Review

Fruit flies (Diptera: Tephritidae) on vegetable crops in Reunion Island (Indian Ocean): state of knowledge, control methods and prospects for management

1 2 3 4 Philippe RYCKEWAERT *, Jean-Philippe DEGUINE , Thierry BRÉVAULT , Jean-François VAYSSIÈRES

1 Cirad, UPR HortSys, Fruit flies (Diptera: Tephritidae) on vegetable crops in Reunion Island (Indian TA B-103/L, CSIRO, Ocean): state of knowledge, control methods and prospects for management. Campus Int. Baillarguet, Abstract –– Significance of fruit flies in vegetable crops. Vegetable crops hold a key position in agri- F-34398 Montpellier, France cultural production in Reunion (Indian Ocean); however, many pests and diseases threaten the profitability [email protected] of this agricultural sector. Fruit flies (Diptera: Tephritidae) figure among the main pests for solanaceous crops and cucurbits (cucumber, zucchini, melon, etc.). Losses of as much as 80% of tomato and 100% of 2 Cirad, UMR PVBMT, Stn. cucurbit crop harvests have been frequently observed. Inventory and distribution. Four fruit fly species Ligne-Paradis, Pôle 3P, belonging to the Tephritidae family cause major damage to vegetable crops in Reunion: Bactrocera cucur- bitae (Coquillet), Dacus ciliatus Loew and D. demmerezi (Bezzi) on Cucurbitaceae, and Neoceratitis cya- 7 chemin de l'IRAT, nescens (Bezzi) on Solanaceae (primarily the tomato). Distribution of each of them is presented. Biology F-97410 Saint-Pierre, La and behavior. A few studies on the biology and behavior of the four fruit flies were conducted in Reunion Réunion, France in the late 1990s. Their main biological characteristics are summarized. Population control methods used in Reunion. Various methods such as chemical control, preventive measures (sanitation), physical 3 Cirad, UR SCA, Univ. Arizona, control, biotechnical control [colored traps, the Male Annihilation Technique (MAT) and the Bait Applica- Dep. Entomol., Forbes 410, tion Technique (BAT)], and biological control currently used in Reunion against fruit flies are reported. PO Box 2100 (36), Tucson Other control methods such as Integrated Pest Management and the Sterile Insect Technique are not used in Reunion. Prospects for implementing agro-ecological management of vegetable fruit flies in AZ 85721, U.S.A. Reunion. This part presents research actions implemented in fly bio-ecology, research actions into the 4 genetic structure of populations and design of an agro-ecological management scheme for vegetable fruit Cirad, UPR HortSys, IITA, flies. Conclusions. The control methods used independently have not been successful to effectively 08 BP 0932, Tri postal control tephritid populations. A more integrated approach is required, also taking into account the lands- Cotonou, Bénin cape scale and its mosaic of habitats, especially wild plants, whose role must be considered within a fra- mework of agro-ecological management of these pest populations. Reunion / vegetable crops / Tephritidae / Bactrocera cucurbitae / Dacus ciliatus / Dacus demmerezi / Neoceratitis cyanescens / pest control / control methods

Les mouches des fruits (Diptera : Tephritidae) sur légumes à la Réunion (océan Indien) : état des connaissances, méthodes de contrôle et perspectives de gestion. Résumé –– Importance des mouches des fruits en cultures maraîchères. Les cultures maraîchères occupent une position clé dans la production agricole à la Réunion (océan Indien), toutefois, de nombreux ravageurs et maladies menacent la rentabilité de ce secteur agricole. Les mouches des fruits (Diptera : Tephri- tidae) figurent parmi les principaux ravageurs des solanacées et des cucurbitacées (concombre, courgette, melon, etc.). Des pertes de près de 80 % des récoltes de tomate et de 100 % de cucurbitacées ont été fré- quemment observées. Inventaire et distribution. Quatre espèces de mouches des fruits appartenant à la famille des Tephritidae provoquent des dommages importants aux cultures légumières à la Réunion : Bac- trocera cucurbitae (Coquillet), Dacus ciliatus Loew et D. demmerezi (Bezzi) sur les cucurbitacées, et Neo- ceratitis cyanescens (Bezzi) sur les solanacées (principalement les tomates). La distribution de chacun d'eux est présentée. Biologie et comportement. Quelques études sur la biologie et le comportement des quatre mouches des fruits ont été menées à la Réunion dans les années 1990. Leurs principales caractéristiques * Correspondence and reprints biologiques ont été résumées. Méthodes de contrôle des populations utilisées à la Réunion. Diverses méthodes utilisées actuellement à la Réunion contre ces mouches des fruits sont exposées : lutte chimique, mesures préventives (assainissement), contrôle physique, contrôle biotechnique [pièges colorés, technique d’élimination des mâles (MAT) et technique d’utilisation d’appâts (BAT)] et lutte biologique. D‘autres Received 24 June 2009 méthodes de lutte comme la lutte intégrée, et la technique des insectes stériles ne sont pas utilisées à la Accepted 22 September 2009 Réunion. Perspectives de mise en œuvre de la gestion bio-écologique des mouches de fruits en culture maraîchère à la Réunion. Cette partie présente les actions de recherche mises en œuvre en bio- écologie de la mouche, les actions de recherche sur la structure génétique des populations et la conception Fruits, 2010, vol. 65, p. 113–130 d'un système de gestion agro-écologique pour les mouches des fruits des légumes. Conclusions. Les © 2010 Cirad/EDP Sciences méthodes utilisées indépendamment les unes des autres n’ont pas prouvé leur efficacité pour contrôler les All rights reserved populations de téphritides. Une approche plus intégrée est nécessaire qui prendrait en compte l’échelle du paysage et de sa mosaïque d’habitats, en particulier les plantes spontanées dont le rôle doit être considéré DOI: 10.1051/fruits/20010006 dans le cadre d’une gestion agro-écologique des populations de ces ravageurs. www.fruits-journal.org Réunion / plante légumière / Tephritidae / Bactrocera cucurbitae / Dacus ciliatus / RESUMEN ESPAÑOL,p.130 Dacus demmerezi / Neoceratitis cyanescens / lutte antiravageur / méthode de lutte

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1. Significance of fruit flies vegetable crops in Reunion: Bactrocera in vegetable crops cucurbitae (Coquillet), Dacus ciliatus Loew and D. demmerezi (Bezzi) on Cucurbita- Vegetable crops hold a key position in agri- ceae, and Neoceratitis cyanescens (Bezzi) cultural production in Reunion Island on Solanaceae (primarily the tomato) [4, 5]. (Indian Ocean) due to the number of farm- Other species specialized on fruit crops such ers involved and the income generated by as Ceratitis capitata (Wiedemann) and Bac- this industry. So besides sugar cane, Reun- trocera zonata (Saunders) have been ion’s historical crop, vegetable production reported on vegetable crops, but do not represented nearly 42 000 t in 2006, with a cause significant damage in Reunion Island surface area of 1800 ha, i.e., slightly less (S. Quilici, pers. comm.). than fruit production [1]. However, many Bactrocera cucurbitae, the melon fly, has pests and diseases threaten the profitability been relatively recently introduced into of this agricultural sector [2], forcing farmers Reunion (identified in 1972), probably from to resort to synthetic pesticides with all the India via Mauritius [3]. Its current distribu- risks that this entails for human health and tion ranges from South Asia, whence it orig- the environment. Fruit flies (Diptera: inates, to many Pacific Islands (including Tephritidae) figure among the main pests Hawaii) and, more recently, the Seychelles for solanaceous crops (in particular, field- and Africa, where it is currently spreading grown tomato, Lycopersicum esculentum [6]. Its biology is relatively well known, and Mill.) and cucurbits: cucumber (Cucumis the species has been much studied in India, sativus L.), zucchini (Cucurbita pepo L.), South-East Asia and Hawaii [7]. It is a ther- melon (Cucumis melo L.), etc. Losses of as mophilic species not commonly found at much as 80% of tomato and 100% of cucurbit altitudes over 800 m in Reunion. crop harvests have been frequently observed. Dacus ciliatus, the Ethiopian cucurbit fly, According to farmers, fruit fly damage to was probably introduced from Africa vegetable crops has become significantly whence it originated. It has been reported greater since the 1990s, although the various in Reunion since 1964 [4]. It is also present species concerned had been reported for in most of the South-West Indian Ocean several decades [3]. Broad-spectrum insec- islands, but also in India and South-East Asia ticides, often unauthorized for the given crop, [8]. It has been much less studied than the have been used at high doses and frequen- species above. It is a eurythermal species, cies, without rotation of chemical families, since it has been found in Reunion from the which has probably negatively impacted on shore to high-altitude areas (at least 1200 m). natural enemies of these pests and led to Dacus demmerezi, the Indian Ocean development of resistance. These practices cucurbit fly, is a more stenothermal species, have led to the impossibility of maintaining probably originating from the Madagascan populations below an economic threshold. plateau. It was first reported in Reunion in Besides poor management of this chemical 1972 [3]; it is also present in Mauritius. Due control and the use of unsuitable insecti- to its limited distribution, the species has cides, other hypotheses regarding changes been very little studied, although this spe- of cropping practices could explain these cies causes sometimes major damage in proliferations: spatial expansion and, during high-altitude areas of Reunion Island (above other seasons of cultivated and wild host 600 m). As such, it is considered to be a sec- plants, lack of rotation and fallow, introduc- ondary damaging species in Mauritius, a tion of more susceptible varieties, and relax- low-altitude island (P. Sookar, pers. comm.). ation in the application of prophylaxis recommendations. Each of these three species may poten- tially cause entire destruction of the crop, although generally two species are found 2. Inventory and distribution coexisting in the same location, according to the altitude and season. Relatively mild Four fruit fly species belonging to the attacks have been registered on certain zuc- Tephritidae family cause major damage to chini, cucumber and melon cultivars [4].

