Potential for areawide integrated management of Mediterranean fruit fly (Diptera: Tephritidae) with a braconid parasitoid and a novel bait spray

The braconid wasp, Fopius arisanus (Sonan), a biological control agent for Mediterranean fruit fly, Ceratitis capitata (Wiedemann), was studied in coffee, Coffea arabica L. Fopius arisanus, comprised 79.3% of the total parasitoids (7,014) recovered from fruits collected at three small coffee farms. Data from seasonal host/parasitoid studies at a large coffee plantation also suggested that the most effective natural enemy of C. capitata in coffee may now reside in Hawaii. The original parasitoids introduced into Hawaii for C. capitata control (Diachasmimorpha tryoni (Cameron), Tetrastichus giffardianus Silvestri, and Dirhinus giffardii Silvestri) are now rare. Abundance of F. arisanus with respect to other parasitoids collected was influenced by elevation (274, 457, 610 m). Fopius arisanus was the dominant parasitoid at all three elevations, Diachasmimorpha longicaudata (Ashmead) occurred consistently, and T. giffardianus was abundant only at low elevation. The impacts on C. capitata and F. arisanus populations of bait sprays containing malathion, spinosad, or phloxine B applied to coffee were also evaluated. All three bait sprays suppressed C. capitata populations. Spinosad and phloxine B bait sprays appeared less harmful to the wasp than malathion. Fopius arisanus offers the potential for areawide management of C. capitata that includes biological control and integration with more environmentally safe chemical controls such as spinosad and phloxine B bait sprays.     

Spatio‐temporal distribution of Ceratitis capitata population in a heterogeneous landscape in Central Italy

The spatio‐temporal dynamics of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), was investigated to evaluate the effect of the landscape elements and host plants on pest distribution, in an agricultural landscape of 500 ha located in Central Italy. Two farms (farm 1 and farm 2) are located in the experimental area, composing mixed fruit orchards and surrounded by hedgerows, small woodlots, private gardens and cereal fields. Ceratitis capitata population fluctuation was monitored, from 2006 to 2008, using traps baited with trimedlure. Geostatistical methods such as Inverse distance squared weighted were used to obtain distributional maps of adults, mainly males. Results showed that the adult Mediterranean fruit flies were primarily distributed inside farm 1, with the maximum density found in the months of September and October. Away from the principal host plants, particularly in cereal fields, the number of trapped individuals was always low or zero. In both farms, flies were caught sequentially in traps located on host plants (i.e. peach, apple, pear, oriental persimmon and prickly pear) at varying times of maturation, especially when fruits remained on the trees. Distributional maps provided evidence that allowed to identify habitats in which the fly developed early in the season (mixed peach orchards) and afterwards during the periodic flights.     

Feeding and foraging of wild and sterile Mediterranean fruit flies (Diptera: Tephritidae) in the presence of spinosad bait

The sterile insect technique (SIT) is used to control wild Mediterranean fruit fly introductions in California and Florida in the U.S. In the past, bait sprays containing malathion proved invaluable in treating new outbreaks or large populations before the use of SIT. Recently, a spinosad protein bait spray, GF-120, has been developed as a possible alternative to malathion, the standard insecticide in protein bait sprays. In this study, protein-deficient and protein-fed Vienna-7 (sterile, mass-reared, "male-only" strain) flies and wild males and females were evaluated to determine the effectiveness of the GF-120 protein bait containing spinosad with respect to bait attraction, feeding, and toxicology. There were no effects of diet or fly type on feeding duration in small laboratory cages. Wild flies, however, registered more feeding events than Vienna-7 males. Flies that fed longer on fresh bait died faster. Protein-deficient flies were more active and found the bait more often than protein-fed flies. Data suggest that adding protein to the diet of SIT flies may decrease their response to baits, therefore, reduce mortality, and thus, allow the concurrent use of SIT and bait sprays in a management or eradication program.     

