these minor compounds were also detected in male rectal glands of B. tryoni and B. cacuminatus (Hering) (Perkins et al., 1992). Sexually excited B. tryoni males excrete an oily blend of six amides, which function as a short range attractant and invoke responses in mature females (Fletcher and Kitching, 1995). Analysis of the volatile emissions from B. tryoni females revealed that major components were N-(3-methylbutyl)propanamide and the spiroacetal (E,E)-2,8-dimethyl1, 7-dioxapiro [5.5]undecane which is present in a wide variety of insects including B. cucumis (Booth et al., 2006). Fletcher et al. (2002) reported the spiroacetals 3 and 4 from B. cucumis incorporate one ring oxygen from water and one ring oxygen (and the hydroxyl oxygen in 4) from [1802]-dioxygen. This discovery revealed the generality of monoxygenase mediation of spiroacetal formation in Bactrocera sp. and also the unexpected complexity in their biosynthesis. McErlean et al. (2002) studied this complexity further.
4. Biology and host damage 4.1. Egg, larval and pupal stages Comparing eight fruit fly species of Dacus, Fitt (1990) found that B. cucumis produced the largest eggs (1.34 mm), with the shortest incubation time at 25 °C (approximately 24 h). A similar finding was reported for two other cucurbit specialists: B. cucurbitae produced large eggs which hatched in less than two days (Vargas et al., 1984; Dhillon et al., 2005) and in B. tau eggs hatched in about 1.3 days (Singh et al., 2010). Overall development time of B. cucumis, B. cucurbitae and B. tau is also short relative to other species. Development from egg to adult at 25 °C and 65% relative humidity was recorded as 16.9 and 17.0 days respectively for male and female B. cucumis (Vuttanatungum and Hooper, 1974), as little as 13 days in B. cucurbitae at 29 °C (Dhillon et al., 2005) and 14 days at 25 °C and 65% relative humidity in B. tau (Singh et al., 2010). In comparison, development of B. tryoni from egg to adult was recorded as 20–34.5 days (at 30 °C and 20 °C respectively) by Bateman (1967). Fletcher (1989) suggested that the fast development time of B. cucumis offered a greater chance of survival and may be connected to the internal environment of the host fruits. Vargas et al. (2000) also claimed two distinctly different life history patterns (1) early reproduction, short life span, and a high intrinsic rate of increase, and (2) later onset of reproduction, longer life span, and a lower intrinsic rate of increase such as B. cucurbitae. In a laboratory held at 25 °C and 65% relative humidity, Vuttanatungum and Hooper (1974) found that egg hatch of B. cucumis was 84 per cent. Mature larvae began to leave the larval media five days after hatching and continued to leave for another five days. Mean larval life was 6.5 days and survival averaged 81 per cent. The duration of the pupal period was 10–11 days. May (1946) and Anon (2014a) reported that larvae mature in 7–10 days in summer and emerge from fruit to pupate in the soil, similar to most fruit flies. The pupal stage is completed in about 10 days. The entire life cycle is completed in about 2.5 weeks in summer (May, 1946). Bactrocera cucumis larvae were described in detail by Exley (1955). They are a deeper colour than those of B. tryoni, with a habit of curling and jumping further than other fruit fly larvae (French, 1907). Over fifty larvae may infest one cucumber (French, 1907).
4.4. Life span Unlike most other fruit flies, the adults are long lived and can survive for up to six months in laboratory conditions (Vuttanatungum and Hooper, 1974; Anon, 2014a). Again in laboratory conditions, B. cucumis females lived up to 274 days (Chinajariyawong et al., 2010). By comparison, Fanson et al. (2014) found the LD50 of B. tryoni in ideal laboratory conditions was 72.5 days. However the mean longevity was 54 h without food or water in the laboratory (Dominiak et al., 2014) so finding adequate resources is important. The genetically close B. cucurbitae is also long lived, surviving up to 249 days in the laboratory (Dhillon et al., 2005). Similarly B. tau can live for more than six months in the laboratory (Chang and Ying, 2000). Kabir et al. (1997) reported two population peaks per year in spring and autumn. Another Australian native fly Dacus newmani (Perkins) also has a long life span with only two generations per year (Gillespie, 2003). The mean weights of male and female B. cucumis were 10.99 mg and 17.51 mg respectively, compared with 13.03 mg and 14.33 mg respectively for B. tryoni (Atuahene and Hooper, 1971).
4.2. Adult behaviour In contrast to B. tryoni, B. cucumis is reputed in one reference to be attracted to packing sheds and can infest produce on the packing line (Anon, 2014a). However there is no published research to support this claim. Papaya fruit ripening on trees or possibly in packing sheds may be attacked, but mature green to a quarter coloured fruit are likely to escape damage (Anon, 2014a). Several fruit fly species, including B. cucumis, inhabit vegetation around the edges of zucchini crops in 36
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reported sourcing adults from Brisbane laboratories but provided no details for the maintenance of fruit fly colonies.
4.5. Reproduction and mating Bactrocera cucumis is capable of a high rate of reproduction. According to Vuttanatungum and Hooper (1974) females produced up to 1300 eggs during the first 14 weeks of life but may live for up to eight months. Egg production declined after the sixth week. Both male and female B. cucumis became sexually mature after 15–18 days at 25 °C. Vuttanatungum and Hooper (1974) claimed males were capable of mating daily but more commonly mated about three times in a five day period. However, Chinajariyawong et al. (2010) found that, in laboratory conditions, 52% of B. cucumis pairs mated three times with a maximum of five times over a 274 day period. The refractory period was at least twice as long as B. tryoni. Mankin et al. (2008) reported that male B. tryoni use a combination of pheromone and stridulation to attract females into the mating site. However, Hooper (1975a) claimed that preliminary research failed to demonstrate any involvement of a male pheromone in the mating sequence of B. cucumis. This species also lacks stridulation combs, indicating that stridulation does not occur (Tychen, 1977). Male B. tryoni may form a flying swarm that gathers towards the top of trees (Tychen, 1977). The closely related B. cucurbitae also displays the lek mating behaviour with male aggregations gathering on non-host plants (Iwashashi and Majima, 1986). Hooper (1976) stated that B. cucumis mate at dusk. Bactrocera cucurbitae also mate at dusk and copulation continues until dawn (Suzuki and Koyama, 1980; Kuba and Soemori, 1988). Similarly B. tau mate at dusk with a duration of up to 12 h (Chang and Ying, 2000). Hooper (1975a) claimed that mating in B. cucumis was very similar to that of Rhagoletis pomonella (Walsh) (Prokopy and Bush, 1973), in which the act of copulation was closely associated with oviposition into fruit (Prokopy et al., 1971). In R. pomonella, arrival at fruit was triggered on the basis of visual cues. Once in close range (within 50 cm), the visual stimulus was important in eliciting the courtship approach of the male. Visual cues therefore play an important role in location of both fruit and potential mates (Prokopy et al., 1972). Compared to sexually active flies, immature flies have a low incidence on host fruit. Anon (2014a) also noted that adults are attracted to and feed on bacterial colonies on the surface of foliage. They mate at these feeding sites and later lay eggs into the fruit, particularly into ripe and damaged fruit (Anon, 2014a). Drew (1997) claimed that B. cucumis was trapped in surrounding vegetation but rarely in traps placed within a cucurbit crop. This behaviour of entering host areas primarily for oviposition is similar to that of B. cucurbitae (Nishida and Bess, 1957) a species genetically close to B. cucumis (Krosch et al., 2012; Nakahara and Muraji, 2008). Given that most of the behavioural information presented in this section pertains to other fruit flies, there is a need to study the mating process for B. cucumis so that more effective management strategies can be designed.