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The tomato fruit fly, Neoceratitis cyanes- females mate very frequently, about three cens, has been described in Madagascar, out of four days [12]. The pre-oviposition where it is probably indigenous. It is not period lasts from 4 to 6 days. Larval devel- considered as a major pest there, though we opment in the fruit lasts from 10 to 15 days have been unable as yet to explain this [13]. Upon maturing, the larvae burst out of observation. The species was introduced the fruit, and then pupate in the soil. As into Reunion and then into Mauritius, where pupation lasts around ten days, the devel- the first damage was reported in 1951 and opment cycle from egg to adult takes 21 to 1958, respectively [9]. Its presence in 31 days [9, 13, 14]. In response to odors Mayotte (Comoro Archipelago) was only released by host plants, and carried by the reported in 1992 [4], while it was present a wind, the tomato fly females are guided to long time before this first mention. In Reun- the source by successive flights [5]. After ion Island, the distribution area of the tomato arriving at the host habitat, visual stimula- fly extends from the coast to an altitude of tion alone is sufficient to guide their landing 1500 m, according to the availability of host onto the fruit [15]. Females respond strongly plants [3]. We observed that there are no flies to a bright orange-colored sphere, which present at altitude during the cool season probably mimics the host fruit [15, 16]. How- but no study has been conducted to test dia- ever, the incorporation of appropriate olfac- pause, quiescence or migration hypotheses. tory signals enhances their search efficiency [17]. The response to stimuli is affected by the nature and structure of the habitat [17]. The response of females to a host fruit type 3. Biology and behavior visual signal depends on their age and their egg load, but also their nutritional condition A few studies on the biology and behavior [15]. This response is at its greatest in the of these insects were conducted in Reunion afternoon, the preferred period for ovipos- Island in the late 1990s. We summarized the iting [18]. main biological characteristics of the four species mentioned (table I). Bactrocera cucurbitae, Datus ciliatus and D. demmerezi are three oligophagous spe- The tomato fruit fly, Neoceratitis cyanes- cies specialized mainly on the Cucurbita- cens, is one of the main pests of solanaceous ceae family, the first two developing on crops, on which it stings young fruits to lay 16 species and the latter on 13 species [4]. its eggs. This species is specialized on the Of these 16 species, four are wild Cucurbita- Solanaceae family, represented by around ceae – Coccinia grandis (L.) Voigt, Momor- twenty species in Reunion, but only eight dica charantia L., Cucumis anguria L. and are considered as host plants [10]. It causes Lagenaria sphaerica (Sonder) Naudin – significant damage to field-grown tomato which act as reservoir plants, enabling and, to a lesser extent, to the sweet pepper above all the reproduction of B. cucurbitae (Capsicum annuum L.), eggplant (Solanum and D. ciliatus all year round, primarily on melongena L.), tree tomato [Cyphomandra the shore with the driest wind [4]. These two betacea (Cav.)] and chilli pepper (Capsicum species are polyvoltine at low altitude. In frutescens L.). Other wild or sub-indigenous Reunion Island, besides Cucurbitaceae, we Solanaceae such as the black nightshade can report rare attacks on the tomato, wild (Solanum americanum Mill.), bug weed passion fruit (Passiflora foetida L.) and pas- (S. mauritianum Scop.) and turkey berry sion fruit (Passiflora edulis Sims) [4]. We (S. torvum Sw.) serve as breeding reser- noted that B. cucurbitae attacks the tomato voirs. The wide distribution of these host and papaya little or not at all (Carica plants on the island up to an altitude of papaya L.) in this island, whereas it causes 1500 m, as well as abundant, nearly unin- damage to these crops in other parts: India terrupted fruit bearing, offer suitable condi- [19], Cameroon [20], Hawaii [21] and Benin tions for the development of tomato fruit [6]. This probably results from competition flies all year round [11]. for resources with N. cyanescens for the Mating starts from the second day after tomato, and with various fruit fly species emergence of the adults. At 25 °C, the (Ceratitis spp.) that might develop on the

Fruits, vol. 65 (2) 115 P. Ryckewaert et al. )=40d ) = 142 d ) = 123 d – o o o At 25 °C At 25 °C: At 25 °C: parameters timeT=47d timeT=51d timeT=45d Reproductive birth (e birth (e birth (e Mean generation Mean generation Mean generation Expectation of life at Expectation of life at Expectation of life at rate = 218–588 eggs rate = 190–310 eggs rate = 142–225 eggs Growth reproductive Growth reproductive Growth reproductive d=8°C d=9°C At 25 °C At 25 °C: At 25 °C: At 25 °C: Development Development Development Development threshol threshol Egg to adult 26 d Egg to adult 26 d Egg to adult 26 d Egg to adult 26 d threshold = 11 °C threshold = 11 °C Development time Ovarian maturity 4 d K = 322 degree days K = 323 degree days K = 355 degree days K = 433 degree days Ovarian maturity 11 d Ovarian maturity 11 d Ovarian maturity 16 d , . Sw . ., (Sonder) (Sonder) (Sonder) Lagenaria Lagenaria Lagenaria Cucumis Cucumis Cucumis Mill L., L., L., Scop Naudin. Naudin. Naudin. Coccinia grandis Coccinia grandis Coccinia grandis Wild host plants sphaerica sphaerica sphaerica (L.) Voigt, (L.) Voigt, (L.) Voigt, L., L., L., anguria anguria anguria Momordica charantia Momordica charantia Momordica charantia Solanum torvum Solanum americanum Solanum mauritianum L., L., L., L., (Cav.) Cucurbita Cucumis (Jacq.) Sw. L., Cucumis melo Duch., Sendtn. 13 species 13 species Solanaceae: L., Cucurbitaceae: Cucurbitaceae: Cucurbitaceae: Capsicum annuum 16 species including Cultivated host plants Solanum melongena Capsicum frutescens maxima Lycopersicon esculentum Sechium edule Mill., sativus Cucurbita pepo Cyphomandra betacea altitude < 800 m > 600 m Preferred 0–1200 m 0–1500 m area Ocean East and Northern Reunion, Reunion, Reunion, Mauritius Comoros Mauritius, Mauritius, Seychelles Distribution West Africa, islands, Asia Asia, Pacific, Madagascar, Madagascar, Africa), Indian Africa (except Asia Africa Madagascar Madagascar Area of origin High High Moderate Moderate economic economic economic economic Economic importance importance importance importance importance fly fly Name Melon fly cucumber fly, Lesser cucurbit fly Tomato fruit pumpkin fly, Indian Ocean Ethiopianfruit Table I. Economic importance and bioecology of fruit flies on vegetables onSpecies Reunion [4, 5]. Bactrocera cucurbitae Dacus ciliatus Dacus demmerezi Neoceratitis cyanescens