Attraction and feeding responses of Mediterranean fruit fly and a natural enemy to protein baits laced with two novel toxins,phloxine B and spinosada

Studies were conducted to determine attraction and feeding propensity of Mediterranean fruit fly, Ceratitis capitata (Wiedemann), to different protein bait mixtures with and without the insecticides malathion, spinosad, and phloxine B. Protein baits were more attractive to females than to males. Protein-starved females responded more than protein-fed females. The type of protein (USB^® yeast hydrolysate enzymatic, Mazoferm^®E802, Nu-Lure^®Insect Bait, or Provesta^® 621 autolyzed yeast extract) in the bait had a major influence on C. capitata attraction, which was strongest to fresh Provesta. Aged baits (four day-old) were not as attractive as fresh baits. In feeding propensity studies, highest response was observed for USB protein. On the basis of attraction and feeding responses Provesta (attraction and feeding) and USB (feeding) outperformed the standard Nu-Lure. Protein-starved flies were much more likely to feed on protein compared to protein-fed flies. For protein-starved flies, a mixture of Provesta and malathion repelled fruit flies, compared to a mixture of Provesta and spinosad or phloxine B. This was not the case with protein–fed flies. The wasp Fopius arisanus (Sonan), one of C. capitata's primary natural enemies in Hawaii, would not consume protein baits. Our studies suggest that spinosad or phloxine B, with low contact toxicity, mixed with protein baits offers a more environmentally friendly choice for control of C. capitata and conservation of F. arisanus, whereby the nontarget effects of broad spectrum contact poisons such as malathion can be avoided. Presumably, due to greater selectivity with spinosad and phloxine B bait treatments, the host would be killed, but not the natural enemy.     

Attract‐and‐kill systems efficiency against Ceratitis capitata (Diptera: Tephritidae) and effects on non‐target insects in peach orchards

For control of the Mediterranean fruit fly Ceratitis capitata (Diptera: Tephritidae), the attract‐and‐kill or attracticide technique is an alternative to the spraying of traditional organophosphate pesticides. In this study, the effectiveness of Ceranock and AAL&K attract‐and‐kill bait stations was assessed for control of C. capitata in Tunisian peach (Prunus persica) orchards. Our results showed that, in orchards with early‐ripening varieties, the numbers of C. capitata males and fruit damage were significantly lower in plots treated with Ceranock and AAL&K bait stations than in plots treated with conventional organophosphate and pyrethroid insecticides. In addition, the abundances of non‐target insects in the Chrysopidae, Coccinellidae and Miridae were significantly greater in plots treated with the bait stations than in plots treated with the conventional pesticides; that is, the use of attract‐and‐kill bait stations had fewer negative effects than the application of conventional pesticides on the biological diversity in Tunisian peach orchards. Overall, the results indicate that Ceranock and AAL&K attract‐and‐kill bait stations are useful alternatives for the control of C. capitata in Tunisian peach orchards planted with early‐ripening varieties.     

Field tests of environmentally friendly malathion replacements to suppress wild Mediterranean fruit fly (Diptera: Tephritidae) populations

This article reports a large-scale field test of two environmentally friendly malathion replacements on wild populations of the Mediterranean fruit fly, Ceratatis capitata (Wiedemann): spinosad, a bacteria-derived toxin, and phloxine B, a red dye with phototoxic properties. The comparison test was conducted on 11 coffee fields infested with wild populations of Mediterranean fruit fly on the Hawaiian island of Kauai with 8-wk protein bait sprays with and without toxicants. To assess effectiveness, adults were trapped and larval infestation levels were evaluated with fruit collections. Malathion was found to be the most effective treatment. However, the two replacements gave significant levels of control, and because they are environmentally safer, should be considered for eradicating incipient populations of this invasive species of fruit fly. Cage tests were also conducted to ensure that the wild flies consumed the bait and to assess how long the bait-toxicant combination remained effective in the field. Although spinosad and phloxine B were found to be effective up to 1 wk, malathion remained effective at least 2 wk.     