5.1. Juvenile stages Hooper (1975a) initially used a pumpkin-based medium (no details provided) to rear larvae but subsequently used pumpkin slices. Slices of cucumber have been used for oviposition (Atuahene and Hooper, 1971; Smith et al., 1988) and rearing larvae (Smith et al., 1988). Ero et al. (2010) reared B. cucumis larvae on pumpkin medium. Swaine et al. (1978) and Quimio and Walter (2001) reported that eggs of B.cucumis were placed into a diet composed of blended cooked pumpkin (100 g), Torula yeast (4 g), concentrated HCl (0.6 ml) and Nipagin. A dome of diet was placed over fine sawdust as a pupation substrate (Quimio and Walter, 2001). Swaine et al. (1978) noted that poor pupation was clearly correlated with low oxygen concentration in the fruit cavity. Bactrocera tryoni pupae in comparison have a high tolerance for long periods of low oxygen (Dominiak et al., 2011). Fitt (1986) experimented with diets in laboratory experiments and found larval development times for B. cucumis varied from 5 days in cucumber to 11 days in bananas, with pumpkin, nectarine, apricot and tomato in between. Pupal weights varied from 9.8 mg in bananas to 17.8 mg in tomatoes. In comparison, pupal weights for B. tryoni male and females are about 10 mg (Fanson et al., 2014). The percentage pupal emergence for B. cucumis varied from 53% in bananas to 96% in tomato and nectarine (Fitt, 1986). 5.2. Adults Hooper (1975a) raised adults on a maintenance diet of yeast hydrolysate, sucrose and water. Colonies were held at 25 ± 1 °C and 65 ± 5% relative humidity (described by Atuahene and Hooper, 1971). The room was artificially illuminated from 0600 to 1700 h with an average light intensity of 8 ft candles (circa 86 lux) and from 1700 to 1800 h with an average light intensity of 0.06 ft candles (circa 0.6 lux) to simulate twilight. Atuahene and Hooper (1971) provided adults with water, sucrose and enzymatic yeast hydrolysate. Fitt (1986) supplied adult B. cucumis a diet of sucrose and enzymatic hydrolysate (4:1 ratio) and water. 6. Control 6.1. Pesticide control Good farm hygiene is important, particularly the destruction of finished crops after last harvest (May, 1946, Anon, 2014a). Reject fruit should not be left near packing sheds (Anon, 2014a). May (1962) reported generally on fruit fly control, stating that the introduction of parasites, release of sterile insects, male annihilation and chemical sprays were used to contain fruit flies. In Queensland, DDT was used as a cover spray, although B. cucumis had a greater capacity than B. tryoni to detoxify DDT to DDE (Atuahene and Hooper, 1971). In 1987, DDT was replaced by organophosphates dimethoate and fenthion (May, 1962, Dominiak and Ekman, 2013). However, following review by the Australian Pesticides and Veterinary Medicines Authority (APVMA) fenthion is no longer available for pre-harvest control of fruit flies in 2015 (APVMA, 2015) and the use of dimethoate has been restricted. Controlling B. cucumis in the vegetation on the edges of crops has been a successful strategy (Allwood 1997). Perimeter baiting of noncrop vegetation is commonly used for control of the closely related B. cucurbitae (Prokopy et al., 2003). Senior et al. (2017) found B. cucumis were more likely to be attracted to bait on sweet corn and forage sorghum compared to other non-crop alternatives. Flies preferred bait applied at 1–1.5 m above the ground, compared to B. tryoni that responded more to bait at about 2 m above the ground. There is no registered label for clothianidin however Permit number 80101 permits
4.6. Oviposition May (1946) noted that B. cucumis infested near mature or damaged cucurbit fruit. Some eggs were laid into immature fruits when flies were abundant but these did not hatch. Callused areas appeared in the rind around oviposition punctures and these sometimes caused fruit deformities. May (1953) noted that damaged or sunburnt fruit were readily attacked and May (1957) also reported that B. cucumis oviposited through scars in the rind of near-mature fruits. Drew (1997) claimed that the infestation levels in zucchinis increased with the size of the fruit. Export size fruit (10–13 cm long) were approximately 5% infested. 5. Rearing colonies Trial work examining various aspects of B. cucumis frequently requires colonies to be reared on laboratory diets. Senior et al. (2017) 37
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its use in the field (APVMA, 2016). Similarly alpha-cypermethrin (Permit 80138) and maldison (Permits 13675 and 13031) are permitted (APVMA, 2016). Dimethoate is permitted preharvest with a one day with-holding period (Permit 80540). Dimethoate use is permitted as a post-harvest treatment (Permit 13170). Bactrocera cucumis is not reported to be a pest in the Australian glasshouse cucurbit industry (Steiner and Goodwin, 2007).
effect of dose rate on sterility and competitiveness of newly emerged adult male B. cucumis. There was no significant effect of dose rate on sterility or longevity. When males were irradiated with 7 and 9 krad at rates of either 9.51 or 0.87 krad/min, there was no significant effect of dose rate on competitiveness of males. A dose of 9 krad produced significantly less competitive males than did a dose of 7 krad. Irradiation was performed with a Gammacell 220 containing approximately 6660 Ci of Co60. Hooper (1976) tested the protective effect of 15 min exposure to an atmosphere of pure nitrogen on irradiation of B. cucumis. The degree of sterility induced was less than that obtained with the same dose in normal air, but the males were significantly more competitive. The nitrogen treatment had no adverse effect on survival. Hooper (1976) suggested that the use of nitrogen would significantly enhance the success of irradiation in a field programme. Ovaries of sterile irradiated B. cucumis did not develop when they were either left intact or transplanted into normal flies but immature ovaries from normal flies developed yolky eggs when transplanted into irradiated flies (Bailey and Shipp, 1970). It appeared that, in B. cucumis puparia, vitellogenins were still produced by irradiated flies but their ovaries were incapable of using them, even when transplanted into normal flies. Meats and Leighton (2004) claimed that the reciprocal transplantation of ovaries of normal and irradiated B. cucumis by Bailey and Shipp (1970) showed that the gonadotrophic environment was normal in irradiated flies. Therefore, many processes pertinent to reproduction in females (including mating and the pattern of food intake) may not be dependent on the presence of an active ovary. Bailey (1973) reported that radiation dose between 0 and 80 krad did not affect oxygen consumption in irradiated female B. cucumis.
6.2. Biological control Fopius arisanus (Sonan) (Hymenoptera: Braconidae) was introduced from Hawaii and established on B. tryoni, but apparently with negligible effect on B. cucumis according to Quimio and Walter (2001). They reported that F. arisanus showed a stronger preference for larval B. tryoni and B. jarvisi than for B. cucumis. No parasitoids emerged from B. cucumis and this fruit fly may not be a suitable host because of its immune response. Ero et al. (2010) found that Diachasmimorpha kraussi (Fullaway) (Hymenoptera: Braconidae), an Australian native and considered a polyphagous fruit fly parasitoid, did not discriminate between physiologically suitable and unsuitable fruit fly hosts, readily ovipositing in B. cucumis larvae. However adult wasps did not emerge from B. cucumis and parasite eggs were found encapsulated in the fruit fly larvae. This parasitoid caused no obvious negative impact by the attempted parasitism and thus was not suitable for augmentative releases for potential biological control (Ero et al., 2010). 