Neoceratitis cyanescens (tomato fruit fly)

Summary of Invasiveness

Top of pageOriginating in Madagascar, N. cyanescens has been introduced to Mauritius, Réunion and Mayotte islands. It is oligophagous on both wild and cultivated Solanaceae species, particularly tomato, where attacks on fruit may cause severe damage to yield and quality of production. Once introduced, populations of N. cyanescens have the potential to build up rapidly in habitats (smallholdings, gardens and village communities) where fruiting wild and cultivated hosts are present throughout the year.

Notes on Taxonomy and Nomenclature

Top of pageN. cyanescens is classified in the family Tephritidae, subfamily Dacinae and tribe Ceratitidini, which includes other genera such as Ceratitis and Trirhithrum. This species was successively described under different names: Perilampsis bourbonica, and Pardalaspis cyanescens, then Trirhithromyia cyanescens (White and Elson-Harris, 1992). The genus Trirhithromyia Hendel, including five African species, was originally described as a subgenus of Ceratitis, before being considered as a distinct genus by Hancock (1984). More recently, Hancock and White (1997) transferred this species to the genus Neoceratitis Hendel, whose host plants belong to the Solanaceae family.

Description

Top of pageTephritidae adults are characterized by the abrupt bend in the subcostal vein (approximately right-angled); and this vein weakens before reaching the costal vein. Many species have wings distinctively patterned with bands or spots, which may be yellow, brown or black. The females usually have a prominent piercing ovipositor, which can penetrate plant tissues. The adults of the tomato fly are easily recognised by the characteristic pattern of brown bands on their wings and the posterior half of the scutellum, which is entirely black. The eggs are white and elongated, slightly curved and approximately 1 mm long. The yellowish larva is a maggot: its slender anterior part has blackish mouth-hooks, whereas the posterior part ends bluntly. At the end of development, it reaches approximately 7-8 mm long. The brown puparium is barrel-shaped and is 4-5 mm long (Quilici and Brévault, 1999). For more details, see Carrol et al. (2002).

Distribution

Top of pageThis major pest of tomato crops occurs throughout the Indian Ocean region and is recorded in Madagascar, Mauritius, Réunion and Mayotte island (CABI/EPPO, 2004). A record for the Comoros islands (OEPP/CABI, 1997) requires confirmation (CABI/EPPO, 2004) and although OEPP/CABI (1997) mention its presence in the Seychelles, this is not listed in White et al. (2000) and is not included in the mapped distribution of CABI/EPPO (2004).

History of Introduction and Spread

Top of pageN. cyanescens was described in 1923 from Madagascar where it is probably indigenous. This species was introduced to Réunion island then to Mauritius where damage was first recorded in 1951 and 1958, respectively (Orian and Moutia, 1960; White et al., 2000). Although it is probably much older, its presence in Mayotte was apparently first reported in 1992 (Bordat, 1992).

Risk of Introduction

Top of pageIn Réunion island, at least six species of fruit flies were accidentally introduced. They entered the island via two unpredictable possible pathways: on infested plant material and produce, or by wind dispersal of the adults (particularly during cyclones). The introduction of plant material has probably been the main way for tephritids to enter Réunion island. Inspection and disinfection of the fruits could be carried out to prevent such introductions. N. cyanescens is already listed as a quarantine pest for Europe (OEPP/CABI, 1997).

Habitat

Top of pageIn Réunion island, the distribution of the tomato fly extends from sea level up to an altitude of 1500 m, depending on the availability of host-plants (Etienne, 1972, 1982). The large distribution area of wild and cultivated host plants in the island, up to an altitude of 1500 m, as well as their abundant and almost continuous fruiting, offer favourable conditions for the fly.

The distribution pattern of the flies in different habitats (host and non-host plants) shows temporal, physiological and sexual differences. The mature females were observed to frequent host plants mainly in the late afternoon. By contrast, immature females prefer to rest on non-host plants throughout the day. The males frequent non-host plants, but some are observed on host fruit in the early morning (Brévault and Quilici, 2000a).

Hosts/Species Affected

Top of pageN. cyanescens is oligophagous and attacks host-plants within the Solanaceae family. Réunion island probably harbours some 20 species of Solanaceae (Lavergne, 1981). The bugweed (Solanum mauritianum) constitutes the main host plant of N. cyanescens in Réunion island (Etienne, 1982). This invasive plant is mostly found between 0 and 1500 m altitude, and flowers and bears fruit all year long. Its berries also constitute one of the food resources of other polyphagous fruit fly species such as Ceratitis rosa and Ceratitis capitata. The flowers, which strongly resemble potato flowers, are grouped in a corymb and have a lilac corolla with an inserted white star. Mature berries are yellow-orange, and olive-sized (Lavergne, 1981).