Toxicity of baited spinosad formulations to Ceratitis capitata: from the laboratory to the application

GF‐120, a fruit fly bait designed to attract and kill adult fruit flies, was tested in the laboratory and outdoors to determine effects of pre‐treatment diet and bait aging on mortality of Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Two spinosad‐based compounds, GF‐120 and Tracer^® Ultra, had generated two distinctive dose–mortality responds, with LC⁸⁰, LC⁹⁰, and LC⁹⁹ values of 2.4, 2.8, and 4.1 p.p.m., and 255, 479, and 1 143 p.p.m., respectively. The residues of GF‐120 drops, after feeding to the flies, generated 14.3% mortality. The droplet size of the baited spray plays an important role. The toxicity of large drops lasted more than that of small droplets. In the field, exposure to the sun further deteriorates the compound, which lost 50% of its toxicity within 6 days. Disappearance of the compound in the field, due to consumption by various insects, also played a role as 50% of the GF‐120 drops disappeared within 7 days. As mortality was directly related to the amount of insecticide eaten, the effect of GF‐120 depended on the feeding status of the flies: well‐fed flies were almost unaffected compared with starved ones.     

Toxicity of spinosad in protein bait to three economically important tephritid fruit fly species (Diptera: Tephritidae) and their parasitoids (Hymenoptera: Braconidae)

The feeding toxicity of the natural insecticide spinosad in Provesta protein bait was evaluated for three economically important fruit fly species, the Mediterranean fruit fly, Ceratitis capitata (Wiedemann); the melon fly, Bactrocera cucurbitae Coquillett; and the oriental fruit fly, Bactrocera dorsalis Hendel. Both females and males were evaluated. Spinosad was remarkably similar in toxicity to all three fruit fly species. Male C. capitata (24 h LC50 values and 95% fiducial limits = 2.8 [2.60-3.0] mg/liter spinosad) were significantly, although only slightly more susceptible to spinosadthan females (4.2 [3.8-4.6] mg/liter). Male (5.5 [4.7-6.6] mg/liter) andfemale (4.3 [3.7-4.9] mg/liter) B. cucurbitae were equally susceptible to spinosad. Female (3.3 [3.1-3.6] mg/liter) and male (3.1 [2.9-3.3] mg/liter) B. dorsalis also were equally susceptible to spinosad. Provesta bait containing spinosad also was evaluated against two parasitoids of tephritid fruit flies, Fopius arisanus (Sonan) and Pysttalia fletcheri (Silvestri). These parasitoids did not feed on the bait, so a contact toxicity test was conducted. Significant amounts of mortality were found only after exposure of parasitoids to spinosad-coated glass vials with concentrations > or =500 mg/liter spinosad. Parasitoids were less susceptible than fruit flies to such a degree that use of spinosad in bait spray should be compatible with these parasitoid species. Because the fruit flies tested in this study were so susceptible to spinosad, this product seems to be promising as a bait spray additive and a replacement for malathion for control of these species.     

Potential for insecticide resistance in populations of Bactrocera dorsalis in Hawaii: spinosad susceptibility and molecular characterization of a gene associated with organophosphate resistance

The potential for populations to become resistant to a particular insecticide treatment regimen is a major issue for all insect pest species. In Hawaii, for example, organophosphate (OP)‐based cover sprays have been the chemical treatment most commonly applied against oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), populations since the 1950s. Moreover, bait spray treatments using spinosad were adopted as a major control tactic in the Hawaii area‐wide fruit fly pest management program beginning in the year 2000. To determine the current level of spinosad and OP tolerance of wild B. dorsalis populations, bioassays were conducted on flies collected from a range of geographic localities within the Hawaiian islands. Adult B. dorsalis flies were tested (1) for the level of susceptibility to spinosad using LC₅₀ diagnostic criteria, and (2) for the presence of alleles of the ace gene previously shown to be associated with OP resistance. Regarding spinosad tolerance, only flies from Puna, the one area lacking prior exposure to spinosad, showed any significant difference compared to controls, and here the difference was only in terms of non‐overlap of 95% fiducial limit values. With respect to OP tolerance, specific mutations in the ace gene associated with resistance to these insecticides were found in only two populations, and in both cases, these alleles occurred at relatively low frequencies. These results suggest that at the present time, populations of B. dorsalis in Hawaii show no evidence for having acquired resistance to the insecticides widely used in control programs.     