6.3. Irradiation and the sterile insect technique Sterility of B. cucumis has been achieved by chemosterilization and by irradiation. For chemosterilization, Vuttanatungum and Hooper (1974) found that male B. cucumis flies fed on metepa (1-[Bis(2-methyl1-aziridinyl)phosphoryl]-2-methylaziridine) for seven days at a concentration of 1.5% resulted in complete sterility while concentrations as low as 0.5% resulted in sterility greater than 97%. Similarly, a diet of hempa (Hydroxyethylamino-di(methylene phosphonic acid)) at a concentration of 1.0% resulted in complete sterility. Concentrations of 2.5% gave unacceptably high mortality. The chemosterilants affected females in two ways; by reducing fecundity and by lowering egg hatch. Infecundity occurred before total non-hatch of eggs was obtained. A concentration of 2.5% metepa was required for total sterility and this caused 31% mortality. Conversely 2% hempa gave complete sterility with no significant increase in mortality. When applied topically, higher doses of hempa than metepa were required to produce sterility in males but the reverse was true for females. Mortality with both chemosterilants became a problem before a high level of sterility was achieved. Hempa produced sterility at lower concentrations than did metepa when applied in the diet. When applied to tarsae, complete sterility of males was obtained with both chemosterilants with metepa being more effective than hempa. Vuttanatungum and Hooper (1974) found that both sexes could be effectively sterilised when fed on the chemosterilants, suggesting that they could be applied in a protein bait for field control. Chemosterilants could be important for control of this pest however more research is required before this technique becomes common practice. Hooper (1975a) examined the effect of gamma radiation on sterility of newly emerged B. cucumis males. This author noted that the reductions in egg hatch produced by 9 and 11 krad treated males were not significantly different, but at both doses the egg hatch was significantly less than that of 5–7 krad treated males. Gamma doses of approximately 7–9 krad produced sterility levels of 97–99 per cent respectively in male B. cucumis. There was no significant effect of any treatment on the survival of males and females with about 20 per cent mortality after six weeks. Sterilizing doses of irradiation reduced competitiveness. As irradiation dose increased from 5 to 11 krad, the competitiveness of male B. cucumis decreased from 0.62 to 0.22. Hooper (1975b) evaluated the
6.4. Post harvest treatments A range of disinfestation treatments have developed over time. Swaine et al. (1978) reported that fumigation with ethylene dibromide (EDB) at 12 g m−3 over 2 h provided control of eggs and larvae exceeding 97.76%. EDB fumigation was effective to treat export zucchini (Jacobi et al., 1996) until EDB was banned in New Zealand in January 1994 (Jessup et al., 1994). Heather et al. (1992) demonstrated that dimethoate and fenthion were effective against B. cucumis in zucchinis and rockmelons. More than 30,000 eggs and larvae of B. cucumis were killed by dips of each of dimethoate and fenthion in each commodity with residue below the Australian maximum residue limit of 2 mg/kg on the day of treatment with no adverse effects on taste (Heather et al., 1992). The dimethoate and fenthion dips were used to export zucchini and rockmelon from Australia to New Zealand following the loss of EDB in 1994. Zucchini was removed from this protocol when some uses of dimethoate were suspended because of dietary concerns (APVMA, 2015) however rockmelon and honeydew melon still have approval to be exported from Australia to New Zealand using this pathway (Anon, 2014b). As worldwide concerns were raised about possible links between pesticide use and human health (Dominiak and Ekman, 2013), nonpesticide treatments were investigated. Chilling treatments were tested. Chilling caused injury to zucchini in the form of circular to longitudinal pits on the surface (Mencarelli et al., 1983). Some hot water treatments caused extensive damage to fruit: hot air treatments were found to be less punitive on fruit quality (Jacobi et al., 1996). Corcoran et al. (1993) found that a vapour heat treatment at 45 °C for 30 min was an adequate disinfestation treatment against B. cucumis in zucchini marrows. This treatment involved heating fruit to a core temperature of 45 °C with > 94% relative humidity for 30 min (Corcoran et al., 1993). Jacobi et al. (1996) examined the treatment developed by Corcoran et al. (1993) for its suitability as an export treatment from the fruit quality perspective. Corcoran concluded that fruit quality could be maintained for up to 11 days if fruit are handled correctly before the disinfestation treatment, particularly avoiding pre-cooling. 38
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Corpus allatum size and ovarian environment in irradiated cucumber fly, Dacus cucumis. J. Insect Physiol. 16, 1293–1299. Bailey, P., 1973. Respiration and nutrition of radiation-sterilized female Dacus cucumis (Diptera: Tephritidae). Entomol. Exp. Appl. 16, 433–444. Balagawi, S., Jackson, K., Clarke, A.R., 2014. Resting sites, edge effects and dispersion of a polyphagous Bactrocera fruit fly within crops of different architecture. J. Appl. Entomol. 138, 510–518. Bateman, M.A., 1967. Adaptations to temperature in geographic races of the Queensland fruit fly, Dacus (Strumeta) tryoni. Aust. J. Zool. 15, 1141–1161. Booth, Y.K., Schwartz, B.D., Fletcher, M.T., Lambert, L.K., Kitching, W., De Voss, J.J., 2006. A diverse suite of spiroacetals, including a novel branched representative, is release by female Bactrocera tryoni (Queensland fruit fly). Chem. Commun. 3975–3977. Chang, L.Y., Ying, L.M., 2000. Morphology, development, longevity and mating behaviour of Bactrocera tau (Diptera: Tephritidae). Chin. J. Entomol. 20, 311–325. Chinajariyawong, A., Drew, R.A.I., Meats, A., Balagaswi, S., Vijaysegaran, S., 2010. Multiple mating by females of two Bactrocera species (Diptera: Tephritidae: Dacinae). Bull. Entomol. Res. 100, 325–330. Corcoran, R.J., Heather, N.W., Heard, T.A., 1993. Vapor heat treatment for zucchini infested with Bactrocera cucumis (Diptera: Tephritidae). J. Econ. Entomol. 86, 66–69. Dhillon, M.K., Singh, R., Naresh, J.S., Sharma, H.C., 2005. The melon fruit fly, Bactrocera cucurbitae: a review of its biology and management. J. Insect Sci. 5, 40. Dominiak, B.C., Sundaralingam, S., Jiang, L., Nicol, H., 2011. Effects of conditions in sealed plastic bags on eclosion of mass-reared Queensland fruit fly. Bactrocera Tryoni. Entomol. Exp. Appl. 141, 123–128. Dominiak, B.C., Daniels, D., 2012. Review of the past and present distribution of Mediterran fruit fly (Ceratitis capitata Wiedemann) and Queensland fruit fly (Bactrocera tryoni Froggatt) in Australia. Aust. J. Entomol. 51, 104–115. Dominiak, B.C., Ekman, J.H., 2013. The rise and demise of control options for fruit fly in Australia. Crop Prot. 51, 57–67. Dominiak, B.C., Sundaralingam, S., Jiang, L., Nicol, H.I., 2014. Longevity of mass-produced Bactrocera tryoni (Diptera: Tephritidae) held without food or water. J. Econ. Entomol. 107, 2103–2106. Dominiak, B.C., Wiseman, B., Anderson, C., Walsh, B., McMahon, M., Duthie, R., 2015. Definition of and management for areas of low pest prevalence for Queensland fruit fly Bactrocera tryoni Froggatt. Crop Prot. 72, 41–46. Dominiak BC & Worsley P. (in this issue). Review of cucumber fruit fly, Bactrocera cucumis (French) (Diptera: Tephritidae: Dacinae): Part 1, host range, surveillance and distribution. Crop Prot. Drew, R.A.I., 1972. The generic and subgeneric classification of Dacini (Diptera: Tephritidae) from the south Pacific area. J. Aust. Entomol. Soc. 11, 1–22. Drew, R.A.I., 1989. The tropical fruit flies (Diptera: Tephritidae: Dacinae) of the Australasian and Oceanian regions. Mem. Qld. Mus. 26, 1–521. Drew, R.A.I., 1997. Whole systems approach for export of zucchini from Queensland to New Zealand. In: Allwood, A.J., Drew, R.A.I. (Eds.), Management of Fruit Flies in the Pacific. Regional Symposium, Nadi, Fiji 28-31 October 1996, pp. 232–233. Ero, M.M., Hamacek, E.L., Peek, T., Clarke, A.R., 2010. Preference among four Bactrocera species (Diptera: Tephritidae) by Diachasmimorpha kraussi (Fullaway) (Hymenoptera: Braconidae). Aust. J. Entomol. 49, 324–331. Exley, E.M., 1955. Comparative morphological studies of the larvae of some Queensland Dacinae (Trypetidae, Diptera). Qld. J. Agric. Sci. 12, 119–150. Fanson, B.G., Sundaralingam, S., Jiang, L., Dominiak, B.C., D'Arcy, G., 2014. A review of 16 years of quality control parameters at a mass-rearing facility producing Queensland fruit fly, Bactrocera tryoni. Entomol. Exp. Appl. 151, 152–159. FAO Food & Agricultural Oranization, 2003. Guidelines for the Use of Irradiation as a Phytosanitary Measure. ISPM#18. Food and Agricultural Organization, Rome, Italy. Fitt, G.P., 1986. The roles of adult and larval specialisations in limiting the occurrence of five species of Dacus (Diptera: Tephritidae) in cultivated fruits. Oecologia Berl. 69, 101–109. Fitt, G.P., 1990. Variation in ovariole number and egg size of species of Dacus (Diptera: Tephritidae) and their relation to host specialization. Ecol. Entomol. 15, 255–264. Fletcher, B.S., 1989. Chapter 8.1 Life history strategies of Tephritid fruit flies. In: In: Robinson, A.S., Hooper, G. (Eds.), World Crop Pests. Fruit Flies, Their Biology, Natural Enemies and Control Vol 3B. Elsevier, pp. 195–208. Fletcher, M.T., Kitching, W., 1995. Chemistry of fruit flies. Chem. Rev. 95, 789–828. Fletcher, M.T., Wood, B.J., Brereton, I.M., Stok, J.E., de Voss, J.J., Kitching, W., 2002. [180]-Oxygen reveals novel pathways in spiroacetal biosynthesis by Bactrocera cacuminata and B. cucumis. J. Am. Chem. Soc. 124 (26), 7666–7667. French, C., 1907. Fruit flies. J. Agric. Vic. 5, 301–312. Froggatt, W.W., 1910. Notes on fruit-flies (Trypetidae) with description of new species. Proc. Lin. Soc. N. S. W. 15, 862–872. Gillespie, P., 2003. Observations on fruit flies (Diptera: Tephritidae) in new south Wales.