Growth Stages

Top of pageFruiting stage

Symptoms

Top of pageGreen fruit at an early stage (from 10 to 24 days after flowering) are the most susceptible to tomato fruit fly attack (Brévault, 1999). Symptoms are characterized by a discoloration on the fruit surface, around the oviposition sting. By transparency, the egg emission may be observed under the fruit skin. Further feeding of the larvae inside the fruit and exit holes of the larvae enhance the rotting process of the fruit.

Biology and Ecology

Top of page Physiology and Phenology

The Indian Ocean region provides favourable ecological requirements for N. cyanescens development and survival. In both Réunion and Madagascar, the high climatic diversity, as a function of altitude range and season, offers continuous food availability for larval development (fruiting stage) with wild and cultivated host plants throughout the year.

Reproductive Biology

Mating begins on the second day following adult emergence (Etienne, 1973; Brévault, 1999; Quilici and Brévault, 1999). The females are attracted by a male pheromone emitted during courtship behaviour (Brévault, 1999; Quilici et al., 2000). The females show a strong daily propensity to engage in mating activity throughout their life. This activity is initiated daily in the early morning on surrounding non-host plants and lasts at least 3 hours (Brévault and Quilici, 2000a). After a 6-day period to complete egg maturation, egg-laying activities begin with a circadian rhythm presenting a peak in the late afternoon (Brévault and Quilici, 2000a). Egg-laying behaviour begins with a typical exploration of the fruit surface with the proboscis, sometimes accompanied by a jerky vibration of the wings. As soon as a favourable site is detected, the female turns back, latches on to the fruit and attempts to perforate the epidermis of the fruit with her ovipositor, most frequently positioned perpendicular to the fruit surface. On tomato, this process is realised rather clumsily because of the slippery structure of the epidermis. Once the epidermis is punctured, the female digs a cavity that will receive the eggs with her ovipositor. Egg-laying stricto sensu begins as soon as the female stops moving. More than eight times out of ten, egg clutches are localised in the inferior half of the tomato fruit (two to ten eggs). The size of the egg clutches may vary according to the size and availability of the substrate. A peak of fecundity is observed between 9 and 17 days after female emergence and the net fecundity reaches 180 eggs (Brévault, 1999). In a choice situation, the female tomato fly preferentially lays her eggs in unripe fruit. When the larvae reach maturity, they leave the fruit to complete the pupal stage in the soil.

Environmental Requirements

Temperature and availability of hosts appear to be the most important factors that influence the distribution and demography of fly populations, by affecting survival, developmental rates of different life stages and fecundity of females. The development and survival of N. cyanescens females from egg to complete ovarian maturity were studied as a prerequisite to understand temporal and geographical patterns of fruit fly occurrence (Brévault and Quilici, 2000b). The fastest development of pre-imaginal instars is recorded at 30°C (22 days) and the slowest at 15°C (98 days). At 25°C, egg hatching occurs after 3 days of incubation in the fruit, whereas larval and pupal developments last for 9 and 14 days, respectively. On the whole, 432 degree-days are required to complete the entire development. Lower temperature thresholds are 11.4, 11.9, 10.0, and 11.1°C for egg, larval, and pupal stages, and ovarian maturation, respectively. The highest mortality was recorded for pupae at 35°C, where no adults emerged. Within the range 15 to 35 °C, except for the egg and larval stages at 15°C, both the lowest and highest temperatures were significantly detrimental to development.

Notes on Natural Enemies

Top of pageIn Réunion island, some natural enemies may contribute to the biological control of N. cyanescens in wild and untreated cultivated hosts. The life stages of the species that are most exposed to the action of natural enemies are those associated with the soil (mature larvae after they have left the fruit, pupae and emerging adults). Several arachnids may prey upon the adults during resting, foraging, mating and egg laying activities. The egg and larval stages are relatively well protected inside the host-fruit, although they may be attacked by parasitoids. Etienne (1973) mentioned some parasitoids attacking N. cyanescens in Réunion. According to Wharton et al. (1999) this species could be Psyttalia insignipennis or Psyttalia distinguenda. All other natural enemy species listed in this datasheet were introduced into the region for fruit fly or stable fly control.

Means of Movement and Dispersal

Top of page Natural Dispersal

Natural dispersal of N. cyanescens could be the transportation of adults over long distances by wind and this may constitute the principal method of dispersal.

