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.     

Attraction of female Chiracanthium mildei(Araneae: Clubionidae) to olfactory cues from maleMediterranean fruit flies Ceratitis capitata(Diptera: Tephritidae)

Chiracanthium mildei, a common sac spider (Clubionidae) in Israel, is an important predator of pest insects in citrus and apple orchards. Field observations indicate that the females of this hunting spider are attracted to traps containing the parapheromone trimedlure and males of the Mediterranean fruit fly (Ceratitis capitata),which were caught in these traps. Laboratory testsshow that C. mildei females are attractedto olfactory cues from male C. capitata, but notto trimedlure. This suggests that C. mildeimay be an important nocturnal predator of C.capitata.     

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.     

Empirical evidence of the mediterranean fruit fly movement between orchard types

Understanding species movement in the agroecological system is an important theme in ecology. A mark–release–capture experiment was conducted to study the dispersion behaviour of the Mediterranean fruit fly, Ceratitis capitata (Wied.; Diptera: Tephritidae; Medfly) in northern Israel. Four pairs of pear and citrus orchards were selected for the field experiments. Sterile flies dyed with different colours were released in three seasons during 2015 and 2016, based on the phenological stages of the hosts. The total number of captured marked sterile flies per trap (FT) was approx 300 in both April and August. In November, FT values decreased by about 35% to approximately 200. The wild Medfly that were also captured showed an opposite trend, from an FT of 1.8 and 6.4 in April and August, respectively, to an FT of about 330 in November. Marked sterile flies were captured in both the release and the neighbouring orchard sites. We found that the Medfly migrates from pear to citrus orchards during spring and from citrus to pear during summer, when there are no fruit-bearing trees in the orchards. However, during November, when the wild Medfly population prevails in the area, a clear pattern of migration is hard to identify, perhaps because of a possible interaction with the wild fly's population.     

Effects of recent experience on foraging in tephritid fruit flies

In field-cage studies, we investigated how the foraging behavior of tephritid fruit flies is modified by experience immediately prior to release on host plants. We observed females of a relatively monophagous species,Rhagoletis mendax (blueberry maggot fly), an oligophagous species,Rhagoletis pomomella (apple maggot fly), and a polyphagous species,Ceratitis capitata (Mediterranean fruit fly). Just prior to release on a host plant, the following kinds of stimuli were supplied: (1) single oviposition in a host fruit, (2) contact with 20% sucrose, (3) contact with a mixture of protein food (bird feces and sucrose), (4) contact with water, and (5) a walk over a host-plant leaf. When flies foraged on host plants without resources, search was most intensive (as measured by number of leaves visited) following a single oviposition in fruit, but residence time generally was the same following exposure to sugar, protein, and fruit stimuli.Rhagoletis mendax andC. capitata females visited the fewest leaves following exposure to water or host leaves, whereasR. pomonella foraged equally intensively following exposure to food stimuli, water, or leaves. On host plants containing resources (fruit and protein food), a single oviposition dramatically increased the number of females of all three species that found fruit compared to females that received experience with food, water or foliar stimuli. We found no significant effect of recent brief experience with any of the stimuli on subsequent attraction to protein food. Overall,C. capitata exhibited a higher propensity to abandon host plants than eitherR. mendax orR. pomonella. We suggest that this may reflect adaptations to differences in distribution of host plants in nature, strategies of dispersal, and host range.     

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.     

Recapture of sterile Mediterranean fruit flies (Diptera: Tephritidae) in California's Preventative Release Program

In southern California, the sterile insect technique has been used since 1994 to prevent establishment of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). This method involves the continual mass release of sterile flies, which suppress or eliminate any introduced wild fly populations. In addition, Jackson traps baited with trimedlure are deployed throughout the preventative release region for the dual purpose of detecting wild flies and monitoring released sterile flies. Sterile fly recapture data for a 3-yr period was compared with climate and to host plant (in which traps were placed). Precipitation was negatively correlated; and temperature and relative humidity were positively correlated with fly recapture levels. The highest numbers of flies were recaptured during trapping periods associated with intermediate relative humidity and temperature, and low precipitation. Flies were recaptured throughout the entire year, in traps that had been frequently relocated to host plants with fruit. This finding suggests that these flies were capable of locating acceptable fruit in a variety of abiotic conditions. However, these data do not necessarily suggest that measurements unimportant in explaining sterile fly recapture are not of value in determining other outcomes important to the goals of sterile release programs, such as reducing the likelihood of establishment of an introduced wild Mediterranean fruit fly population. Future research might build on these results in developing more precise models useful in predicting recapture of sterile flies.     