Hall et al. (2007) demonstrated that heat disinfestation treatments resulted in high mortality of B. cucumis in zucchini and rockmelon and should meet the quarantine requirements for both international and interstate trade within Australia. In zucchinis, button squash, rockmelon, honeydew and watermelons, the eggs were the most tolerant life stage, followed by third instar larvae. In cucurbit vegetables, confirmatory trials conducted in zucchini showed that a treatment of 45 °C for 40 min resulted in no survivors from a total of 109,480 B. cucumis mature eggs. Confirmatory trials conducted in rockmelon showed that a treatment of 44 °C with no holding period resulted in no survivors from a total of 234,429 B. cucumis mature eggs. Currently, heat protocols have not been negotiated for market access. Host fruit of B. cucumis was exported from Australia to New Zealand using the winter window pathway, which relied on field control mechanisms, from 1 May–September 30 in any year (Anon, 2014b; Hall et al., 2007). The term ‘winter window’ refers to quarantine agreements which allow commodities to be imported, at times when fruit fly infestation is very low, into areas that have a winter climate that is not conducive to fruit fly establishment (Allwood 1997). The use of ionizing irradiation is also approved as a phytosanitary treatment against fruit flies including B. cucumis (FAO, 2003). For domestic trade, the Interstate Certification Assurance (ICA) No. 55 recognises a minimum dose of 150 Gy as a disinfestation treatment (QDAF, 2016). 7. Overview Bactrocera cucumis fills an unusual position in the Australian fruit fly landscape. It is an Australian native but has not transitioned to a larger host range as B. tryoni did, despite exposure to many new hosts for at least a century. It has stayed confirmed to the Northern Territory and Queensland; similarly B. frauenfeldi (Schiner) (Royer et al., 2016) did not spread into southern environments as did B. tryoni. It is one of the largest flies and the longest lived, compared with most other Australian fruit flies. Bactrocera cucumis spends much of its life cycle in non-crop vegetation and enters crop for egg laying while other species spend much of their time in crop vegetation for food, shelter and egg laying. The mating ritual is different to most other species as B. cucumis has no stridulation combs. Some aspects such as chemosterilization is much studied in B. cucumis but virtually not at all in other Australian fruit flies. Bactrocera cucumis many characteristics similar to B. tau and B. curcurbitae but has evolved in different locations. Bactrocera cucumis occupies an unusual and contradictory place in the Australian fruit fly landscape. This review of B. cucumis places the current level of knowledge of biology, ecology and management in one publication. Research into mating rituals, lures, distribution, seasonality, biological control, pre and post-harvest control and host range of cucumber fruit fly is ongoing. This information will be important in understanding B. cucumis and the development of new International Standards for Phytosanitary Measures to facilitate trade. All future management strategies are likely to use a systems approach, particularly following decline of the dimethoate and fenthion as end-point treatments. Acknowledgements Many scientists contributed to this manuscript and their support is acknowledged. Bruce Browne and Alison Seyb reviewed and improved earlier versions of this manuscript. Bruce Browne provided information from the APVMA website. Darryl Barbour and Craig Hull also provided early guidance. Dr Mark Krosch reviewed the Phylogenetic section. Two anonymous referees provided comments and improved the manuscript. References Allwood, A.J., 1997. Biology and ecology: prerequisites for understanding and managing fruit fly (Diptera: Tephritidae). In: Allwood, A.J., RAI Drew (Eds.), Management of
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genes. Res. B. Plant Prot. Jpn. 44, 1–12. Nishida, T., Bess, H.A., 1957. Studies on the ecology and control of the melon fly Dacus (Strumeta) cucurbitae Coquillett (Diptera: Tephritidae). Tech. B., Hawaii Agric. Exp. Stat.(34) 44 pp. Perkins, F.A., 1937. Studies in Australian and oriental Trypaneidae Part 1. – New Genera Dacinae. Proc. R. Soc. Qld. 48, 51–60. Perkins, M.V., Jacobs, M.F., Kitching, W., Cassidy, P.J., Lewis, J.A., Drew, R.A.I., 1992. Diastereo- and Enantioselective Routesto some 2,8-Dimethyl-7,7-dioxaspiro[5.5]undecanols. Absolute stereochemistry of (E, E,E)-2,8-Dimethyl-1,7-dioxaspiro[5.5]undecan-3-ol and of ((E,E)-8-Methyl-1,7-dioxaspiro[5.5]undecan-2-yl)methanol present in Bactrocera cucumis. J. Org. Chem. 57, 3365–3380. Prokopy, R.J., Bennett, E.W., Bush, G.L., 1971. Mating behaviour in Rhagoletis pomonella (Diptera: Tephritidae) I. site of assembly. Can. Entomol. 103, 1405–1409. Prokopy, R.J., Bennett, E.W., Bush, G.L., 1972. Mating behaviour in Rhagoletis pomonella (Diptera: Tephritidae) II temporal organisation. Can. Entomol. 104, 97–104. Prokopy, R.J., Bush, G.L., 1973. Mating behaviour of Rhagoletis pomonella (Diptera: Tephritidae): IV courtship. Can. Entomol. 105, 873–891. Prokopy, R., Miller, N.W., Piñero, J.C., Barry, J.D., Tran, L.C., Oride, L., Vargas, R.I., 2003. Effectiveness of GF-120 fruit fly bait spray applied to border area plants for control of melon flies (Diptera: Tephritidae). J. Econ. Entomol. 96, 1485–1493. QDAF, 2016. Queensland Department of Agriculture and Fisheries. https://www.daf.qld. gov.au/__data/assets/pdf_file/0008/69578/ICA-55.pdf. Quimio, G.M., Walter, G.H., 2001. Host preference and host suitability in an egg-pupal fruit fly parasitoid, Fopius arisanus (Sonan) (Hym. Braconidae). J. Appl. Entomol. 125, 135–140. Royer, J.E., Wright, C.L., Hancock, D.L., 2016. Bactrocera fraunfeldi (Tephritidae: Dacinae), an invasive fruit fly in Australia that may have reached the extent of its spread due to environmental variable. Austral Entomol. 55, 100–111. Senior, L.R., Wright, C.L., Missenden, B., DeFaveri, S., 2017. Protein feeding of Queensland fruit fly Bactrocera tryoni and cucumber fly Zeagodacus cucumis (Diptera: Tephritidae) on non-host vegetation: effect of plant species and bait height. Austral Entomol. 56, 296–301. Singh, S.K., Kumar, D., Ramamurthy, V.V., 2010. Biology of Bactrocera (Zeugodacus) tau (Walker) (Diptera: Tephritidae). Entomol. Res. 40, 259–263. Smith, E.S.C., Chin, D., Allwood, A., Collins, S.C., 1988. A revised host list of fruit flies (Diptera: Tephritidae) from the Northern Territory of Australia. Qld. J. Agric. Anim. Sci. 45, 19–28. Steiner, M.Y., Goodwin, S., 2007. Challenges for the implementation of integrated pest management of cucumber pests in protected crops – an Australian perspective. Acta Hortic. 731, 309–315. Suzuki, Y., Koyama, J., 1980. Temporal aspects of mating behaviour of the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae): a comparison between laboratory and wild strains. Appl. Entomol. Zool. 15, 215–224. Swaine, G., Corcoran, R.J., Davey, M., 1978. Commodity treatment against infestations of the cucumber fly, Dacus (Austrodacus) cucumis French, in cucumbers. Qld. J. Agric. Anim. Sci. 35, 5–9. Tryon, H., 1926. Queensland fruit flies (Trypetidae), Series 1. Proc. R. Soc. Qld. 38, 176–223. Tychen, P.H., 1977. Mating behaviour of the Queensland fruit fly, Dacus tryoni (Diptera: Tephritidae), in field cages. J. Aust. Entomol. Soc. 16, 459–465. Vargas, R.I., Miyashita, O., Nishida, T., 1984. Life history and demographic parameters of three laboratory-reared tephritids (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 77, 651–656. Vargas, R.I., Walsh, W.A., Kanehisa, D., Stark, J.D., Nishiyuki, T., 2000. Comparative demography of three Hawaiian fruit flies (Diptera: Tephritidae) at alternating temperatures. Ann. Entomol. Soc. Am. 93, 75–81. Virgilio, M., Jordaens, K., Verwimp, C., White, I.M., De Meyer, M., 2015. Higher phylogeny of frugivorous flies (Diptera, Tephritidae, Dacini): localised partition conflicts and a novel generic classification. Mol. Phylogenet. Evol. 85, 171–179. Vuttanatungum, A., Hooper, G.H.S., 1974. Biology and chemical sterilization of the fruit fly Dacus cucumis French (Diptera: Tephritidae). J. Aust. Entomol. Soc. 13, 169–178.