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papaya in Reunion. It could also involve a 4. Population control methods special biotype of this species, but this used in Reunion Island aspect has not been investigated. The fruit of cultivated species is attacked In Reunion Island, control of fruit flies is still by females of the three species within largely based on the use of insecticides. around ten days of fruit setting and some- Research issues have gradually turned times even before the ovary has been ferti- towards alternative methods, taking inspira- lized, as it is often the case with the pumpkin tion from work already conducted on and zucchini. Hence these fruits are gener- orchard fruit flies in the island, or on vege- ally punctured two days before fruit setting, table fruit flies worldwide. We summarized the fruits of the watermelon [Citrullus lana- the various methods currently used against tus (Thunb.)] are punctured two to six days these flies in Reunion Island (table II). after, and the fruits of the cucumber are punctured four to ten days after [22]. These 4.1. Chemical control three Dacini species may lay their eggs in either the vegetative part of the plant (stems) Until now, farmers have applied foliar insec- or in the floral organs (male and female ticides directly onto plots in order to control flowers). These two biological characteris- either adults present in the crop directly via tics relating to egg-laying may partly explain contact or inhalation, or adults arriving at why some farmers do not identify the dam- the plot subsequently via a residual or repel- age caused by these pests [4]. Furthermore, lent effect. Overall, farmers have reported the extensive cropping systems (picking the effectiveness of these sprayings, although type) which are quite frequently encoun- they have not been proved by field experi- tered are a factor favoring development of ments in the island. These applications have Tephritidae populations because of (i) the no effect on larvae survival, which are pro- absence of cropping and control practices, tected inside the fruits. Laboratory studies and (ii) the presence of “reservoir plants” have demonstrated the efficacy of several through the absence of human intervention. active ingredients on imagoes [26, 27], but transposing this to the field did not neces- Study of demographic parameters of sarily give the same results. D. ciliatus showed a high biotic potential, The frequent and repeated use of various which could partly explain its wide geo- insecticides belonging to three main chem- graphic distribution in Asia and Africa [23], ical families (organophosphates, carbamates just like B. cucurbitae [24]. Experiments on and pyrethroids), has perhaps led to resist- the behavior of D. ciliatus showed that the ance, which could partly explain the increase orange color was significantly more attrac- in damage observed over the past few years, tive to sexually mature females, and that the but no studies have been conducted on this yellow color was significantly more attrac- issue in Reunion. Furthermore, these insec- tive to sexually mature males [25]. These ticide sprayings probably reduce populations responses of D. ciliatus to visual stimuli of natural enemies (predators, parasitoids, could be used to improve trapping of this etc.), as a natural pest control. species as part of biotechnical control, as could the investigation of chemical stimuli. Observations of daytime activities of some fruit fly species demonstrated that only The spatio-temporal distribution of these females entered the plot to lay eggs, whereas insects depends both on biotic factors (spe- males or immature females remained located cific bio-ecological characteristics, host fruit in the immediate surroundings of fields availability, presence of other competing (e.g., hedges) to feed, mate or rest [4, 5]. species, etc.) and abiotic factors (tempera- Hence treatments applied to the field will at ture, humidity, wind, etc.). Populations are best only affect part of the adult population. particularly high during the southern sum- mer (December to March) both in terms of 4.2. Preventive measures (sanitation) spatial distribution and density. Conse- quently, their economic impact on crops is Unsellable fruits, especially those housing considerable during this period. larvae, left on the ground or on plants, are

Fruits, vol. 65 (2) 117 P. Ryckewaert et al. – Propositions Farmers’ training Collective buying of nets; Reduction of pesticide use release of new parasitoid species. conduct trials on other crops (tomato) Development of new sexual attractants Production of parasitoids in augmentorium; Development of new products (success bait…) management of environment to favor beneficials; Drawbacks A bit applicable Man-power cost; for great releases are not registered sheltered cucurbits registered products uncommon practice Useful insect capture Mass rearing techniques and Net costs; only applicable for Unavailability of effective and production costs of beneficials Attractants for only two species Cost, dangerous, some products Not used Not used Often used Rarely used Rarely used Rarely used Moderately used in Reunion Island Actual use by farmers Yes control Efficacy in the field Not enough Not enough Shown in Hawaii natural beneficial populations are low Efficient in collective Not enough because Not validated or proven Table II. Control methods used against vegetable fruit flies in Reunion. Methods Chemical control Prophylaxis (gathering of stung fruits) Physical control (mosquito net) Yellow sticky traps Male Annihilation Technique (MAT) Bait Application Technique (BAT) Biological control

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a major reservoir for the next generation forward against flies. However, using agro- [28]. Elimination of these fruits should be textile nets has often proven problematic systematic so as to reduce subsequent infes- under tropical conditions due to the plant tations. It is also recommended to destroy being subjected to big temperature and crop residues after harvest. However, these humidity rises, causing poor plant develop- principles are still little implemented by ment or development of diseases (pers. obs.). farmers in Reunion, above all for issues of Furthermore, these nets prevent flower pol- custom and labor costs. lination, which is essential in most Cucur- The absence of host plants (cultivated or bitaceous plants, especially as fruit fly egg- not) during a period in principle offers little laying starts even before the female flowers benefit on a single farm in view of the flies’ open [4]. Finally, the cost of these nets high mobility capacities and their lifetime of remains prohibitive in Reunion Island, as several months. However, these periods well as the labor required to handle them. exist at high altitude during the Southern However, mini-tunnel systems communicat- winter (June to September), but we soon ing with hives have been tested with success observe recolonization of the crops when inSenegal[30,31].Practicesofindividualfruit the temperature increases, although we can- bagging using nets are sometimes employed not say whether these are overwintering in some countries with low labor costs [32]. populations (very likely for D. demmerezi In Guinea, straw protection of very young in view of its distribution primarily at high pumpkin and zucchini fruits has yielded altitude), or migrants from lower altitude. beneficial results, significantly reducing Eliminating uncultivated host plants around infestations (J.-F. Vayssières, pers. obs.). the edges of plots, such as the wild bitter Observations, followed by a trial by the melon, does not seem to have much effect Fédération Départementale des Groupe- on infestation. Indeed, most Cucurbitaceous ments de Défense contre les Organismes plots located in areas where they are not Nuisibles (FDGDON, St Paul, La Reunion), normally grown (big sugar cane cropping demonstrated that cucurbit flies do not regions) but with bitter melons (Mormodica enter open plastic tunnels housing cucum- charantia) present around the edges, have ber crops, the openings of which are closed always had very little infestation (pers. obs.). off by bird nets (mesh size around 3 cm, It would also seem that the permanent pres- black). The phenomenon has not currently ence of suitable crops in a production area been explained; the net may disrupt the maintains the high population levels flight behavior of the flies, preventing them observed. For the tomato fruit fly, the impor- from entering in spite of the large mesh tance of bug weed (Solanum mauritianum) size. Another case concerns open tomato as a source of infestation needs to be stud- crop shelters (without nets over the open- ied. Conversely, these indigenous plants ings) with which all farmers observed very may have a positive role, acting as auxiliary little tomato fly damage, although major reservoirs (banker plants). Trials conducted attacks can be observed on neighboring in Hawaii demonstrated that implementing open field crops. Although no studies have preventive measures in a production region been conducted to date on this aspect, the reduced populations on their own by over behavior of N. cyanescens may be affected 60% (E. Harris, pers. commun.), which by the transparent plastic film, as it modi- emphasizes the usefulness of these practices fies the light spectrum [33]. This phenome- on the scale of a whole production area, non is already known for other insects in rather than on a single plot or farm. greenhouses, where UV filtering through certain plastic films impairs movement or egg-laying [34]. 4.3. Physical control

Mechanical protection of crops via nets or 4.4. Biotechnical control screens to prevent insect egg-laying is a solution already employed on some crops Biotechnical control is defined as the use of such as cabbage [29], and could be a way stimuli or visual and chemical agents that