Movement in Trade

The eggs or larvae may also be easily dispersed in the fresh fruit trade (tomato, chilli, etc.). The pest has probably been introduced into Réunion island and Mauritius by this route.

Impact

Top of pageIn the Indian Ocean region, the tomato fruit fly is a major pest of cultivated Solanaceae in the unripe fruit of which the female fly lays her eggs. In Madagascar, the species is not considered as an important pest, but damage to crops has never really been quantitatively assessed. Mostly, the importance of yield loss is underestimated because of early attacks on unripe fruit (olive size) and rapid rotting and drop of the infested fruit. In Réunion island, in the absence of chemical control, damage levels could attain 25 to 50% of a given fruit cohort (Brévault, 1999). The resulting yield loss can be quantified in terms of a reduced number of fruit and organoleptic quality of fruit. Repeated and improper insecticide spraying is costly for smallholders, but also harmful to the environment, with side effects on natural enemies and biodiversity.

Detection and Inspection

Top of pageOn the crop or in shipped commodities, a detailed observation of the fruit surface is necessary to detect the presence of eggs or larvae (discoloration around oviposition stings). Suspected fruit may be dissected to look for eggs (in a cavity just under the skin) and larvae (internal feeding, tunnelling and rotting). The presence of adults can be detected on a local scale using bright-orange spherical sticky traps within crops (Brévault et al., 1999; Brévault and Quilici, 1999).

Similarities to Other Species/Conditions

Top of pageOther species attacking tomato are present in other parts of the world: Rhagoletis tomatis in Chile (Frias and Martinez, 1991), Rhagoletis lycopersella in Peru (Smyth, 1960), Rhagoletis blanchardi in Brazil (Fenilli, 1993), Dacus punctatifrons in Cameroon (Tindo and Tamo, 1999) and Bactrocera latifrons in the South Pacific (Hardy, 1973).

Prevention and Control

Top of page Cultural Control and Sanitary Methods

It is recommended to destroy attacked fruit and wild host plants that surround the cultivated crop in order to limit increase in the fly population.

Biological Control

Parasitoids play a role in controlling populations of N. cyanescens in wild host or untreated crops.

Chemical Control

Chemical control is mainly based on the use of pyrethroids during the fruiting stage of the crop. Sprayings with deltamethrin or lambda-cyhalothrin are recommended as soon as the crop reaches the fruiting stage.

Early Warning Systems

The adult females strongly respond to a bright orange sphere, which may have a potential use in the development of a specific trapping system (Brévault et al., 1999; Brévault and Quilici, 1999).

Field Monitoring/Economic Threshold Levels

Before an effective trapping system becomes available, counting symptoms on fruit can help in forecasting pest incidence and determining the necessity and timing of insecticide applications.

IPM Programmes

Checking for the presence of immature stages in fruit can be helpful for spraying decisions. By contrast with some other tephritids of economic significance in Réunion island, no effective lure or bait is known to attract the male or female flies.

References

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Bordat D, 1992. Evaluation des problèmes entomologiques des cultures légumières de Mayotte. Rapport de mission du 7 au 11/12/1992. Doc. CIRAD-CA, Montpellier.

Brévault T, 1999. Mécanismes de localisation de l’hôte chez la mouche de la tomate, Neoceratitis cyanescens (Diptera:Tephritidae). Thèse. Montpellier, France: l’Université de Montpellier II - Ecole Nationale Supérieure Agronomique de Montpellier.

Brevault T, Quilici S, 1999. Factors affecting behavioural responses to visual stimuli in the tomato fruit fly, Neoceratitis cyanescens. Physiological Entomology, 24(4):333-338; 17 ref.

Brevault T, Quilici S, 2000. Diel patterns of reproductive activities in the tomato fruit fly, Neoceratitis cyanescens. Physiological Entomology, 25(3):233-241; 28 ref.

BrTvault T, Quilici S, 2000. Relationships between temperature, development and survival of different life stages of the tomato fruit fly, Neoceratitis cyanescens. Entomologia Experimentalis et Applicata, 94(1):25-30; 19 ref.

BrTvault T, Quilici S, GlTnac S, 1999. Tomato fruit fly on Reunion Island: using signals emitted by the host plant to trap females. Phytoma, No. 515:35-36; 5 ref.

CABI/EPPO, 1998. Distribution maps of quarantine pests for Europe (edited by Smith IM, Charles LMF). Wallingford, UK: CAB International, xviii + 768 pp.

CABI/EPPO, 2004. Neoceratitis cyanescens. Distribution Maps of Plant Pests, No. 140. Wallingford, UK: CAB International.