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.     

Population fluctuations and interspecific competition between Tephritid flies attacking fruit crops in the New Valley oases,Egypt

Population fluctuations of the Mediterranean fruit fly Ceratitis capitata (Wiedemann) and the peach fly Bactrocera zonata (Saunders) were monitored with lure trap collections in three provinces in the New Valley oases, Western Desert, Egypt. Results showed marked temporal differences in peak trap catches of the two flies in the selected sites all over the entire studied areas. One annual peak of C. capitata was recorded during both October 2005 and February 2006 and coincided with the ripening period of citrus trees in Kharga oases. However, two annual peaks were recorded during June and September 2005 in Bodkholow province and coincided with the ripening period of apple and mango. On the other hand, two annual peaks of B. zonata were recorded in Kharga oases throughout May and September and coincided with the ripening periods of apricot, mango and guava. One annual peak only was recorded in the round up of September and/or October in both Moot and Bodkholow in Dakhla oases and coincided with the ripening period of mango, guava and citrus. The occurrence of C. capitata was very limited in comparison with B. zonata. Population fluctuations of the two pests in the studied sites were significantly different. The ability of the traps used in capturing both C. capitata and B. zonata indicated that the yellow sticky trap was more effective in capturing C. capitata. However, the Abdel-Kawi trap was significantly efficient at trapping B. zonata. The occurrence of B. zontata in high numbers all over the study period compared to C. capitata is considered as good proof that this invading fly may be considered as a vigorous competitive tephritid fly to the native fly C. capitata.     

Electronic traps for detection and population monitoring of adult fruit flies (Diptera: Tephritidae)

During the last decades, the economic importance of tephritid fruit flies (FF) has increased worldwide because of recurrent invasions and expansions into new areas, and reduced control capabilities of current control systems. Efficient monitoring systems, thus, are required to provide fast information to act promptly. With this aim in mind, we developed two electronic trap (e‐trap) versions for adult FF: one with specific volatiles for male and female adult Ceratitis capitata, and the second, based on the attraction of adult FF to yellow colour, targeting Dacus ciliatus, Rhagoletis cerasi and Bactrocera oleae. In the case of B. oleae, the female pheromone and ammonium bicarbonate were added as synergists. In the two versions, attracted FF were retained in the trap on glued surfaces. Real‐time images of the surfaces were automatically taken and transmitted to a server. We tested the two e‐trap versions in insect‐proof cages, where flies were released and recaptured, and in commercial orchards throughout the Mediterranean: C. capitata in peach orchards in Italy; R. cerasi in cherry orchards in Greece; B. oleae in olive orchards in Spain and in Greece; and D. ciliatus in melons in plastic tunnels in Israel. The e‐trap showed excellent abilities to transmit real‐time images of trapped FF and a high specificity for trapping different FF species. The ability of the entomologist to correctly classify FF from images in the office was >88%. In addition, average number of flies/trap in e‐trap grids did not differ from numbers reported on grids of conventional traps that were operating simultaneously. The e‐traps developed and tested in this study provide the basis for the real‐time monitoring of FF were no olfactory attractants are available, and for the surveillance of alien FF incursions where generic, but not specific, olfactory attractants exists.     

Riding the Trojan horse: combating pest insects with their own symbionts

Insects form an extremely large group of animals and bear a consequently large variety of associated microbes. This microbiota includes very specific and obligate symbionts that provide essential functions to the host, and facultative partners that are not necessarily required for survival. The Tephritidae is a large family that includes many fruit pests such as the Mediterranean fruit fly (the medfly, Ceratitis capitata) and the Olive fly (Bactrocera oleae). Community and functional analyses showed that the microbiota of both flies contribute to their diet, and affect host fitness parameters. The analysis of the microbiota's community structure of mass‐reared, sterilized medfly males used in the sterile insect technique revealed a strong reduction in Klebsiella spp. compared with non‐sterile and wild flies. Inoculation of sterile males with this gut population affected female mating behaviour as they preferentially mated with inoculated versus non‐inoculated males. These studies suggest that control can be significantly improved by manipulating symbionts in pest animals.     