Field efficacy of Ceratitis capitata (Diptera: Tephritidae) mass trapping technique on clementine groves in Spain

Mass trapping is being used in Mediterranean regions to control Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) in citrus. The technique is based on placing a high density of traps with an attractant (Ferag CC D TM^®, a three‐membrane dispensers of trimethylamine, ammonium acetate and diaminoalkane), and a toxicant, aiming to capture the highest numbers of adults in the grove. From 2006 to 2008, field trials were conducted in commercial Clementine (Citrus reticulata Blanco) groves to evaluate the efficacy against medfly of using different trap densities, 25, 50, 75 and 100 traps per ha. Based on the number of adults captured, fruit maturity parameters and medfly fruit damage, a 25 trap per ha density appears to be a valid stand‐alone method to protect mid‐season varieties (Clemenules) from the attack of C. capitata, because <0.5% of fruits on average were damaged at harvest. For early‐season varieties (Loretina and Marisol), mass trapping technique alone did not offer a satisfactory medfly control, because medfly populations were higher in the warmer months of the early‐season variety production, which led to a higher percentage of attacked fruits, even when increasing the trap density from 50 to 100 per ha. However, using 50 traps per ha density combined with chemical treatments only to the perimeter row of the grove gave good results, because <2% of fruits in average were damaged at harvest.     

Sterile males of Ceratitis capitata (Diptera: Tephritidae) as disseminators of Beauveria bassiana conidia for IPM strategies

Sterile Mediterranean fruit fly, Ceratitis capitata (Wied.), males were evaluated as vectors to spread Beauveria bassiana (Bals) conidia to wild C. capitata populations under field conditions. The inoculated sterile males were released by air, using the chilled adult technique over 7000 ha of coffee growing in Chimaltenango, Guatemala, Central America. The impact of releases was determined using dry traps baited with a food attractant. The effects of these releases on Apis mellifera, Linnaeus (honey bee), Hypothenemus hampei, Ferrari (coffee berry borer) and the parasitic mite Varroa destructor (Oudeman) were also evaluated. Inoculated sterile males were able to transmit fungal spores to 44% of the wild C. capitata flies captured in traps, which likely were infected through intra- and intersexual interactions during leks, mating or mating attempts. There was no transmission of the fungal spores to non-target insect species such as coffee berry borer, honey bees or varroa. We conclude that sterile males of Mediterranean fruit fly inoculated with B. bassiana can act as effective vectors of conidia to wild populations, constituting a safe, environmentally friendly and selective alternative for suppressing the medfly under a Sterile Insect Technique-based IPM approach.     

Advancements in management of major fruit flies (Diptera: Tephritidae) in North Africa and future challenges: A review

Fruit flies are one of the most economically damaging pests of fleshy fruits worldwide. Two species of highest concern for fruit production in North Africa are the Mediterranean fruit fly (Medfly) Ceratitis capitata (Wied.) and the peach fruit fly (PFF) Bactrocera zonata (Saunders) (in Egypt and Libya only). Currently, both fruit fly species are mainly targeted by chemical applications of broad-spectrum contact insecticides. Despite the disparities in control efforts among North African countries, government and research are focused on reducing chemical reliance and adopt more environmentally friendly technologies. In this review, advances in integrated pest management (IPM) implementation against fruit flies are outlined for each country. In addition, challenges for future efforts are identified with emphasis on the efficacy of trapping for monitoring and control.     

Comparative evaluation of spinosad and phloxine B as toxicants in protein baits for suppression of three fruit fly (Diptera: Tephritidae) species