Gen. Appl. Entomol. 32, 41–47. Hall, E.A., Leach, P.L., Kopittke, R.A., 2007. Non-chemical postharvest disinfestation treatments for cucurbits against Bactrocera cucumis (French) (Diptera: Tephritidae). Acta Hortic. 731, 59–65. Hardy, D.E., 1951. The Krauss collection of Australian fruit flies (Tephritidae-Diptera). Pac. Sci. 5, 115–189. Heather, N.W., Walpole, D.E., Corcoran, R.J., Hargreaves, P.A., Jordan, R.A., 1992. Postharvest quarantine disinfestation of zucchinis and rockmelons against Bactrocera cucumis (French) using insecticide dips of fenthion or dimethoate. Aust. J. Exp.Agric 32, 241–244. Hooper, G.H.S., 1975a. Sterilization of Dacus cucumis French (Diptera: Tephritidae) by gamma radiation. I effect of dose on fertility, survival and competitiveness. J. Aust. Entomol. Soc. 14, 81–87. Hooper, G.H.S., 1975b. Sterilization of Dacus cucumis French (Diptera: Tephritidae) by gamma radiation. II Effect of dose rate on sterility and competitiveness of adult males. J. Aust. Entomol. Soc. 14, 175–177. Hooper, G.H.S., 1976. Sterilization of Dacus cucumis French (Diptera: Tephritidae) by gamma radiation. III Effect of irradiation in nitrogen on sterility, competitiveness and mating propensity. J. Aust. Entomol. Soc. 15, 13–18. Iwashashi, O., Majima, T., 1986. Lek formation and male-male competition in the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Appl. Entomol. Zool. 21, 70–75. Jacobi, K.K., Wong, L.S., Giles, J.E., 1996. Postharvest quality of zucchini (Cucurbita pepo L.) following high humidity hot air disinfestation treatments and cool storage. Postharvest Biol. Tec. 7, 309–316. Jessup, A.J., Sloggett, R.F., Quinn, N.M., 1994. Residues of methyl bromide and inorganic bromide in fumigated produce. J. Agric. Food Chem. 42, 108–111. Kabir, S.M.H., Rahman, R., Molla, M.A.S., 1997. Biology of Dacus (Zeugodacus) tau Walker (Tephritidae: Diptera). Bangladesh J. Zool. 25, 115–120. Kitching, W., Lewis, J.A., Perkins, M.V., Drew, R., Moore, C.J., Schurig, V., Konig, W.A., Francke, W., 1989. Chemistry of fruit flies. Composition of the rectal gland secretion of (male) D.cucumis (Cucumber fly) and Dacus halfordiae. Characterisation of (Z,Z)2,8-Dimethyl-1,7-dioxaspiro[5.5]undecane. J. Org. Chem. 54, 3893–3902. Kuba, H., Soemori, H., 1988. Characteristics of copulation duration, hatchability of eggs and remating intervals in the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Appl. Entomol. Zool. 32, 321–324. Krosch, M.N., Schutze, M.K., Armstrong, K.F., Graham, G.C., Yeates, D.K., Clarke, A.R., 2012. A molecular phylogeny for the Tribe Dacini (Diptera: Tephritidae): systematic and biogeographic implications. Mol. Phylogenet. Evol. 64, 513–523. McErlean, C.S.P., Fletcher, M.T., Wood, B.J., De Voss, J.J., Kitching, W., 2002. Monooxygenase stereoselectivity in the biosynthesis of stereoisomeric spiroacetals in the cucumber fly, Bactrocera cucumis. Org. Lett. 4 (16), 2775–2778. Mankin, R.W., Lemon, M., Harmer, A.M.T., Evans, C.S., Taylor, P.W., 2008. Time-pattern and frequency analyses of sounds produced by irradiated and untreated male Bactrocera tryoni (Diptera: Tephritidae) during mating behaviour. Ann. Entomol. Soc. Am. 101, 664–674. May, A.W.S., 1946. Pests of cucurbit crops. Qld. Agric. J. 62, 137–150. May, A.W.S., 1953. Queensland host records for the Dacinae (Fam. Trypetidae). Qld. J. Agric. Sci. 10, 36–79. May, A.W.S., 1957. Queensland host records for the Dacinae (Fam. Trypetidae). First Suppl. lists Qld. J. Agric. Sci. 14, 29–39. May, A.W.S., 1962. The fruit fly problem in eastern Australia. J. Aust. Entomol. Soc. 1, 1–4. Meats, A., Leighton, S.M., 2004. Protein consumption by mated, unmated, sterile and fertile adults of the Queensland fruit fly, Bactrocera tryoni and its relation to egg production. Physiol. Entomol. 29, 176–182. Mencarelli, F., Lipton, W.J., Peterson, S.J., 1983. Responses of “Zucchini” squash to storage in low-O2 atmospheres at chilling and nonchilling temperatures. J. Am. Soc. Hort. Sci. 108, 884–890. Nakahara, S., Muraji, M., 2008. Phyogenetic analyses of Bactrocera fruit flies (Diptera: Tephritidae) based on nucleotide sequenceas of the mitochondrial COI and COII
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Review of cucumber fruit fly, Bactrocera cucumis (French) (Diptera: Tephritidae: Dacinae): Part 2, biology, ecology and control in Australia
MARK
Bernard C. Dominiak New South Wales Department of Primary Industries, 161 Kite Street, Orange, New South Wales 2800, Australia
A R T I C L E I N F O
A B S T R A C T
Keywords: Cucurbit Reproduction Rearing Disinfestation
Bactrocera cucumis is one of many fruit fly species of concern for Australia's international trade partners. This species is one of the lesser known native fruit flies in Australia and its distribution and hosts have been reviewed. Eggs are larger than in most other species with a short hatching period. The adults and larvae are also larger than most other Australian fruit flies. Adults are long lived and have a high rate of reproduction. Stridulation and pheromones appear not to be used in the mating process. Adults can be managed using a range of measures including chemosterilants, the sterile insect technique and chemical sprays. Produce can be disinfested using a range of post-harvest treatments. Current export protocols include hot air and chilling treatments, irradiation, methyl bromide fumigation and winter window.
1. Introduction In Asia and the Pacific regions, Dacine fruit flies (Diptera: Tephritidae: Dacinae) are key pests, adversely impacting food production and international trade. Larval stages feed on a broad range of fruit and vegetables causing direct damage, fruit drop and loss of export markets (Dominiak et al., 2015). In the last century, fruit fly research in Australia has concentrated on the major economic species such as Queensland fruit fly Bactrocera tryoni (Froggatt) (Qfly) and Mediterranean fruit fly Ceratitis capitata (Weidemann) (Medfly) (Dominiak and Daniels, 2012). As knowledge on these species improves, other fruit fly species are now being increasingly studied. Cucumber fruit fly Bactrocera cucumis (French) is the main pest of cucurbits in Australia and is a species that has been less well studied (Anon, 2014a). The hosts, lures and distribution of this species were reviewed by Dominiak and Worsley (Submitted). In this manuscript review, the published reports covering biology, ecology and controls of B. cucumis are reviewed, and research gaps identified.
(Austrodacus) cucumis and B. (Papuodacus) neopallescentis were nested in the B. (Zeugodacus) clade that seems to have diverged from the Dacus clade in the early Paleogene period. Zeugodacus and Bactrocera groups appear to have experienced increased speciation rates in the last 25–50 million years. Zeugodacus is an almost entirely monophyletic sister group to Dacus. Krosch et al. (2012) noted that it is important for applied workers to recognise that significant pest taxa of the Zeudodacus group, such as Zeugodacus cucurbitae (Coquillet), B. cucumis and B. tau (Walker), are more closely related to African Dacus species than they are to Asian pest species such as B. dorsalis (Hendel). Using mitochondrial analysis, Nakahara and Muraji (2008) also found that B. cucumis, B. tau and B. cucurbitae all had a common origin. Bactrocera cucurbitae and B. tau are attracted to cuelure; B. dorsalis is attracted to methyl eugenol and B. cucumis is not attracted to cuelure or methyl eugenol. Virgilio et al. (2015) have inferred higher phylogeny of frugivorous fruit flies (Diptera, Tephritidae, Dacini) from mitochondrial and nuclear gene fragments.
2. Phylogenetic placement
3. Taxonomy
Krosch et al. (2012) undertook a detailed genetic analysis of the tribe Dacini. While the analysis may have been directed at more economically important fruit flies, the evolution of B. cucumis was also identified. Bactrocera cucumis falls under the Zeugodacus group. All but two members of the Zeugodacus group of subgenera (including B. (Zeugodacus)) formed a clade that was more closely related to Dacus than Bactrocera. The species B. (Sinodacus) abdopallescens, B.
French (1907) originally described some morphology of Dacus cucumis and indicated it was a variant of Dacus tryoni var. cucumis. Froggatt (1910) described more adult morphology and supported the formation of a new species due to the differences to Dacus tryoni. Tryon (1926) provided a detailed key of all life stages and identified D. cucumis as a new species but noted that this insect was an exceptional species of Dacus due to the presence of four scutellar bristles,
E-mail address: [email protected]. http://dx.doi.org/10.1016/j.cropro.2017.10.005 Received 21 April 2017; Received in revised form 26 September 2017; Accepted 4 October 2017 0261-2194/ © 2017 Elsevier Ltd. All rights reserved.
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Queensland and females enter the fields to lay eggs (Allwood 1997; Balagawi et al., 2014). Numerous samples of adult B. cucumis were collected from the leaves of Ficus racemosa L. to start a laboratory culture in Northern Territory because B. cucumis was not known to infest commercial fruit (Smith et al., 1988). Senior et al. (2017) reported that bait sprays were best placed on vegetation surrounding crops as these roosting sites were preferred by B. cucumis. Bactrocera tryoni also rest in non-crop areas near host crops (Balagawi et al., 2014) and these plants, such as Ficus, may offer features such as resting sites, protection from predators, food not found elsewhere or other attributes to support life.
uncommon in other fruit flies at that time. Perkins (1937) also claimed it was necessary to create a new genus for cucumis as it was so different from the other Dacinae. Perkins placed the species in Dacus in the new Austrodacus genus. It was very easily distinguished from other genera with four bristles by the absence of both a.sa and pr.sc bristles (Perkins, 1937). The species was described in detail by Hardy (1951) and Hardy claimed that Dacus (Zeugodacus) was a group close to Dacus (Strumeta) differing only by possessing four scutellar bristles rather than two. Drew (1972) reviewed many species and noted that morphologically the supernumerary lobe is present in the male wing and was very strong in most species of Zeugodacus. In B. cucumis, the posterior lobe of the surstylus was extremely long and more so than in other species of Dacus group of the subgenera. Bactrocera cucurbitae possesses a long posterior lobe on surstylus and abdominal sternite (Drew, 1972). Drew (1989) placed B. cucumis in the Zeugodacus subgenera under the subgenus Austrodacus.