Comparative response to citrus foliage and citrus fruit odour by wild and mass-reared sterile Mediterranean fruit fly males of a genetic sexing strain

In greenhouse behavioural assessments conducted at Seibersdorf, Austria that allowed flies the choice of different types of potted host trees and plants, it was found that mature laboratory mass-reared Mediterranean fruit fly males, Ceratitis capitata (Wied), (Dipt. Tephritidae), strain Vienna-42 (temperature-sensitive lethal genetic sexing strain) showed the same preference for orange foliage, over other plants types and parts, as wild males. They aggregated in leks, released pheromone, and courted approaching females almost exclusively on orange foliage. Even though a number of other trees and plants were available to Vienna-42 males, less than 1% of these sexual activities occurred on the foliage or other plant parts of non-Citrus trees and not a single mating occurred there. In choice tests carried out in Chios, Greece in large field cages housing naturally planted orange trees, it was determined that mature and sterile Mediterranean fruit fly males of the same sexing strain responded to the odour emanating from the flavedo (due to superficial cuts made in the fruit peel containing the oil glands) of ripening sweet, sour oranges and lemons, in a similar intensity, order of fruit preference and time of day as did mature males of the local wild population. Males of both strains were frequently observed contacting with their mouth parts the oils exuding from the cuts made in the flavedo of the orange peel, or exhibiting homosexual activity on, or near the cuts. The results show that mass-reared, sterile males of the Vienna-42, genetic sexing strain behave in a comparable way to wild males in an important component of habitat location (odour of host foliage and host fruit) and hence are competitive with them in these respects. None of the standard international quality control tests for sterile Mediterranean fruit flies evaluates this important habitat location behaviour, which is a prerequisite for the successful encounter of the sexes in a sterile release programme.     

The influence of host fruit and temperature on the body size of adult Ceratitis capitata (Diptera: Tephritidae) under laboratory and field conditions

The adult body size of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), varies in natural conditions. Body size is an important fitness indicator in the Mediterranean fruit fly; larger individuals are more competitive at mating and have a greater dispersion capacity and fertility. Both temperature during larval development and host fruit quality have been cited as possible causes for this variation. We studied the influence of host fruit and temperature during larval development on adult body size (wing area) in the laboratory, and determined body size variation in field populations of the Mediterannean fruit fly in eastern Spain. Field flies measured had two origins: 1) flies periodically collected throughout the year in field traps from 32 citrus groves, during the period 2003-2007; and 2) flies evolved from different fruit species collected between June and December in 2003 and 2004. In the lab, wing area of male and female adults varied significantly with temperature during larval development, being larger at the lowest temperature. Adult size also was significantly different depending on the host fruit in which larvae developed. The size of the flies captured at the field, either from traps or from fruits, varied seasonally showing a gradual pattern of change along the year. The largest individuals were obtained during winter and early spring and the smallest during late summer. In field conditions, the size of the adult Mediterannean fruit fly seems apparently more related with air temperature than with host fruit. The implications of this adult size pattern on the biology of C. capitata and on the application of the sterile insect technique are discussed.     

Mediterranean fruit fly (Dipt., Tephritidae) suppression in persimmon through bait sprays in adjacent coffee plantings*

Abstract: Oriental persimmon, Diospyros kaki L., in Upper Kula on the island of Maui (Hawaii) is attacked by the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Recent suppression trials using mass trapping with a synthetic food‐based bait, initiated in alternate host crops before the start of persimmon season, had shown promise as a means of reducing C. capitata population levels. However, this did not adequately suppress C. capitata population where there were adjacent plantings of coffee, Coffea arabica L., a favoured alternate host, which bears fruits before and during the persimmon season. To improve C. capitata population suppression, we applied a spinosad‐based bait spray to coffee plants, starting before persimmon fruits became susceptible to oviposition by the Mediterranean fruit fly. The bait spray suppressed the C. capitata population and led to reduced infestation of both coffee cherries and persimmon fruits. Percentage parasitization of C. capitata in coffee cherries by established biological control agents, primarily Fopius arisanus (Sonan), was not significantly different in unsprayed vs. sprayed plots even after 11 weekly sprays. These results suggest that mass trapping, combined with spinosad‐based bait sprays, are control components that are compatible with biological control and can be combined in an integrated pest management system for C. capitata.     

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.     

Field evaluation of three-component solid food-based dispenser versus torula yeast for capturing Mediterranean and oriental fruit flies (Diptera: Tephritidae)