Spinosad and phloxine B are two more environmentally friendly alternative toxicants to malathion for use in bait sprays for tephritid fruit fly suppression or eradication programs. Laboratory tests were conducted to assess the relative toxicity of these two toxicants for melon fly, Bactrocera cucurbitae Coquillett; oriental fruit fly, Bactrocera dorsalis Hendel; and Mediterranean fruit fly, Ceratitis capitata (Wiedemann) females. Field tests also were conducted with all three species to compare these toxicants outdoors under higher light and temperature conditions. In laboratory tests, spinosad was effective at much lower concentrations with LC50 values at 5 h of 9.16, 9.03, and 4.30 compared with 250.0, 562.1, and 658.9 for phloxine B (27, 62, and 153 times higher) for these three species, respectively. At 16 ppm spinosad, LT50 values were lower for all three species (significantly lower for C. capitata and B. dorsalis) than 630 ppm phloxine B LT50 values. At 6.3 ppm spinosad, the LT50 value for C. capitata (3.94) was still significantly less than the 630 ppm phloxine B LT50 value (6.33). For all species, the 100 ppm spinosad concentrations gave LT50 values of < 2 h. In comparison among species, C. capitata was significantly more sensitive to spinosad than were B. cucurbitae or B. dorsalis, whereas B. cucurbitae was significantly more sensitive to phloxine B than were C. capitata or B. dorsalis. LC50 values were reduced for both toxicants in outdoor tests, with greater reductions for phloxine B than for spinosad for B. dorsalis and B. cucurbitae. Fly behavior, though, is likely to keep flies from being exposed to maximum possible outdoor light intensities. Comparable levels of population suppression for any of the three species tested here will require a much higher concentration of phloxine B than spinosad in the bait.     

Effectiveness of GF‐120NF Fruit Fly Bait as a suppression tool for Bactrocera latifrons (Diptera: Tephritidae)

Bactrocera latifrons (Hendel) is a tephritid fruit fly of primarily Asian distribution that has invaded Hawaii and, more recently, the continent of Africa (Tanzania and Kenya). It primarily infests solanaceous fruits, so has the potential to impact production of crops such as peppers (Capsicum annuum L. and Capsicum frutescens L.), eggplant (Solanum melongena L.), African eggplant (Solanum aethiopicum L.) and tomatoes (Solanum lycopersicum L.). Because little work has been done to develop suppression techniques for this fruit fly species, field cage tests of the effectiveness of a commercially available bait spray, GF‐120NF Fruit Fly Bait, against wild B. latifrons were conducted. Sexually mature B. latifrons adults (75 male and 75 female) were introduced to both a control cage and a treatment cage, each of which held six fruiting Anaheim chili pepper (C. annuum L.) plants. Fruits were harvested, and assessed for infestation, both before and after the application of the bait spray in the treatment cage. There was no difference in infestation rate between control and treatment cages before the application of the bait spray, whereas there was a significantly lower infestation rate in treatment cages following the application of the bait spray. Post‐spray infestation rate in the treatment cages (in two separate, replicated bioassays) was always zero and no live flies were detected in the treatment cages at the end of the trials. The results of this study provide evidence that GF‐120NF Fruit Fly Bait should be effective in suppressing B. latifrons populations in the field.     

Eradication versus control of Mediterranean fruit fly in Western Australia

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Suppression of Ceratitis capitata (Wied.) (Diptera: Tephritidae) populations in coffee in the Mexico–Guatemala border region through the augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae)

In Guatemalan coffee plantations, Ceratitis capitata populations were suppressed by the application of augmentative releases of parasitoids. These releases significantly increased parasitism of this fruit fly over paired no-release control areas. Integrated management plus biological control presented a significant reduction in the pest population. These results support the application of biological control in C. capitata management.     

Acceptability and suitability of six fruit fly species (Diptera: Tephritidae) for Kenyan strains of Psyttalia concolor (Hymenoptera: Braconidae)

Host acceptability and suitability Psyttalia concolor (Szépligeti) is a koinobiont, larval parasitoid of tephritid fruit flies. Individuals of P. concolor were field-collected from coffee in the central highlands of Kenya, and cultured initially on Mediterranean fruit fly (medfly), Ceratitis capitata (Wiedemann). They were then examined for their ability to oviposit in and develop on five other tephritid species that are pests in Kenya. In addition to the medfly, acceptability for oviposition and suitability for development were tested against the mango fruit fly, Ceratitis cosyra (Walker), the Natal fruit fly, Ceratitis rosa Karsch, Ceratitis fasciventris (Bezzi), Ceratitis anonae Graham and the melon fruit fly, Bactrocera cucurbitae (Coquillett). Ceratitis capitata and C. cosyra were accepted as hosts significantly more often than the other species. Superparasitism was recorded only from C. capitata and C. cosyra. Two days after oviposition, parasitoid eggs in C. fasciventris and B. cucurbitae were encapsulated, whereas those in C. rosa and C. anonae were encapsulated, and often melanized. Ceratitis capitata was the most suitable host for Kenyan populations of Psyttalia concolor in terms of progeny production, and proportion of female progeny.     