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affect the behavior or development of the are attracted by a known parapheromone, target insect [35]. This involves using tech- the cuelure. Comparative tests have been niques that will act on the insects’ behavior conducted with various diffusers: the one via visual or olfactory stimuli, and guide supplied locally by the FDGDON, compris- them to an attractive source, trapping or kill- ing a wooden cube impregnated with cue- ing them, thereby enabling a count (moni- lure and malathion, currently appears to be toring) or elimination (mass trapping). the most useful in terms of effectiveness, Improving biotechnical control must be cost and availability in Reunion. As based on better knowledge of the bio-ecol- malathion in the long term may be with- ogy and behavior of the species. drawn from the market, other active ingre- dients such as spinosad could replace it [36]. 4.4.1. Colored traps In vegetable producing areas, these traps It has long been known that fruit flies are can capture a very high number of males attracted by the color yellow. It is possible (sometimes hundreds per trap per week), to use panels of this color, or bottles of oil which reflects the high population levels. covered with glue, and set them up within However, this method cannot significantly or around the crops (a traditional method reduce populations and damage when the used by some farmers in Reunion Island). traps are set up inside or around a single plot Tests have been conducted on chayote as the adults probably move to an entire area [Sechium edule (Jacq.)], a cucurbit crop (reinfestation via migrations). In addition, locally grown on vines, which demonstrated uncaptured males are capable of fertilizing better attractiveness with yellow bottles put a number of females (polygyny), and the under the vine than those above it. Other females also have the ability to live for sev- more specific colors, as well as the shape of eral months. Hence this method used alone the glue-coated traps, have been tested [4, may be insufficient [37]. This constraint has 5, 16, 17]. These types of visual traps, also been observed with the use of sexual intended rather for tracking the develop- pheromones [38] which may, on the other ment of populations, are not very practical hand, give good results as, for example, with as besides the drawbacks due to the glue we forest moths such as Lymantria dispar (L.) have found a lack of selectivity in the yellow [39], provided that the populations are low traps, as many predator and pollinator insect density and the infested area isolated. species are also attracted. In addition, we Therefore, it would be necessary to apply have not observed a significant population a combined control method to an entire pro- or damage decrease by setting traps in a sin- duction area. A campaign against flies gle plot in our trials. attacking chayote was conducted by the FDGDON using cuelure traps in an isolated 4.4.2. Male Annihilation Technique production area located at an average alti- (MAT) tude of 400 m in the South of the island. After several months of trapping, the quan- A few chemical substances, known as par- tity of trapped B. cucurbitae males had apheromones, have the property of strongly greatly decreased as D. demmerezi was attracting the males of some fruit fly species barely present at this altitude. However, fruit in the same way as sexual pheromones. damage did not decrease and the rearing of Consequently, these products can be used larvae taken from the fruit primarily pro- in trapping systems. Several types of traps, duced D. ciliatus, a species not attracted by based on the “Tephritrap®” used in fruit cuelure. Hence, generalized trapping led to orchards, have been tested locally. These the replacement of an initially dominant were most often dry traps containing a par- species by another less competitive species. apheromone-soaked capsule or plate, with an added vapor action insecticide (dichlor- 4.4.3. Bait Application Technique (BAT) vos, malathion). Fruit flies need water, carbohydrates and Two vegetable fruit fly species present in proteins to ensure their survival, but also Reunion, B. cucurbitae and D. demmerezi, for egg maturation. The foraging behavior

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for these nutrients can be exploited by These experiments in field cages are, attracting the flies with products providing however, fairly remote from the reality of them with these substances. Numerous spot treatments, where small quantities of products containing proteins or yeasts, or products are applied to the leaves in the even plant-derived substances, have been form of drops, which will dry more or less used as attractants worldwide [40–44] used quickly. Hence a new protocol for compar- either in traps or mixed with an insecticide ative tests in large cages has been proposed for spot treatments on crops. using dry traps containing an insecticide plate, a piece of maize leaf mounted on a These attractants can be used with two wet piece of cotton, onto which a drop of methods. First, McPhail-type liquid traps are a given volume of attractant is placed. The used, in which the flies are attracted and results proved to be contradictory depend- drowned. Yet this device attracts few indi- ing on the replicates. Trials have started to viduals compared to the parapheromone this end to explain the variability of the traps and so remains insufficient for signif- responses observed, which appears to be icantly reducing populations, although the related to the position of the traps in the specificity is lower and the attraction applies cage relative to the sun, the time of fly activ- to both sexes. Furthermore, there do not ity, the temperature and the attraction by the always seem to be correlations between the maize leaf, wet piece of cotton and yellow number of individuals trapped and the level color of the insecticide plate. of damage, but we have a lack of data. Nonetheless, these traps are good indicators Field tests conducted in collaboration of the species presence and their changes with several local partners (FDGDON, Plant over time. Protection Service) provided an opportunity for testing a new product, GF 120 (= SYNEIS Spot sprayings, long since successfully APPAT®), a mixture of a food attractant and used in fruit orchards [45], consist of apply- a natural insecticide, spinosad), applied in ing to some plants or plant parts a food spot spraying to the crop or border plants attractant acting as a lure, mixed with an favorable to flies, such as maize. Indeed, insecticide. Several protein or yeast-based studies in Reunion into fly behavior have food attractants were tested in large outdoor demonstrated that the applications would cages with laboratory-reared flies. This type gain effectiveness if applied around the of attractant was tested in liquid form in edges of the plot [18], as it is done in West McPhail-type traps. The products tested Africa [6]. These tests have not, however, (Nulure®, Solbait®, Hymlure®, Corn Steep demonstrated the effectiveness of GF 120 water®, Pinnacle®, Torula® and various under the conditions of Reunion, even if the yeasts including brewing waste derivatives) doses, concentrations or application fre- were all more effective than the Buminal® quency are increased, whereas it appears to control, the only food attractant for fruit flies be effective in other parts of the world [51]. sold in France [46, 47]. However, authoriza- Laboratory tests have confirmed its toxicity tion for their use is classified as minor usage against several fly species [52] and we have in Reunion, which has not yet been defined, observed it for ourselves in large outdoor and they cannot yet be put on the market. cages, as in Mauritius [53]. Furthermore, Improvements in effectiveness by reducing studies on B. cucurbitae have demonstrated the pH or increasing the concentration have that the age of the flies, exposure time and also been observed to a certain degree, but product concentration had an effect on using additives (borax, ammonium acetate) attractiveness and mortality [54]. or using enzymes (papain) had no positive effect [48, 49], unlike the findings with other A hypothesis may be drawn up regarding fruit fly species. Though the methodology this lack of effectiveness in the field. As flies has been gradually refined to eliminate are highly mobile insects, it is highly likely some biases [50], we have not tested the that they are constantly arriving from sur- effectiveness or repellent effect of only a rounding host crops, where populations few insecticides intended for mixing with may be high. Furthermore, we do not know attractants. the remanence of attractants, and their rapid

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breakdown could also explain the phenom- and its installation have been a success [58], enon. It is also possible that the females but the level of parasitism observed in the have time to lay even before being elimi- past few years is still low in crops (< 5%), nated by spot sprayings. However, accord- including on plots without insecticides [4]. ing to manufacturer sources, GF 120 would However, it is possible that the levels be effective in fruit crops when applied to obtained from larvae in the fruit underesti- hundreds of hectares of single crop land, in mate the real parasitism rate because some an environment with few natural areas or lit- larvae could be parasited when they tle wild land. This situation is therefore dif- emerge from the fruit before pupation in the ferent to that in Reunion where vegetable soil. Furthermore, we have not studied the crop plots are piecemeal, and surrounded effectiveness of this parasitoid against by a variety of habitats. Furthermore, tests D. demmerezi and D. ciliatus, although it is conducted in Reunion [50] and the USA known that this hymenopterous insect can [55] have demonstrated that flies with pro- parasite them in the laboratory [56]. The tein-sufficient diets are much less attracted main P. fletcheri reservoir in Reunion by attractants containing protein, such as GF appears to be the wild bitter melon (Mor- 120, for example. Hence it is highly possible modica charantia), which primarily hosts that flies can easily find protein sources in B. cucurbitae [4]. a local context rich in food resources (plant On the other hand, the effectiveness of exudates, excrement, maize pollen, fruits, this species has been demonstrated in etc.). Hawaii provided that pre-reared individuals are released in mass (over 60,000 –1 4.5. Biological control individuals·ha per week) [59], which poses the problem of cost. A complemen- tary technique aimed at increasing parasi- Fruit flies have a number of natural enemies, toid populations consists of putting sting which generally attack the eggs or larvae. fruits in a cage (with larvae therefore partly However, these stages are more or less pro- parasited), the mesh of which enables emer- tected by the fruits hosting them, except gent parasitoids to escape but prevents the when the larvae emerge from the fruit to flies from passing through. This technique pupate in the soil. They can then fall prey used in Hawaii is known as the “augmen- to various predators (including ants) and torium” (E. Harris, pers. commun.). parasitoids. The eggs inserted under the fruit skin can also be parasited fairly easily by A fruit fly egg parasitoid, Fopius arisa- oophagous species, whereas only larvae nus (Sonan) (Hymenoptera: Braconidae), near the edges of the fruit can be reached has been recently imported to the island to by other parasitoids. Adults may also be cap- control Bactrocera zonata, but a study has tured by various organisms (spiders, for demonstrated that it cannot complete its example), but this aspect has still been little cycle on B. cucurbitae and that it develops studied. little on the three other species concerned [60]. Several entomophagous species have been listed across the world, but their effec- In the cases of D. ciliatus, D. demmerezi tiveness is not always sufficient in economic and N. cyanescens, the parasitoids are terms. Only a few species are recognized as much less known, and further research beneficial and have been introduced to var- would need to be conducted in their areas ious countries, and some of them to Reunion of origin, which are assumed to be in Africa in the past few years, but not all are accli- and Madagascar. Some parasitoid species mated or are still at too low a level to have have been recently mentioned on D. ciliatus a useful action [56]. in Egypt [61]. In Reunion, very little data exists on parasitoids of N. cyanescens: the Psyttalia fletcheri (Silvestri) (Hymenop- ones mentioned are Psyttalia near dis- tera: Braconidae) is the most used parasi- tinguenda (Granger) and Ps. insignipennis toid worldwide for controlling B. cucurbitae (Granger), but this parasitism seems to be [57]. Its introduction into Reunion in 1995 occasional [5].