Certain species of true fruit flies (Diptera: Tephritidae) are worldwide pests of fruits and vegetables, and many countries operate trapping programs to detect and monitor invasions. Torula yeast-borax (TYB) solution is a widely used food bait, although its effective field longevity is relatively short (1–2 weeks). This led to the development of a synthetic cone-shaped food dispenser that contains ammonium acetate, putrescine, and trimethylamine. The food cone has received limited testing, and the objective of this study was to compare captures of the Mediterranean fruit fly (Ceratitis capitata (Wiedemann)) and the oriental fruit fly (Bactrocera dorsalis (Hendel)) in traps baited with the fresh TYB solution versus traps baited with fresh or weathered food cones. Captures showed a female bias for both baits and both species. For C. capitata, fresh food cones generally attracted more individuals than fresh TYB. Weathered food cones attracted similar or greater numbers of medflies than TYB for the initial two weeks, but food cones weathered for 4 or 6 weeks attracted fewer flies than TYB. For B. dorsalis, TYB-baited traps captured more females than fresh or weathered food cone-baited traps in each of six weekly sampling periods, and the differences were statistically significant in weeks 1–4. In a release-recapture experiment, both C. capitata and B. dorsalis were captured in higher numbers in traps baited with fresh TYB than those baited with food cones weathered for 0 (fresh) to 6 weeks. The implications of these results for fruit fly surveillance are discussed.     

Mediterranean fruit fly subplot hot spots prediction by experts' experience

The Mediterranean fruit fly (medfly), Ceratitis capitata (Wiedemann), is a major pest, infesting hundreds of crop types. Since current field monitoring is mostly manual, understanding the spatiotemporal patterns of pest emergence at the fine scale can optimize precise trap placement and site‐specific treatment activities, also within area wide integrated pest management projects. We carried out a three‐year study in deciduous orchards in Israel, testing for the existence of subplot hot spots in which medfly populations display small‐scale aggregations over consecutive seasons, beyond the expected spatial variability resulting from host type and ripening sequence. medfly population increase in these locations often preceded or was parallel to infestations in surrounding orchards, suggesting that hot spots can provide an important tool for effective prediction and control of pest emergence. We also examined the use of expert knowledge to predict hot spot locations and suggest a methodology for verifying them.     

Medfly Ceratitis capitata as Potential Vector for Fire Blight Pathogen Erwinia amylovora: Survival and Transmission

Monitoring the ability of bacterial plant pathogens to survive in insects is required for elucidating unknown aspects of their epidemiology and for designing appropriate control strategies. Erwinia amylovora is a plant pathogenic bacterium that causes fire blight, a devastating disease in apple and pear commercial orchards. Studies on fire blight spread by insects have mainly focused on pollinating agents, such as honeybees. However, the Mediterranean fruit fly (medfly) Ceratitis capitata (Diptera: Tephritidae), one of the most damaging fruit pests worldwide, is also common in pome fruit orchards. The main objective of the study was to investigate whether E. amylovora can survive and be transmitted by the medfly. Our experimental results show: i) E. amylovora can survive for at least 8 days inside the digestive tract of the medfly and until 28 days on its external surface, and ii) medflies are able to transmit the bacteria from inoculated apples to both detached shoots and pear plants, being the pathogen recovered from lesions in both cases. This is the first report on E. amylovora internalization and survival in/on C. capitata, as well as the experimental transmission of the fire blight pathogen by this insect. Our results suggest that medfly can act as a potential vector for E. amylovora, and expand our knowledge on the possible role of these and other insects in its life cycle.     

Cytogenetic analysis of chromosome 5 from the Mediterranean fruit fly,Ceratitis capitata

A cytogenetic map of chromosome 5 from the Mediterranean fruit fly, Ceratitis capitata, was constructed. Six mutations were located by translocation, transposition or deletion mapping. This knowledge allowed alignment and orientation of the existing linkage map with the polytene chromosomes. In addition, mapping of mutations used as selectable markers in genetic sex-separation strains is an essential prerequisite for the improvement of genetic stability during mass-rearing.     

Potential for host range expansion in Ceratitis capitata flies: impact of proximity of adult food to egg-laying sites

Abstract.

• 1 In field cage and field tests, female Mediterranean fruit flies, Ceratitis capitata (Wiedemann), in trees alighted in significantly greater numbers upon sticky-coated (non-odour-emitting) kumquats, Fortunella japonica, that were in the vicinity of odorous natural proteinaceous food (bird faeces) or synthetic food odour than on similar kumquats distant from bird faeces or synthetic food odour.
• 2 In field cage tests, oviposition in non-sticky kumquats nearby bird faeces was significantly greater than in non-sticky kumquats distant from bird faeces.
• 3 In field tests, medflies laid significantly more eggs in host kumquat and non-host hawthorn, Crataegus mollis, fruit adjacent to bird faeces and synthetic food odour than in fruit of these types distant from food-type stimuli.
• 4 These findings suggest that odour of natural food of medflies could lure flies to plants whose fruit emit little or no attractive odour and are not permanent hosts but which are nonetheless susceptible to egg-laying and larval development, resulting in temporary expansion of host range.