Carrol LE, White IM, Friedberg A, Norrbom AL, Dallwitz MJ, Thompson FC, 2002. Pest Fruit Flies of the World: Descriptions, Illustrations, Identification, and Information Retrieval. Version: 8th August, 2002.

Dubois J, 1965. La mouche des fruits malgache (Ceratitis malagassa Munro) et autres insectes des agrumes, pêchers et pruniers à Madagascar. Fruits, 20(9):435-460.

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Etienne J, 1972. The principal injurious Trypetids of the Island of Reunion. Annales de la Societe Entomologique de France, 8(2):485-491

Etienne J, 1973. The permanent rearing of Pardalaspis cyanescens (Dipt. Trypetidae) on an alternative food-plant. Annales de la Societe Entomologique de France, 9(4):853-860

Etienne J, 1982. Etude systématique, faunistique et écologique des Tephritidae de la Réunion. Doctoral thesis, Ecole Pratique des Hautes Etudes, Paris, France.

Fenilli R, 1993. Occurrence of Rhagoletis blanchardi Aczel (Diptera: Tephritidae) on tomato plants. Anais da Sociedade Entomologica do Brasil, 22(2):415-416

Frias L D, Martinez H, 1991. Taxonomic study on Rhagoletis tomatis Foote (Diptera: Tephritidae). Acta Entomologica Chilena, No. 16:247-254

Hancock DL, 1984. Ceratitinp (Diptera: Tephritidae) from the Malagasy subregion. Journal of the Entomological Society of Southern Africa, 47(2):277-301

Hancock DL, White IM, 1997. The identity of Trirhithrum nigrum (Graham) and some new combinations in Ceratitis MacLeay (Diptera: Tephritidae). Entomologist, 116(3/4):192-197; 10 ref.

Hardy DE, 1973. The fruit flies (Tephritidae-Diptera) of Thailand and bordering countries. Pacific Insects Monograph, No. 31:353pp.

Lavergne R, 1981. Fleurs de Bourbon. Tome IV. Saint-Denis, La Réunion: Cazal.

Msaidie Kassim, Soilihi AM, 2000. Fruit flies in the Federal Islamic Republic of the Comoros. Proceedings of the Indian Ocean Commission, Regional Fruit Fly Symposium, Flic en Flac, Mauritius, 5th-9th June, 2000, 71-72.

Orian AJE, Moutia LA, 1960. Fruit flies (Trypetidae) of economic importance in Mauritius. Revue Agricole et Sucriere de l'Ile Maurice, 39:142-150.

Quilici S, Brevault T, 1999. The tomato fruit fly: Neoceratitis cyanescens (Bezzi). Diptera : Tephritidae. French name : la mouche de la tomate. The tomato fruit fly: ^italic~Neoceratitis cyanescens^roman~ (Bezzi). Diptera : Tephritidae. French name : la mouche de la tomate, 2 pp.

Quilici S, Brevault T, Hurtrel B, 2000. Major research achievements in RTunion within the Indian Ocean Commission regional fruit fly programme. Proceedings of the Indian Ocean Commission, Regional Fruit Fly Symposium, Flic en Flac, Mauritius, 5th-9th June, 2000, 29-33; 6 ref.

Smith IM, McNamara DG, Scott PR, Holderness M, 1997. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization., Ed. 2:vii + 1425 pp.; many ref.

Smyth EG, 1960. A new Tephritid fly injurious to tomatoes in Peru. Bulletin of the California Department of Agriculture, 49:16-22.

Tindo M, Tamo M, 1999. The fruit fly Dacus punctatifrons (Diptera: Tephritidae) as a problem in tomato production in the LekiT region (southern Cameroon). Annales de la Socie^acute~te^acute~ Entomologique de France, 35(Supp.):525-527; 2 ref.

Wharton RA, Quilici S, Hurtrel B, Mercado I, 1999. The status of two species of Psyttalia Walker (Hymenoptera: Braconidae: Opiinae) reared from fruit-infesting Tephritidae (Diptera) on the Indian Ocean Islands of RTunion and Mauritius. African Entomology, 7(1):85-90; 95 ref.

White IM, Elson-Harris MM, 1992. Fruit flies of economic significance: their identification and bionomics. Wallingford, UK: CAB International, 601 pp.

White IM, Meyer Mde, Stonehouse J, 2000. A review of native and introduced fruit flies (Diptera, Tephritidae) in the Indian Ocean islands of Mauritius, RTunion, Rodrigues and Seychelles. Proceedings of the Indian Ocean Commission, Regional Fruit Fly Symposium, Flic en Flac, Mauritius, 5th-9th June, 2000, 15-21; 22 ref.

Distribution Maps

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