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5. Other control methods not controlled over several years, which presup- used in Reunion poses setting up a production factory. In the case of flies attacking vegetables in Reunion, the techniques and experience are known 5.1. Integrated Pest Management for just one species, B. cucurbitae, and it would be necessary to launch studies to Integrated Pest Management (IPM), devel- develop large-scale rearing of three other oped since the 1970s in the Northern coun- species, especially since mass rearing of tries, has generally aimed to harmonize N. cyanescens and above all of D. ciliatus organic control with rational chemical con- has always been problematic in the labora- trol in a curative approach, with rather dis- tory. There is also the added problem of the appointing results in most situations [62]. females’ mating capacity throughout their Furthermore, there are no insecticides spe- lifetime with several males: for example, the cific to fruit flies. Hence, as with other pests, N. cyanescens females mate nearly every fly control has until now been almost exclu- day [5]. Moreover, following eradication of sively based on chemicals, where the insec- some species in other lands, species dis- ticides used may subsequently end up on placement phenomena through elimination the fruits, in the soil and in the water tables, of the competition have been observed [65]. not to mention the adverse effects on useful Consequently, SIT should be applied simul- fauna (entomophagous species, pollinators, taneously to the three species present on etc.). For example, an experimental tomato Cucurbitaceae in Reunion. Hence, for eco- plot managed without chemical sprayings in nomic reasons and due to the relatively the South of the island exhibited major fruit small crop surface areas concerned, it damage due half to N. cyanescens and half appears unlikely that this method will be to tomato fruitworm noctuid moth Helico- implemented. It could possibly be profitable verpa armigera (Hubner), which does not at a regional level, but not all lands are normally cause damage in Reunion, proba- affected by the same species. bly controlled by broad-spectrum treat- ments applied against N. cyanescens. Finally, we need to take into account all 6. Prospects for implementing of the pests of the crops concerned, since agro-ecological management of their overall management may be difficult in vegetable fruit flies in Reunion some cases following the cessation of broad-spectrum insecticide applications. 6.1. Approach and references The structure of landscape as a mosaic of 5.2. Sterile Insect Technique habitats affects the spatio-temporal dynamic of insect populations. Landscape manage- Also known as genetic control, the principle ment may contribute to maintaining insect of the Sterile Insect Technique (SIT) consists populations at non-harmful levels, by pro- of releasing very great quantities of males moting faunistic balances and preserving pre-sterilized by ionizing rays. They then biodiversity. This approach is based on compete with the wild males and mate with agro-ecological pest management [66] and the females, which will lay sterile eggs. This can be applied in particular in the form of method, which may form part of IPM, does, management of their habitats or those of however, assume that the sterile males are their natural enemies and of pollinators on much greater in number than the wild males expanded time, space and management and that their fitness for mating is unaltered. scales [67]. Enhancement of beneficial fauna This technique has completely eradicated may be achieved through increasing plant species such as B. cucurbitae on some diversity, whether cultivated (rotations, Pacific islands [63, 64]. However, it poses mosaics, intercropping, etc.) or uncultivated several drawbacks, particularly in the con- (borders, hedges, fallows, natural environ- text of Reunion. Firstly, the mass rearing of ments, etc.). This biodiversity also ensures millions of individuals would need to be better resilience of agro-systems [68].

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Planting service plants around plots has ble fly damage in horticultural systems; a several objectives depending on the spe- certain skepticism on the part of some pro- cies: a trap or repellent effect for pests tagonists, primarily the farmers, already dis- (“push-pull”), or acting as a reservoir for appointed by previous proposals; a common, beneficials (functional biodiversity). Regard- shared and conscious desire on the part of ing trap plants, the initial observations seem stakeholders in the project [76]. Seven years to indicate that the wild bitter melon (Mor- of findings are now available to evaluate its modica charantia) is more attractive to effectiveness,bothintechnicalterms[72,77, B. cucurbitae females than the zucchini, 78]andeconomicterms[79].Fouryearsafter which therefore appears to be protected, its initiation, the profits generated exceeded but the opposite clearly applies to D. cilia- the annual costs of its application. This pro- tus. Similarly, with traps placed in large field gram is currently considered in the United cages, we have found that bitter melon States as a model for success in IPM, and one leaves were clearly more attractive to of the keys to this success is due to the effi- B. cucurbitae females than the same weight cient coordination between the different of zucchini leaves. The importance of this protagonists in the program [80]. Further- sub-indigenous plant as a parasitoid reser- more, it has been subject to adaptations that voir, however, is still limited as levels of para- have been successful in other countries, sitism remain low (< 10%) (P. Ryckewaert, such as Japan [81] and Taiwan [82]. Other unpublished). initiatives are being launched based on this model, such as on Mauritius, with the support Observations have shown that vegetable of the International Atomic Energy Agency. fruit flies could gather on certain field border plants on which they feed [69], mate [4] and rest [18]. Hence grasses such as maize, sor- 6.2. Research actions implemented ghum or sugar cane often act as shelter in fly bio-ecology plants for these flies. Maize seems particu- Among the research actions to be devel- larly favorable to these insects, which prob- oped, those relating to acquisition of knowl- ably find water, exudates and pollen [4, 70], edge of fly bio-ecology are the first to or even aphid honeydew or other nutrients. intensify. While B. cucurbitae is a fly whose Therefore, it appears more logical to place biology has been well studied in the world, traps or apply spot treatments to this type the same does not apply to the three other of plant rather than to the crop [51, 71, 72]. species found in Reunion (D. ciliatus, D. dem- Finally, these plants may also promote merezi and N. cyanescens). The aim of the development of beneficials, or host them. studies should be to establish the main bio- The approach initiated in Reunion is con- ecological characteristics of these flies, and sistent with the agro-ecological approach will cover the circadian rhythm, particularly described above, the conceptual bases of the flies’ movements between cultivated plants which were summarized by Deguine et al. (Cucurbitaceae, Solanaceae) and uncultivated [73]. It is also completely consistent with the plants (primarily borders). Similarly, studies guidelines adopted in some countries for into the main natural enemies need to be vegetable fruit fly control based on a large- conducted, both on predators (ants, ground scale management approach (Area-Wide beetles, rove beetles) and on parasitoids Pest Management) [74]. In Hawaii, a pro- (including Psyttalia fletcheri). Tri-trophic gram of this type was initiated in 2000 on interactions (pests, natural enemies, plants) several hundred hectares, on several crops will be a key object for study in this approach. (cucurbits, papayas, etc.) and on several fruit fly species including B. cucurbitae,a 6.3. Research actions into genetic species present in Reunion [75]. Besides the structure of populations fact that Hawaii and Reunion exhibit numer- ous similarities, particularly in terms of agri- A work program is being initiated at the culture and climate, the situation on this InternationalCenterforAgriculturalResearch island in 2008 may be compared to that of for Development (CIRAD, Reunion) to ana- Hawaii in 2000: significant fruit and vegeta- lyze via micro-satellite markers the genetic