4.3. Chemical spiroketals Male tephritids store pheromones in a reservoir and secrete it from a sac: both organs are located in the lower rectal area. The release of pheromone is generally associated with courting behaviour, but females may respond to other stimuli (Fletcher and Kitching, 1995). Some species such as B. tryoni use stridulation combs to disperse these pheromones, however B. cucumis do not have these combs (Tychen, 1977). Kitching et al. (1989) found 14 compounds in rectal glands of male B. cucumis. Fletcher and Kitching (1995) reported that extracts of male B. cucumis rectal glands showed the presence of one major component (about 60%) ((E,E)- (E,E)-2,8-dimethyl-1, 7-dioxapiro [5.5]undecane) and several minor components. Kitching et al. (1989) also reported on the E,Z, and Z,Z diastereomers of (E,E)-2,8-dimethyl-1, 7dioxapiro [5.5]undecane making up 5% and 8% respectively. Perkins et al. (1992) reported minor amounts of Z, E isomers. The other two main components were 3-hydroxy-2, 8-dimethyl-1,7-dioxaspiro[5.5] (15%) and (R)-(-)-1,3-nonanediol (10%) (Kitching et al., 1989). Some of these minor compounds were also detected in male rectal glands of B. tryoni and B. cacuminatus (Hering) (Perkins et al., 1992). Sexually excited B. tryoni males excrete an oily blend of six amides, which function as a short range attractant and invoke responses in mature females (Fletcher and Kitching, 1995). Analysis of the volatile emissions from B. tryoni females revealed that major components were N-(3-methylbutyl)propanamide and the spiroacetal (E,E)-2,8-dimethyl1, 7-dioxapiro [5.5]undecane which is present in a wide variety of insects including B. cucumis (Booth et al., 2006). Fletcher et al. (2002) reported the spiroacetals 3 and 4 from B. cucumis incorporate one ring oxygen from water and one ring oxygen (and the hydroxyl oxygen in 4) from [1802]-dioxygen. This discovery revealed the generality of monoxygenase mediation of spiroacetal formation in Bactrocera sp. and also the unexpected complexity in their biosynthesis. McErlean et al. (2002) studied this complexity further.
4. Biology and host damage 4.1. Egg, larval and pupal stages Comparing eight fruit fly species of Dacus, Fitt (1990) found that B. cucumis produced the largest eggs (1.34 mm), with the shortest incubation time at 25 °C (approximately 24 h). A similar finding was reported for two other cucurbit specialists: B. cucurbitae produced large eggs which hatched in less than two days (Vargas et al., 1984; Dhillon et al., 2005) and in B. tau eggs hatched in about 1.3 days (Singh et al., 2010). Overall development time of B. cucumis, B. cucurbitae and B. tau is also short relative to other species. Development from egg to adult at 25 °C and 65% relative humidity was recorded as 16.9 and 17.0 days respectively for male and female B. cucumis (Vuttanatungum and Hooper, 1974), as little as 13 days in B. cucurbitae at 29 °C (Dhillon et al., 2005) and 14 days at 25 °C and 65% relative humidity in B. tau (Singh et al., 2010). In comparison, development of B. tryoni from egg to adult was recorded as 20–34.5 days (at 30 °C and 20 °C respectively) by Bateman (1967). Fletcher (1989) suggested that the fast development time of B. cucumis offered a greater chance of survival and may be connected to the internal environment of the host fruits. Vargas et al. (2000) also claimed two distinctly different life history patterns (1) early reproduction, short life span, and a high intrinsic rate of increase, and (2) later onset of reproduction, longer life span, and a lower intrinsic rate of increase such as B. cucurbitae. In a laboratory held at 25 °C and 65% relative humidity, Vuttanatungum and Hooper (1974) found that egg hatch of B. cucumis was 84 per cent. Mature larvae began to leave the larval media five days after hatching and continued to leave for another five days. Mean larval life was 6.5 days and survival averaged 81 per cent. The duration of the pupal period was 10–11 days. May (1946) and Anon (2014a) reported that larvae mature in 7–10 days in summer and emerge from fruit to pupate in the soil, similar to most fruit flies. The pupal stage is completed in about 10 days. The entire life cycle is completed in about 2.5 weeks in summer (May, 1946). Bactrocera cucumis larvae were described in detail by Exley (1955). They are a deeper colour than those of B. tryoni, with a habit of curling and jumping further than other fruit fly larvae (French, 1907). Over fifty larvae may infest one cucumber (French, 1907).
4.4. Life span Unlike most other fruit flies, the adults are long lived and can survive for up to six months in laboratory conditions (Vuttanatungum and Hooper, 1974; Anon, 2014a). Again in laboratory conditions, B. cucumis females lived up to 274 days (Chinajariyawong et al., 2010). By comparison, Fanson et al. (2014) found the LD50 of B. tryoni in ideal laboratory conditions was 72.5 days. However the mean longevity was 54 h without food or water in the laboratory (Dominiak et al., 2014) so finding adequate resources is important. The genetically close B. cucurbitae is also long lived, surviving up to 249 days in the laboratory (Dhillon et al., 2005). Similarly B. tau can live for more than six months in the laboratory (Chang and Ying, 2000). Kabir et al. (1997) reported two population peaks per year in spring and autumn. Another Australian native fly Dacus newmani (Perkins) also has a long life span with only two generations per year (Gillespie, 2003). The mean weights of male and female B. cucumis were 10.99 mg and 17.51 mg respectively, compared with 13.03 mg and 14.33 mg respectively for B. tryoni (Atuahene and Hooper, 1971).
4.2. Adult behaviour In contrast to B. tryoni, B. cucumis is reputed in one reference to be attracted to packing sheds and can infest produce on the packing line (Anon, 2014a). However there is no published research to support this claim. Papaya fruit ripening on trees or possibly in packing sheds may be attacked, but mature green to a quarter coloured fruit are likely to escape damage (Anon, 2014a). Several fruit fly species, including B. cucumis, inhabit vegetation around the edges of zucchini crops in 36
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reported sourcing adults from Brisbane laboratories but provided no details for the maintenance of fruit fly colonies.
4.5. Reproduction and mating Bactrocera cucumis is capable of a high rate of reproduction. According to Vuttanatungum and Hooper (1974) females produced up to 1300 eggs during the first 14 weeks of life but may live for up to eight months. Egg production declined after the sixth week. Both male and female B. cucumis became sexually mature after 15–18 days at 25 °C. Vuttanatungum and Hooper (1974) claimed males were capable of mating daily but more commonly mated about three times in a five day period. However, Chinajariyawong et al. (2010) found that, in laboratory conditions, 52% of B. cucumis pairs mated three times with a maximum of five times over a 274 day period. The refractory period was at least twice as long as B. tryoni. Mankin et al. (2008) reported that male B. tryoni use a combination of pheromone and stridulation to attract females into the mating site. However, Hooper (1975a) claimed that preliminary research failed to demonstrate any involvement of a male pheromone in the mating sequence of B. cucumis. This species also lacks stridulation combs, indicating that stridulation does not occur (Tychen, 1977). Male B. tryoni may form a flying swarm that gathers towards the top of trees (Tychen, 1977). The closely related B. cucurbitae also displays the lek mating behaviour with male aggregations gathering on non-host plants (Iwashashi and Majima, 1986). Hooper (1976) stated that B. cucumis mate at dusk. Bactrocera cucurbitae also mate at dusk and copulation continues until dawn (Suzuki and Koyama, 1980; Kuba and Soemori, 1988). Similarly B. tau mate at dusk with a duration of up to 12 h (Chang and Ying, 2000). Hooper (1975a) claimed that mating in B. cucumis was very similar to that of Rhagoletis pomonella (Walsh) (Prokopy and Bush, 1973), in which the act of copulation was closely associated with oviposition into fruit (Prokopy et al., 1971). In R. pomonella, arrival at fruit was triggered on the basis of visual cues. Once in close range (within 50 cm), the visual stimulus was important in eliciting the courtship approach of the male. Visual cues therefore play an important role in location of both fruit and potential mates (Prokopy et al., 1972). Compared to sexually active flies, immature flies have a low incidence on host fruit. Anon (2014a) also noted that adults are attracted to and feed on bacterial colonies on the surface of foliage. They mate at these feeding sites and later lay eggs into the fruit, particularly into ripe and damaged fruit (Anon, 2014a). Drew (1997) claimed that B. cucumis was trapped in surrounding vegetation but rarely in traps placed within a cucurbit crop. This behaviour of entering host areas primarily for oviposition is similar to that of B. cucurbitae (Nishida and Bess, 1957) a species genetically close to B. cucumis (Krosch et al., 2012; Nakahara and Muraji, 2008). Given that most of the behavioural information presented in this section pertains to other fruit flies, there is a need to study the mating process for B. cucumis so that more effective management strategies can be designed.