Insecticide,sugar, and diet effects on feeding and mortality in Rhagoletis indifferens (Dipt., Tephritidae)

The effects of spinosad bait and various insecticides, the presence of sugar in insecticides, and diet on feeding responses and mortality in western cherry fruit fly, Rhagoletis indifferens Curran (Dipt., Tephritidae), were determined. Numbers of feeding events on insecticides with sugar were greater than on insecticides alone, but there was only a small effect of diet on feeding responses to insecticides with sugar. Feeding durations on imidacloprid, thiamethoxam and acetamiprid with sugar were shorter than on sugar water and spinosad bait, as the neonicotinoids paralysed flies quickly. Flies that fed on sugar only (nitrogen‐starved) suffered higher mortalities when exposed to spinosad, thiamethoxam and azinphos‐methyl than to imidacloprid, acetamiprid and indoxacarb, and mortality in between these two groups of treatments when exposed to spinosad bait. Mortalities were greater when sugar was added to insecticides, and were higher in nitrogen‐starved than fully‐fed (yeast extract + sugar fed) flies. Flies that fed once on thiamethoxam were killed more quickly than those that fed once on spinosad bait and spinosad. Results suggest that thiamethoxam is comparable to spinosad in its effects on mortality, and that using it with sugar in bait may also have similar results as using spinosad bait or spinosad. One benefit of using thiamethoxam with sugar may be that it kills flies more quickly, before they can oviposit, than spinosad bait, although whether a fly will feed on it may depend on how much sugar or nitrogenous food it has eaten.     

Nontarget impact of spinosad GF-120 bait sprays for control of the Mexican fruit fly (Diptera: Tephritidae) in Texas citrus

Bait sprays containing the toxicant spinosad (GF-120) were applied to citrus groves in the Rio Grande Valley of Texas where Mexican fruit flies were detected in surveillance traps. The sprays were applied as a supplement to a continuous sterile insect release program. Sterile fly captures were 47-63% lower in the treated groves compared with control groves. Eight of 10 secondary pest populations declined in the test groves subsequent to spray applications, but they also declined in the control groves, suggesting that the decline was a seasonal phenomenon rather than a result of the bait sprays. Citrus whitefly, Dialeurodes citri (Ashmead), populations increased modestly and citrus blackfly, Aleurocanthus woglumi (Ashby), populations remained unchanged compared with pretreatment levels. Thus, no outbreaks of secondary pests occurred as a result of the spinosad bait sprays in this instance, as has been reported for malathion bait sprays in citrus. The bait sprays had no detectable effect on populations of specific indicator species of parasitoids (including Aphytis spp. and Comperiella bifasciata Howard), or on numbers of beneficial insects in general, in the treated groves.     

Interference between male‐targeted and female‐targeted lures of the Mediterranean fruit fly Ceratitis capitata (Dipt., Tephritidae) in Italy

The efficacy of male‐targeted and female‐targeted baits was compared when lures were presented together or singly in traps for capturing the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). For male‐targeted baits, either trimedlure or ceralure presented singly attracted large numbers of flies, supporting data from many previous reports. The present results are the first published data on the attractiveness of ceralure to a European population of C. capitata. The quaternary female bait consisting of ammonium carbonate, putrescine, trimethylamine and acetic acid was a potent attractant for female flies (and also showed some activity for males). Replacing acetic acid with ammonium acetate in the quaternary female bait did not influence activity. Traps with female‐targeted and male‐targeted baits together always showed a tendency of catching fewer flies than traps with only one type of bait. The decrease was significant in females, regardless of whether ceralure or trimedlure was the male‐targeted bait. In males, the tendency was the same for traps with trimedlure or ceralure alone, catching higher numbers than those with both male and female baits. Our present results suggest that both types of baits mutually decrease the numbers of the non‐target sex in the trap. In conclusion, it is advisable to use both male‐ and female‐targeted baits in separate and distant traps and not jointly in the same trap, lest the efficacy of detection or monitoring trials be compromised.