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variability of vegetable fruit fly populations, live for several months and move around by the following parameters: host plants easily, the presence of high population lev- (wild vs. cultivated), altitude gradient [(0 to els probably resulting from an imbalance, 1200) m] and seasonal temperatures (win- the presence of scattered plots, and the dif- ter-summer). This work will enable one to ficulty in implementing preventive meas- specify the importance of reservoir plants ures may explain the failures observed up and shelter plants in the reproduction of until now. fruit flies, and gain a better knowledge of Fly population control should be imple- dispersal, seasonal migration and practical mented at production area level, with col- details of the winter season transition. The lective and coordinated resources, to year 2008 was devoted to starting sampling promote a new agro-ecological balance on 25 sites (B. cucurbitae and D. demme- centered on the role of functional plants, rezi), tool construction (D. demmerezi, habitat management and development of D. ciliatus and N. cyanescens) and develop- natural beneficials, on a landscape scale. ing DNA extraction. The program will con- Other alternative methods (MAT, BAT, etc.) tinue these preliminary activities on the four may be used as complements. These envi- fly species concerned. ronmentally friendly techniques can there- fore be included under Organic Agriculture 6.4. Design of an agro-ecological and IPM approaches. management scheme for vegetable fruit flies Thereafter, it will be a matter of developing Acknowledgements and evaluating a technical management package for fly populations, based on an We would like to thank the Regional Council agro-ecological approach. The design of of Reunion for its assistance in enabling us this package is based on existing foreign to successfully conduct past and future experience, especially from Hawaii, while research into vegetable fruit flies. We also taking into account the particularities of express our thanks to the various collabo- Reunion (socio-economic characteristics of rators in the studies, and to the project part- agriculture, biological characteristics of the ners (FDGDON, Plant Protection Service). flies present, etc.). The technical consist- ency of this package is an essential prelim- inary step. The foundation of the package References is based on the following techniques: mon- itoring, trap plants and using new products [1] Anon., Mémento statistique agricole. La (assisted push-pull), the Male Annihilation Réunion (résultats 2006), Agreste, Dir. Agric. Technique (MAT), biological control and Pêche, 2007. agro-ecological practices. [2] Ryckewaert P., Les insectes et acariens des cultures maraîchères dans les DOM-TOM : situation et perspectives, Phytoma 562 7. Conclusions (2003) 26–31. [3] Etienne J., Étude systématique, faunistique The control methods tested hitherto in et écologique des Téphritides de la Réunion, Reunion against vegetable fruit flies have École Prat. Hautes Études, Thèse, Paris, proven to be greatly insufficient in limiting France, 1982, 100 p. damage to the crops concerned. The [4] Vayssières J.-F., Les relations insectes-plan- absence of parapheromones for all species, tes chez les Dacini (Diptera : Tephritidae) genuinely effective food attractants which ravageurs des Cucurbitaceae à La Réunion, are approved and have sufficiently long- Cirad-Flhor, Mus. Natl. Hist. Nat., Univ. lasting action, the existence of short crop Créteil, Thesis, Paris, France, 1999, 241 p. cycles repeated all year round without no- [5] Brévault T., Mécanismes de localisation de host plant zones, the ability of the flies to l'hôte chez la mouche de la tomate,

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Neoceratitis cyanescens (Bezzi) (Diptera : [19] Ranganath H.R., Veenakumari K., Tomato Tephritidae), Ensam, Thesis, Cirad-Flhor, (Lycopersicon esculentum Miller): A con- Montpellier, France, 1999, 139 p. firmed host of the melon fly Bactrocera (Zeu- godacus) cucurbitae Coquillett, Insect [6] Vayssières J.-F., Rey J.-Y., Traoré L., Distri- Environ. 2 (1) (1996) 3. bution and host plants of Bactrocera cucur- bitae in West and Central Africa, Fruits 62 (6) [20] Fontem D.A., Gumedzoe M.Y.D., Nono W.R., (2007) 391–396. Biological constraints in tomato production in the western highlands of Cameroon, [7] Dhillon M.K., Singh R., Naresh J.S., Sharma Tropicultura 16 (17) (1999) 89–92. H.C., The melon fruit fly, Bactrocera cucurbi- tae: A review of its biology and management, [21] Vargas R.I., Stark J.D., Nishida T., Population J. Insect Sci. 5 (2005) 40. dynamics, habitat preference, and seasonal distribution patterns of Oriental fruit fly and [8] Anon., Dacus ciliatus. Distribution map, melon fly (Diptera: Tephritidae) in an agricul- CAB-Int., U.K., 2002. tural area, Environ. Entomol. 19 (6) (1990) [9] Orian A.J., Moutia L.A., Fruit flies of eco- 1820–1828. nomic importance in Mauritius, Rev. Agric. [22] Vayssières J.-F., Carel Y., Les Dacini Sucr. île Maurice 39 (1960) 142–150. (Diptera : Tephritidae) inféodés aux Cucur- [10] Lavergne R., Fleurs de Bourbon, Tome IV, bitaceae à La Réunion : gamme de plantes– Cazal (Eds), Saint Denis, La Réunion, hôtes et stades phénologiques préférentiels France, 288 p. des fruits au moment de la piqûre pour des espèces cultivées, Ann. Soc. Entomol. Fr. 35 [11] Brévault T., Datasheet on alien invasive spe- (1999) 197–202. cies, Neoceratitis cyanescens Bezzi., CABI Crop Prot. Compend., U.K., 2003. [23] Vayssières J.-F, Carel Y., Coubès M., Duyck P.-F., Development of immature stages and [12] Brévault T., Quilici S., Sexual attraction, male comparative demography of two cucurbit- courtship and female remating in the tomato attacking fruit flies in Reunion Island, Bac- fruit fly, Neoceratitis cyanescens, J. Insect trocera cucurbitae and Dacus ciliatus (Dip- Behav. 21 (2008) 366–374. tera: Tephritidae), Environ. Entomol. 37 (2) [13] Brévault T., Quilici S., Relationships between (2008) 307–314. temperature, development and survival of [24] Vargas R.I., Walsh W.A., Kanehisha D., Stark different life stages of the tomato fruit fly, J.D., Nishida T. , Comparative demography Neoceratitis cyanescens, Entomol. Exp. of three Hawaiian fruit fly (Diptera: Tephriti- Appl. 94 (2000) 25–30. dae) at alternating temperatures, Ann. Ento- [14] Brévault T., Duyck P.-F., Quilici S., Life-his- mol. Soc. Am. 93 (1) (2000) 75–81. tory strategy of an oligophagous tephritid, [25] Vayssières J.-F., Dal F., Responses of the Neoceratitis cyanescens, Ecol. Entomol. 33 Ethiopian fruit fly, Dacus ciliatus Loew (Dip- (2008) 529–536. tera: Tephritidae), to coloured rectangles, [15] Brévault T., Quilici S., Factors affecting spheres and ovoids, Proc. 6th Int. Fruit Fly behavioural responses to visual stimuli in the Symp., 6–10 May 2002, Stellenbosch, S. tomato fruit fly, Neoceratitis cyanescens, Afr., pp. 111–116. Physiol. Entomol. 24 (1999) 333–338. [26] Dong Y.J., Cheng L.L., Chen C.C., Labora- [16] Brévault T., Quilici S., Visual response of the tory bioassay of 10 insecticides against the tomato fruit fly, Neoceratitis cyanescens,to melon fly (Bactrocera cucurbitae), J. Agric. colored fruit models, Entomol. Exp. Appl. Res. Chin. 51 (4) (2002) 66–72. 125 (2007) 45–54. [27] Hsu J.C., Feng H.T., Susceptibility of melon [17] Brévault T., Quilici S., Influence of habitat pat- fly (Bactrocera cucurbitae) and oriental fruit tern on visual orientation during host finding fly (B. dorsalis) to insecticides in Taiwan, in the tomato fruit fly, Neoceratitis cyanes- Plant Prot. Bull. (Taichung) 44 (4) (2002) 303– cens, Bull. Entomol. Res. 97 (2007) 1–6. 315. [18] Brévault T., Quilici S., Diel patterns of repro- [28] Liquido N.J., Fruit on the ground as a reser- ductive activities in the tomato fruit fly, voir of resident melon fly (Diptera: Tephriti- Neoceratitis cyanescens, Physiol. Entomol. dae) populations in papaya orchards, 25 (3) (2000) 233–241. Environ. Entomol. 20 (2) (1991) 620–625.