5.1. Juvenile stages Hooper (1975a) initially used a pumpkin-based medium (no details provided) to rear larvae but subsequently used pumpkin slices. Slices of cucumber have been used for oviposition (Atuahene and Hooper, 1971; Smith et al., 1988) and rearing larvae (Smith et al., 1988). Ero et al. (2010) reared B. cucumis larvae on pumpkin medium. Swaine et al. (1978) and Quimio and Walter (2001) reported that eggs of B.cucumis were placed into a diet composed of blended cooked pumpkin (100 g), Torula yeast (4 g), concentrated HCl (0.6 ml) and Nipagin. A dome of diet was placed over fine sawdust as a pupation substrate (Quimio and Walter, 2001). Swaine et al. (1978) noted that poor pupation was clearly correlated with low oxygen concentration in the fruit cavity. Bactrocera tryoni pupae in comparison have a high tolerance for long periods of low oxygen (Dominiak et al., 2011). Fitt (1986) experimented with diets in laboratory experiments and found larval development times for B. cucumis varied from 5 days in cucumber to 11 days in bananas, with pumpkin, nectarine, apricot and tomato in between. Pupal weights varied from 9.8 mg in bananas to 17.8 mg in tomatoes. In comparison, pupal weights for B. tryoni male and females are about 10 mg (Fanson et al., 2014). The percentage pupal emergence for B. cucumis varied from 53% in bananas to 96% in tomato and nectarine (Fitt, 1986). 5.2. Adults Hooper (1975a) raised adults on a maintenance diet of yeast hydrolysate, sucrose and water. Colonies were held at 25 ± 1 °C and 65 ± 5% relative humidity (described by Atuahene and Hooper, 1971). The room was artificially illuminated from 0600 to 1700 h with an average light intensity of 8 ft candles (circa 86 lux) and from 1700 to 1800 h with an average light intensity of 0.06 ft candles (circa 0.6 lux) to simulate twilight. Atuahene and Hooper (1971) provided adults with water, sucrose and enzymatic yeast hydrolysate. Fitt (1986) supplied adult B. cucumis a diet of sucrose and enzymatic hydrolysate (4:1 ratio) and water. 6. Control 6.1. Pesticide control Good farm hygiene is important, particularly the destruction of finished crops after last harvest (May, 1946, Anon, 2014a). Reject fruit should not be left near packing sheds (Anon, 2014a). May (1962) reported generally on fruit fly control, stating that the introduction of parasites, release of sterile insects, male annihilation and chemical sprays were used to contain fruit flies. In Queensland, DDT was used as a cover spray, although B. cucumis had a greater capacity than B. tryoni to detoxify DDT to DDE (Atuahene and Hooper, 1971). In 1987, DDT was replaced by organophosphates dimethoate and fenthion (May, 1962, Dominiak and Ekman, 2013). However, following review by the Australian Pesticides and Veterinary Medicines Authority (APVMA) fenthion is no longer available for pre-harvest control of fruit flies in 2015 (APVMA, 2015) and the use of dimethoate has been restricted. Controlling B. cucumis in the vegetation on the edges of crops has been a successful strategy (Allwood 1997). Perimeter baiting of noncrop vegetation is commonly used for control of the closely related B. cucurbitae (Prokopy et al., 2003). Senior et al. (2017) found B. cucumis were more likely to be attracted to bait on sweet corn and forage sorghum compared to other non-crop alternatives. Flies preferred bait applied at 1–1.5 m above the ground, compared to B. tryoni that responded more to bait at about 2 m above the ground. There is no registered label for clothianidin however Permit number 80101 permits
4.6. Oviposition May (1946) noted that B. cucumis infested near mature or damaged cucurbit fruit. Some eggs were laid into immature fruits when flies were abundant but these did not hatch. Callused areas appeared in the rind around oviposition punctures and these sometimes caused fruit deformities. May (1953) noted that damaged or sunburnt fruit were readily attacked and May (1957) also reported that B. cucumis oviposited through scars in the rind of near-mature fruits. Drew (1997) claimed that the infestation levels in zucchinis increased with the size of the fruit. Export size fruit (10–13 cm long) were approximately 5% infested. 5. Rearing colonies Trial work examining various aspects of B. cucumis frequently requires colonies to be reared on laboratory diets. Senior et al. (2017) 37
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its use in the field (APVMA, 2016). Similarly alpha-cypermethrin (Permit 80138) and maldison (Permits 13675 and 13031) are permitted (APVMA, 2016). Dimethoate is permitted preharvest with a one day with-holding period (Permit 80540). Dimethoate use is permitted as a post-harvest treatment (Permit 13170). Bactrocera cucumis is not reported to be a pest in the Australian glasshouse cucurbit industry (Steiner and Goodwin, 2007).
effect of dose rate on sterility and competitiveness of newly emerged adult male B. cucumis. There was no significant effect of dose rate on sterility or longevity. When males were irradiated with 7 and 9 krad at rates of either 9.51 or 0.87 krad/min, there was no significant effect of dose rate on competitiveness of males. A dose of 9 krad produced significantly less competitive males than did a dose of 7 krad. Irradiation was performed with a Gammacell 220 containing approximately 6660 Ci of Co60. Hooper (1976) tested the protective effect of 15 min exposure to an atmosphere of pure nitrogen on irradiation of B. cucumis. The degree of sterility induced was less than that obtained with the same dose in normal air, but the males were significantly more competitive. The nitrogen treatment had no adverse effect on survival. Hooper (1976) suggested that the use of nitrogen would significantly enhance the success of irradiation in a field programme. Ovaries of sterile irradiated B. cucumis did not develop when they were either left intact or transplanted into normal flies but immature ovaries from normal flies developed yolky eggs when transplanted into irradiated flies (Bailey and Shipp, 1970). It appeared that, in B. cucumis puparia, vitellogenins were still produced by irradiated flies but their ovaries were incapable of using them, even when transplanted into normal flies. Meats and Leighton (2004) claimed that the reciprocal transplantation of ovaries of normal and irradiated B. cucumis by Bailey and Shipp (1970) showed that the gonadotrophic environment was normal in irradiated flies. Therefore, many processes pertinent to reproduction in females (including mating and the pattern of food intake) may not be dependent on the presence of an active ovary. Bailey (1973) reported that radiation dose between 0 and 80 krad did not affect oxygen consumption in irradiated female B. cucumis.