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[29] Martin T., Assogba-Komlan F., Houndete T., Control of low-density gypsy moth (Leidop- Hougard J.M., Chandre F., Efficacy of mos- tera: Lymantriidae) populations by mating quito netting for sustainable small holders’ disruption with pheromone, J. Chem. Ecol. cabbage production in Africa, J. Econ. Ento- 22 (1996) 1255–1272. mol. 99 (2006) 450–454. [40] Qureshi Z.A., Hussain T., Efficacy of Nu-lure [30] Froissart R., Gerard M., Vaissiere B.E., Inte- and protein hydrolysate baits in controlling grated production of out of season canta- Ethiopian melon fly Dacus ciliatus, Pak. J. loupes in West Africa, Fruits 50 (5) (1995) Agric. Res. 13 (2) (1992) 150–154. 359–374. [41] Akhtaruzzaman M., Zinnatul A., Ali S.M.M., [31] Vaissière B.E., Froissart R., Pest manage- Efficacy of different bait sprays for suppress- ment and pollination of cantaloupes grown ing fruit fly on cucumber, Bull. Inst. Trop. under spunbonded row covers in West Agric. (Kyushu Univ.) 23 (2000) 15–26. Africa, J. Hortic. Sci. 71 (5) (1996) 755–766. [42] Satpathy S., Rai S., Luring ability of indige- [32] Truong H.X., Rapusas H.R., Valdez E.M., nous food baits for fruit fly, Bactrocera Marquez L.V., Casimero M.C., Community- cucurbitae (Coq.), J. Entomol. Res. 26 (3) based IPM [Integrated Pest Management] in (2002) 249–252. rice-bitter gourd cropping system., Philipp. Entomol. 17 (2) (2003) 183. [43] Jiji T., Napolean A., Stonehouse J., Verghese A., Efficient food baits for trapping fruit flies, [33] Langlais C., Ryckewaert P., Guide to shel- Insect Environ. 9 (3) (2003) 143–144. tered vegetable cultivation in the humid trop- ics, Cirad-Flhor, Montpellier, France, 2001, [44] Barry J.D., Miller N.W., Pinero J.C., Tuttle A., 92 p. Mau R. F.L., Vargas R.I., Effectiveness of pro- tein baits on melon fly and oriental fruit fly [34] Cheng C.H., Ho S.C., Evaluation of the (Diptera: Tephritidae): attraction and feeding, effects of ultraviolet-absorbing film on the J. Econ. Entomol. 4 (2006) 1161–1167. population of insect pests and yield of musk- melon, Plant Prot. Bull. (Taipei) 39 (4) (1997) [45] Robinson A.S., Hooper G., Fruit flies, their 289–304. biology, natural enemies and control, Else- vier, Amst., Neth., 1989. [35] Boller E.F., Biotechnical methods for the man- agement of fruit fly populations, in: Cavalloro [46] Fabre F., Ryckewaert P., Duyck P.F., Chiroleu R. (Ed.), Fruit flies of economic importance F., Quilici, S., Comparison of the efficacy of 82, Proc. CEC/IOBC Int. Symp., Athens, different food attractants and their concen- Greece, 1983, pp. 342–351. tration for melon fly (Diptera: Tephritidae), J. Econ. Entomol. 96 (1) (2003) 231–238. [36] Vargas R.I., Miller N.W., Stark J.D., Field tri- als of spinosad as a replacement for naled, [47] Duyck P.F., Quilici S., Fabre F., Ryckewaert DDVP, and malathion in methyl eugenol and P., Comparison and optimization of the effi- cue-lure bucket traps to attract and kill male cacy of different food attractants for both oriental fruit flies and melon flies (Diptera: sexes of the melon fly, Bactrocera cucurbi- Tephritidae) in Hawaii, J. Econ. Entomol. 96 tae (Coquillett) (Diptera:Tephritidae), Proc. (6) (2003) 1780–1785. 6th Int. Symp. Fruit flies of economic impor- [37] Matsui M., Nakamori H., Kohama T., Nag- tance, Stellenbosch, S. Afr., 2002 May 6–10, amine Y., The effect of male annihilation on a 2004, pp. 351–354. population of wild melon flies, Dacus cucur- [48] Duyck P.F., Rousse P., Ryckewaert P., Fabre bitae Coquillett (Diptera: Tephritidae) in F., Quilici S., Influence of adding borax and Northern Okinawa, Jpn. J. Appl. Entomol. modifying pH on effectiveness of food Zool. 34 (4) (1990) 315–317. attractants for melon fly (Diptera: Tephriti- [38] Royer L., Delisle J., Utilisation des pièges à dae), J. Econ. Entomol. 97 (3) (2004) 1137– phéromone sexuelle dans la gestion des 1141. ravageurs, in: Regnault-Roger C. (Ed.), [49] Rousse P., Duyck P.F., Quilici S., Ryckewaert Enjeux phytosanitaires pour l'agriculture et P., Development and optimization of food l'environnement, Lavoisier, Paris, France, attractants for the melon fly Bactrocera 2005. cucurbitae (Coquillet) (Diptera: Tephritidae), [39] Leonhardt B.A., Mastro V.C., Leonard D.S., Rev. Agric. Sucr. île Maurice 83 (2/3) (2004) McLane W., Reardon R.C., Thorpe K.W., 43–49.

Fruits, vol. 65 (2) 127 P. Ryckewaert et al.

[50] Rousse P., Duyck P.F., Quilici S., Ryckewaert [59] Vargas R.I., Long J., Miller N.W., Delate K., P., Adjustment of field cage methodology for Jackson C.G., Uchida G.K., Bautista R.C., testing food attractants for fruit flies (Diptera: Harris E.J., Releases of Psyttalia fletcheri Tephritidae), Ann. Entomol. Soc. Am. 98 (3) (Hymenoptera: Braconidae) and sterile flies (2005) 402–408. to suppress melon fly (Diptera: Tephritidae) in Hawaii, J. Econ. Entomol. 97 (5) (2004) [51] Prokopy R.J., Miller N.W., Pinero J.C., Barry 1531–1539. J.D., Tran L.C., Oride L., Vargas R., Effective- ness of GF-120 fruit fly bait spray applied to [60] Rousse P., Gourdon F., Quilici S., Host spe- border area plants for control of melon flies cificity of the egg pupal parasitoid Fopius (Diptera: Tephritidae), J. Econ. Entomol. 96 arisanus (Hymenoptera: Braconidae) in La (5) (2003) 1485–1493. Reunion, Biol. Control 37 (3) (2006) 284–290. [52] Stark J., Vargas R., Miller N., Toxicity of [61] Fetoh B.E.A., Recent record of parasitoid spinosad in protein bait to three economi- species of cucurbit fruit fly, Dacus ciliatus cally important tephritid fruit fly species (Dip- (Loew) (Diptera: Tephritidae) in Egypt, Egypt, tera: Tephritidae) and their parasitoids J. Biol. Pest Control 13 (1/2) (2003) 127. (Hymenoptera: Braconidae), J. Econ. Ento- mol. 97 (3) (2004) 911–915. [62] Ehler L.E., Integrated Pest Management (IPM): definition, historical development and [53] Sookar P., Seewooruthun S.I., Khayratee F., implementation, and the other IPM, Pest Assessment of protein baits for the monitor- Manag. Sci. 62 (2006) 787–789. ing and control of fruit flies (Diptera: Tephriti- dae), Rev. Agric. Sucr. Île Maurice 80 (2001) [63] Sekiguchi Y., Eradication of the melon fly 287–294. (Dacus cucurbitae) from Amani Islands of Japan, Q. Newsl. Asia Pac. Plant Prot. [54] Revis H.C., Miller N.W., Vargas R., Effects of Comm. 33 (2) (1990) 19–20. aging and dilution on attraction and toxicity of GF-120 fruit fly bait spray for melon fly [64] Ito Y., Kakinohana H., Yamagishi M., control in Hawaii, J. Econ. Entomol. 97 (5) Kohama T., Eradication of the melon fly, Bac- (2004) 1659–1665. trocera cucurbitae, from Okinawa, Japan, by means of the sterile insect technique, with [55] Miller N., Vargas R., Prokopy R., Mackey B., special emphasis on the role of basic stud- State-dependent attractiveness of protein ies, J. Asia Pac. Entomol. 6 (2) (2003) 119– bait and host fruit odor to Bactrocera cucur- 129. bitae (Diptera: Tephritidae) females, Ann. Entomol. Soc. Am. 97 (5) (2004) 1063–1068. [65] Ito Y., Effect of eradication of the Oriental fruit fly, Bactrocera dorsalis, on the popula- [56] Hurtrel B., Biologie du développement et tion density of the melon fly, Bactrocera écologie comportementale de deux parasi- cucurbitae, in the Ryukyu Archipelago, esti- toïdes de mouches des fruits à la Réunion, mated from the number of male flies cap- Univ. Rennes, Thesis, Rennes, France, 2000, tured by attractant traps, Appl. Entomol. 157 p. Zool. 40 (4) (2005) 625–630. [57] Bautista R.C., Harris E.J., Vargas R.I., Jang [66] Nicholls C.I., Altieri M.A., Agroecological E.B., Parasitization of melon fly (Diptera: bases of ecological engineering for pest Tephritidae) by Fopius arisanus and Psyttalia management, in: Gurr G.M., Wratten S.D., fletcheri (Hymenoptera: Braconidae) and the Altieri M.A. (Eds.), Ecological engineering for effect of fruit substrates on host preference pest management. Advances in habitat by parasitoids, Biol. Control 30 (2) (2004) manipulation for arthropods, CSIRO, Colling- 156–164. wood, Aust., CABI, Wallingford, U.K., 2004, [58] Quilici S., Hurtrel B., Messing R.H., pp. 33–54. Montagneux B., Barbet A., Gourdon F., [67] Ferron P., Deguine J.-P., Crop protection, Malvolti A., Simon A., Successful acclimati- biological control, habitat management and zation of Psyttalia fletcheri (Braconidae: Opi- integrated farming, Agron. Sustain. Dev. 25 inae) for biological control of the melon fly, (2005) 1–8. Bactrocera cucurbitae (Diptera: Tephritidae), on Reunion Island, Proc. 6th Int. Symp. Fruit [68] Altieri M.A., The ecological role of biodiver- flies of economic importance, Stellenbosch, sity in agroecosystems, Agric. Ecosyst. Envi- S. Afr., 6–10 May 2002, pp. 457–459. ron. 74 (1999) 19–31.

128 Fruits, vol. 65 (2) Fruit flies on vegetable crops in Reunion Island

[69] Nishida T., Bess H.A., Studies on the ecol- [77] Jang E.B., Klungness L.M., McQuate G.T., ogy and control of the melon fly Dacus Extension of the use of augmentoria for san- (Strumeta) cucurbitae Coquillett (Diptera: itation in a cropping system susceptible to Tephritidae), Hawaii Agric. Exp. Stn. Tech. the alien tephritid fruit flies (Diptera: Tephriti- Bull. 84 (1957) 1–44. dae) in Hawaii, J. Appl. Sci. Environ. Manag. [70] McQuate G.T., Assessment of corn pollen as 11 (2007) 239–248. a food source for two tephritid fruit fly spe- [78] McQuate G., Assessment of border bait cies, Environ. Entomol. 32 (1) (2003) 141– sprays and male annihilation for Bactrocera 150. spp. suppression in papaya orchards, In: [71] Prokopy R.J., Miller N.W., Pinero J.C., Oride Proc. 6th Ann. Meet. Rev. Hawaii fruit fly L., Chaney N., Revis H., Vargas R., How area-wide management programme, April effective is GF-120 fruit fly bait spray applied 16–19, 2007, Waikoloa, Hawaii, U. S. A. to border area sorghum plants for control of melon flies (Diptera: Tephritidae), Fla. Ento- [79] McGregor A.M., An economic evaluation of mol. 87 (3) (2004) 354–360. the Hawaii fruit fly area-wide pest manage- ment program, Trade Dev. Off., U. S. A., [72] McQuate G., Vargas R., Assessment of 2007, 81 p. attractiveness of plants as roosting sites for the melon fly, Bactrocera cucurbitae, and [80] Mau R.F.L., Jang E.B., Vargas R.I., The oriental fruit fly, Bactrocera dorsalis, J. Insect Hawaii area-wide fruit fly pest management Sci. 7 (2007) 57. programme: Influence of partnerships and a good education programme, in: Vreysen [73] Deguine J.-P., Ferron P., Russell D., Crop M.J.B., Robinson A.S., Hendrichs J. (Eds.), protection: from agrochemistry to agroecol- Area-wide control of insect pests. From ogy, Sci. Publ., Enfield, NH, U.S.A., 2009. research to field implementation, Springer, [74] Tan K.H., Area-wide control of fruit flies and 2007. other insect pests, CABI, Wallingford, U. K., 2000. [81] Koyama J., Kahinohana H., Miyatake T., Eradication of the melon fly, Bactrocera [75] Vargas R.I., Area-wide pest management for cucurbitae, in Japan: Importance of behav- exotic fruit flies in Hawaii, in: FLC awards ior, ecology, genetics, and evolution, Ann. program, FLC-TPWG Natl. Meet., May 2004, Rev. Entomol. 49 (2004) 331–349. San Diego, Calif., U. S. A., pp. 15–16. [76] Vargas R.I., Highlights and milestones of the [82] Huang T.C., Expansion of the area wide fruit Hawaii area-wide fruit fly pest management fly management program in Taiwan. Some program, in: Proc. 6th Ann. Meet. Rev. contributions from Hawaii, in: Proc. 6th Ann. Hawaii fruit fly area-wide management pro- Meet. Rev. Hawaii fruit fly area-wide man- gramme, April 16–19, 2007, Waikoloa, agement programme, April 16–19, 2007, Hawaii, U. S. A. Waikoloa, Hawaii, U. S. A.

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Las moscas de las frutas (Diptera: Tephritidae) en verduras en la Reunión (océano Índico): estado de los conocimientos, métodos de control y perspectivas de gestión. Resumen –– Importancia de las moscas de las frutas en cultivos de hortalizas. Los cultivos de hortalizas ocupan una posición determinante en la producción agrícola en la Reunión (océano Índico). No obstante, existen numerosas plagas así como enfermedades, que suponen una amenaza para la rentabilidad de este sector agrícola. Las moscas de las frutas (Diptera: Tephritidae) se clasifican entre las plagas principales de las solanáceas y de las cucurbitáceas (pepino, calabacín, melón, etc.). Se observaron frecuentemente pérdidas de cerca del 80 % de las cosechas de tomate y del 100 % de cucurbitáceas. Inventario y distribución. Cuatro especies de moscas de las frutas pertenecientes a la familia de los Tephritidae provocan importantes daños en los cultivos de verduras en la Reunión: Bactrocera cucurbitae (Coquillet), Dacus ciliatus Loew y D. demmerezi (Bezzi) en los cucurbitáceos, y Neoceratitis cyanescens (Bezzi) en las solanáceas (principalmente los tomates). La distribución de cada uno de ellos está presentada. Biología y comportamiento. En la Reunión en los años 1990 se realizaron ciertos estudios sobre la biología así como sobre el comportamiento de las cuatro moscas de las frutas. Se resumieron sus principales características biológicas. Métodos de control de las poblaciones empleadas en la Reunión. Se exponen diversos métodos empleados actualmente en la Reunión contra estas moscas de las frutas: lucha química, medidas preventivas (saneamiento), control físico, control biotécnico [color de las trampas, técnica de anihilación del macho (MAT), así como técnica de empleo de cebos (BAT)], y lucha biológica. En la Reunión no se emplean otros métodos de lucha como la lucha antiparasitaria integrada o la técnica del insecto estéril. Perspectivas de puesta en marcha de la gestión agro-ecológica de las moscas de las frutas en cultivo de hortaliza en la Reunión. Esta parte presenta tanto las acciones de investigación puestas en marcha en bio-ecología de la mosca, como las acciones de investigación en la estructura genética de las poblaciones, o incluso la concepción de un sistema de gestión agro-ecológico para las moscas de las frutas de las verduras. Conclusiones. Los métodos empleados independientemente unos de otros no demostraron su eficacia para el control de las poblaciones de las Tephritidae. Se necesita un acercamiento más íntegro, que tome en cuenta la escala del paisaje y de su mosaico de hábitats, en concreto las plantas espontáneas, cuyo papel debe considerarse en el marco de una gestión agro-ecológica de las poblaciones de estas plagas.

Reunión / hortalizas (plantas) / Tephritidae / Bactrocera cucurbitae / Dacus ciliatus / Dacus demmerezi / Neoceratitis cyanescens / control de plagas / métodos de control

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