6.2. Biological control Fopius arisanus (Sonan) (Hymenoptera: Braconidae) was introduced from Hawaii and established on B. tryoni, but apparently with negligible effect on B. cucumis according to Quimio and Walter (2001). They reported that F. arisanus showed a stronger preference for larval B. tryoni and B. jarvisi than for B. cucumis. No parasitoids emerged from B. cucumis and this fruit fly may not be a suitable host because of its immune response. Ero et al. (2010) found that Diachasmimorpha kraussi (Fullaway) (Hymenoptera: Braconidae), an Australian native and considered a polyphagous fruit fly parasitoid, did not discriminate between physiologically suitable and unsuitable fruit fly hosts, readily ovipositing in B. cucumis larvae. However adult wasps did not emerge from B. cucumis and parasite eggs were found encapsulated in the fruit fly larvae. This parasitoid caused no obvious negative impact by the attempted parasitism and thus was not suitable for augmentative releases for potential biological control (Ero et al., 2010). 6.3. Irradiation and the sterile insect technique Sterility of B. cucumis has been achieved by chemosterilization and by irradiation. For chemosterilization, Vuttanatungum and Hooper (1974) found that male B. cucumis flies fed on metepa (1-[Bis(2-methyl1-aziridinyl)phosphoryl]-2-methylaziridine) for seven days at a concentration of 1.5% resulted in complete sterility while concentrations as low as 0.5% resulted in sterility greater than 97%. Similarly, a diet of hempa (Hydroxyethylamino-di(methylene phosphonic acid)) at a concentration of 1.0% resulted in complete sterility. Concentrations of 2.5% gave unacceptably high mortality. The chemosterilants affected females in two ways; by reducing fecundity and by lowering egg hatch. Infecundity occurred before total non-hatch of eggs was obtained. A concentration of 2.5% metepa was required for total sterility and this caused 31% mortality. Conversely 2% hempa gave complete sterility with no significant increase in mortality. When applied topically, higher doses of hempa than metepa were required to produce sterility in males but the reverse was true for females. Mortality with both chemosterilants became a problem before a high level of sterility was achieved. Hempa produced sterility at lower concentrations than did metepa when applied in the diet. When applied to tarsae, complete sterility of males was obtained with both chemosterilants with metepa being more effective than hempa. Vuttanatungum and Hooper (1974) found that both sexes could be effectively sterilised when fed on the chemosterilants, suggesting that they could be applied in a protein bait for field control. Chemosterilants could be important for control of this pest however more research is required before this technique becomes common practice. Hooper (1975a) examined the effect of gamma radiation on sterility of newly emerged B. cucumis males. This author noted that the reductions in egg hatch produced by 9 and 11 krad treated males were not significantly different, but at both doses the egg hatch was significantly less than that of 5–7 krad treated males. Gamma doses of approximately 7–9 krad produced sterility levels of 97–99 per cent respectively in male B. cucumis. There was no significant effect of any treatment on the survival of males and females with about 20 per cent mortality after six weeks. Sterilizing doses of irradiation reduced competitiveness. As irradiation dose increased from 5 to 11 krad, the competitiveness of male B. cucumis decreased from 0.62 to 0.22. Hooper (1975b) evaluated the
6.4. Post harvest treatments A range of disinfestation treatments have developed over time. Swaine et al. (1978) reported that fumigation with ethylene dibromide (EDB) at 12 g m−3 over 2 h provided control of eggs and larvae exceeding 97.76%. EDB fumigation was effective to treat export zucchini (Jacobi et al., 1996) until EDB was banned in New Zealand in January 1994 (Jessup et al., 1994). Heather et al. (1992) demonstrated that dimethoate and fenthion were effective against B. cucumis in zucchinis and rockmelons. More than 30,000 eggs and larvae of B. cucumis were killed by dips of each of dimethoate and fenthion in each commodity with residue below the Australian maximum residue limit of 2 mg/kg on the day of treatment with no adverse effects on taste (Heather et al., 1992). The dimethoate and fenthion dips were used to export zucchini and rockmelon from Australia to New Zealand following the loss of EDB in 1994. Zucchini was removed from this protocol when some uses of dimethoate were suspended because of dietary concerns (APVMA, 2015) however rockmelon and honeydew melon still have approval to be exported from Australia to New Zealand using this pathway (Anon, 2014b). As worldwide concerns were raised about possible links between pesticide use and human health (Dominiak and Ekman, 2013), nonpesticide treatments were investigated. Chilling treatments were tested. Chilling caused injury to zucchini in the form of circular to longitudinal pits on the surface (Mencarelli et al., 1983). Some hot water treatments caused extensive damage to fruit: hot air treatments were found to be less punitive on fruit quality (Jacobi et al., 1996). Corcoran et al. (1993) found that a vapour heat treatment at 45 °C for 30 min was an adequate disinfestation treatment against B. cucumis in zucchini marrows. This treatment involved heating fruit to a core temperature of 45 °C with > 94% relative humidity for 30 min (Corcoran et al., 1993). Jacobi et al. (1996) examined the treatment developed by Corcoran et al. (1993) for its suitability as an export treatment from the fruit quality perspective. Corcoran concluded that fruit quality could be maintained for up to 11 days if fruit are handled correctly before the disinfestation treatment, particularly avoiding pre-cooling. 38
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Fruit Flies in the Pacific. A Regional Symposium, Nadi, Fiji 28–31 October 1996, pp. 95–101. Anon, 2014a. Cucumber Fruit Fly. Accessed 6/11/2014. http://www.daff.qld.gov.au/ plants/fruit-and-vegetables/a-z-list-of-horticultural-insect-pests. Anon, 2014b. Australia – New Zealand Bilateral Quarantine Arrangement. Systems Operation Manual 6E.Department of Agriculture Biosecurity Plant Division. Australian Government. APVMA, 2015. Australian Pesticides and Veterinary Medicines. Accessed 5/6/2015. http://apvma.gov.au/sites/default/files/fenthion-finalisation-report-rfrd-report.pdf. APVMA, 2016. Australian Pesticides and Veterinary Medicines. Accessed 11/07/2016. https://portal.apvma.gov.au/permits. Atuahene, S.K.N., Hooper, G.H.S., 1971. Insecticide susceptibility of, and metabolism of DDT by Dacus tryoni (Froggatt) and Dacus cucumis French (Diptera: Tephritidae). J. Aust. Entomol. Soc. 11, 135–142. Bailey, P., Shipp, E., 1970. 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A review of 16 years of quality control parameters at a mass-rearing facility producing Queensland fruit fly, Bactrocera tryoni. Entomol. Exp. Appl. 151, 152–159. FAO Food & Agricultural Oranization, 2003. Guidelines for the Use of Irradiation as a Phytosanitary Measure. ISPM#18. Food and Agricultural Organization, Rome, Italy. Fitt, G.P., 1986. The roles of adult and larval specialisations in limiting the occurrence of five species of Dacus (Diptera: Tephritidae) in cultivated fruits. Oecologia Berl. 69, 101–109. Fitt, G.P., 1990. Variation in ovariole number and egg size of species of Dacus (Diptera: Tephritidae) and their relation to host specialization. Ecol. Entomol. 15, 255–264. Fletcher, B.S., 1989. Chapter 8.1 Life history strategies of Tephritid fruit flies. In: In: Robinson, A.S., Hooper, G. (Eds.), World Crop Pests. Fruit Flies, Their Biology, Natural Enemies and Control Vol 3B. Elsevier, pp. 195–208. Fletcher, M.T., Kitching, W., 1995. Chemistry of fruit flies. Chem. Rev. 95, 789–828. Fletcher, M.T., Wood, B.J., Brereton, I.M., Stok, J.E., de Voss, J.J., Kitching, W., 2002. [180]-Oxygen reveals novel pathways in spiroacetal biosynthesis by Bactrocera cacuminata and B. cucumis. J. Am. Chem. Soc. 124 (26), 7666–7667. French, C., 1907. Fruit flies. J. Agric. Vic. 5, 301–312. Froggatt, W.W., 1910. Notes on fruit-flies (Trypetidae) with description of new species. Proc. Lin. Soc. N. S. W. 15, 862–872. Gillespie, P., 2003. Observations on fruit flies (Diptera: Tephritidae) in new south Wales.
Hall et al. (2007) demonstrated that heat disinfestation treatments resulted in high mortality of B. cucumis in zucchini and rockmelon and should meet the quarantine requirements for both international and interstate trade within Australia. In zucchinis, button squash, rockmelon, honeydew and watermelons, the eggs were the most tolerant life stage, followed by third instar larvae. In cucurbit vegetables, confirmatory trials conducted in zucchini showed that a treatment of 45 °C for 40 min resulted in no survivors from a total of 109,480 B. cucumis mature eggs. Confirmatory trials conducted in rockmelon showed that a treatment of 44 °C with no holding period resulted in no survivors from a total of 234,429 B. cucumis mature eggs. Currently, heat protocols have not been negotiated for market access. Host fruit of B. cucumis was exported from Australia to New Zealand using the winter window pathway, which relied on field control mechanisms, from 1 May–September 30 in any year (Anon, 2014b; Hall et al., 2007). The term ‘winter window’ refers to quarantine agreements which allow commodities to be imported, at times when fruit fly infestation is very low, into areas that have a winter climate that is not conducive to fruit fly establishment (Allwood 1997). The use of ionizing irradiation is also approved as a phytosanitary treatment against fruit flies including B. cucumis (FAO, 2003). For domestic trade, the Interstate Certification Assurance (ICA) No. 55 recognises a minimum dose of 150 Gy as a disinfestation treatment (QDAF, 2016). 7. Overview Bactrocera cucumis fills an unusual position in the Australian fruit fly landscape. It is an Australian native but has not transitioned to a larger host range as B. tryoni did, despite exposure to many new hosts for at least a century. It has stayed confirmed to the Northern Territory and Queensland; similarly B. frauenfeldi (Schiner) (Royer et al., 2016) did not spread into southern environments as did B. tryoni. It is one of the largest flies and the longest lived, compared with most other Australian fruit flies. Bactrocera cucumis spends much of its life cycle in non-crop vegetation and enters crop for egg laying while other species spend much of their time in crop vegetation for food, shelter and egg laying. The mating ritual is different to most other species as B. cucumis has no stridulation combs. Some aspects such as chemosterilization is much studied in B. cucumis but virtually not at all in other Australian fruit flies. Bactrocera cucumis many characteristics similar to B. tau and B. curcurbitae but has evolved in different locations. Bactrocera cucumis occupies an unusual and contradictory place in the Australian fruit fly landscape. This review of B. cucumis places the current level of knowledge of biology, ecology and management in one publication. Research into mating rituals, lures, distribution, seasonality, biological control, pre and post-harvest control and host range of cucumber fruit fly is ongoing. This information will be important in understanding B. cucumis and the development of new International Standards for Phytosanitary Measures to facilitate trade. All future management strategies are likely to use a systems approach, particularly following decline of the dimethoate and fenthion as end-point treatments. Acknowledgements Many scientists contributed to this manuscript and their support is acknowledged. Bruce Browne and Alison Seyb reviewed and improved earlier versions of this manuscript. Bruce Browne provided information from the APVMA website. Darryl Barbour and Craig Hull also provided early guidance. Dr Mark Krosch reviewed the Phylogenetic section. Two anonymous referees provided comments and improved the manuscript. References Allwood, A.J., 1997. Biology and ecology: prerequisites for understanding and managing fruit fly (Diptera: Tephritidae). In: Allwood, A.J., RAI Drew (Eds.), Management of
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