Authors: J. van der Berg, A. Erasmus, M. van Rooyen. Text extracted with permission from the editors from: Prinsloo, G.L. & Uys, V.M. (Eds) 2015. Insects of Cultivated Plants and Natural Pastures in Southern Africa. Entomological Society of Southern Africa.
Bactrocera invadens
Other common names: invader fruit fly; Asiatiese vrugtevlieg (A); mosca-invasiva-da-fruta (P)
The Asian fruit fly belongs to the Bactrocera dorsalis species complex and is therefore very similar to the other species in this group. To the untrained eye, the Asian fruit fly may at first be mistaken for a red and yellow wasp (Vespidae). This fruit fly bears some similarity to African fruit flies of the genus Dacus. The adults can be separated from the latter genus by looking for the following: a complete yellow scutellum; yellow longitudinal lines on the upper, lateral margins of the thorax; a dark “T” shape on the upper surface of the abdomen consisting of a dark band just anterior of the middle of the abdomen, with a medium, dark stripe running from this band to the posterior of the abdomen; all femora are yellow and hind tibiae are conspicuously dark; wings clear with a uniformly dark edge (continuous coastal band). The maggots are difficult to distinguish from other fruit fly species without molecular techniques.
Origin and distribution
The Asian fruit fly is native to Sri Lanka, India and Bhutan and presently occurs throughout Africa south of the Sahara, where it was first recorded from Kenya and Tanzania in 2003. In southern Africa it is known from Namibia, Botswana, Mozambique and Zimbabwe, but is not yet established in South Africa.
Host plants
The Asian fruit fly is evidently highly polyphagous and over 70 wild and cultivated exotic host plants in more than 25 plant families have been recorded so far from Africa. Mango is preferred, followed by guava, papaya, banana, citrus and tomato. Other commonly cultivated hosts such as apple, peach, persimmon, coffee and avocado are also known.
Damage
The fruit fly devastates mango crops and in tropical Africa can result in much of the crop dropping before reaching maturity. It therefore has a large socio-economic impact in rural areas where people depend on mangos to supplement their income. Its effect on citrus is less devastating and it only attacks fruit shortly before maturity. Being an internal fruit pest, the Asian fruit fly is considered a quarantine pest and infested fruit will be rejected for export. Due to its absence from most export destinations, most countries will require a postharvest treatment or a system control approach before accepting fruit from an area known to be affected by this pest.
Life history
The Asian fruit fly is primarily a tropical species that prefers high relative humidity. In the tropics at low altitude it can be found throughout the year but its numbers decline during the dry season. At altitudes above 1000 m and during dry seasons it is less able to compete with Mediterranean fruit fly and marula fruit fly. The mean generation time is 31 days at an optimal temperature of 28 ?C and the time from egg to adult, 25 days. Average net fertility is 608 eggs with a mean daily oviposition rate of 18 eggs. Adult females will survive for about 75 days.
Natural enemies
Being an introduced fly, little is known about the efficacy of indigenous parasitoids but in parts of Africa the foreign parasitoid Fopius arisanus (Sonan) is being released for biological control. Ants on the orchard floor will attack the larvae that are about to pupate and spiders attack the adult flies.
Management
As with other flies in the Bactrocera dorsalis complex, the Asian fruit fly can be attracted to methyl eugenol from up to 800 m away. This lure is therefore an excellent attractant for monitoring males in traps and for eliminating males with attract-and-kill techniques. Female flies can be monitored with Bio-lure® 3-component lure. Sanitation, or the removal of infested fruit from and under trees, is an essential part of management and should take place once a week. Infested fruit should be buried in the ground, at least 30 cm deep or chopped up finely. Flies can be controlled by using a combination of male annihilation techniques and bait sprays or bait stations. Male annihilation can take the form of mass trapping with traps containing methyl eugenol and an insecticide that are hung in trees at approximately 12 per hectare. Male annihilation alone may provide adequate control over a long period of time but usually baits or bait stations are required to reduce the number of females that damage the fruit. Baits are applied as large droplets at very low volumes so that little residue occurs on the fruit. Baiting must be implemented when the fruit start to colour as it will take a few weeks to reduce populations sufficiently.
Two-spotted pumpkin fly
Dacus bivittatus
Other common names: greater pumpkin fly; grootpampoenvlieg (A)
Lesser cucurbit fly
Dacus ciliates
Other common names: kleinpampoenvlieg (A)
Pumpkin fly
Dacus frontalis and Dacus punctatifrons
Jointed pumpkin fly
Dacus vertebratus
Other common names: naatpampoenvlieg (A)
Eggs: Small, whitish and oval; laid in groups under the skin of the fruit. Larvae: White to cream-coloured, legless maggots, 8-10 mm in length. The rear end is blunt and the head is pointed.
Pupae: Small, brown and formed in soil.
Adults: All five pumpkin fly species look alike and it is not easy to distinguish them from each other. Dacus bivittatus, D. ciliantus and D.vertebratus are illustrated here. With their elongated, reddish-brown bodies and yellow markings, they resemble small wasps. They all have a very characteristic yellow area on the thorax where it joins the abdomen. Smaller yellow markings occur on the thorax, but they are less noticeable. All five species have clear wings with varying black markings. The black markings on the wings of Dacus bivittatus are more pronounced than in the other four species. The size (length) of the flies varies from 6-10 mm. The sizes of the three most common species are as follows: Dacus ciliatus 6-7 mm, Dacus verterbratus 8 mm and Dacus bivittatus 9-10 mm.
Origin and distribution
All species treated here are indigenous to sub-Saharan Africa from where they were originally described. They are all widespread throughout Africa.
Host plants
All five species primarily attack cucurbits, but Dacus bivittatus, Dacus bivittatus and Dacus ciliates also attack tomatoes and Dacus bivittatus also attacks eggplant. Dacus vertebratus is more common on watermelon. Other crops attacked as secondary hosts include green beans, papayas and granadilla.
Damage
Apart from flowers that are sometimes attacked, pumpkin flies have a preference for young, soft fruit, smaller than 100 mm. The sites where eggs are laid are usually referred to as “sting sites”. The areas around these “sting sites” sink in (illustrated) and the fruit discolours around the eggs. The symptoms persist even when eggs fail to hatch. Damage is therefore irreversible and fruit may be deformed without rotting. Feeding by the larvae (illustrated) and secondary infections cause the fruit to turn soft and rot rapidly. Sometimes young fruit are aborted by the plant and some fruit will fail to ripen, while others continue to grow, but will be severely deformed. Sometimes excess fluid produced by the fruit oozes from affected areas and excreta of maggots may also be present. Puncture sites are vulnerable to secondary infestations by pathogens and other insects, i.e. other non-related fly larvae.
Pumpkin flies are significant pests of cucurbits and sometimes cause serious yield loss. They are especially troublesome late in the season when most of the young fruits are attacked. Their status as pests of cucurbits varies from year to year.
Life history
After mating, females lay their eggs under the skin of fruit, in groups of fewer than 10. The eggs take approximately two days to hatch and the larvae live for approximately seven days inside the fruit where they remain until they are ready to pupate in the soil. Fully-grown larvae leave the fruit after approximately a week of feeding and move to the ground. Here they bury themselves shallowly in loose soil, usually under or close to the fruit. When the soil is too hard or compact, the larvae characteristically propel themselves to a more suitable location, by folding the body in two, and releasing their grip at the right moment, thrusting themselves forward for distances up to 160 mm. This is a dramatic but quick and effective way to escape unfavourable conditions and to dislodge predators like ants.
Adult pumpkin flies emerge after approximately two weeks and following another two weeks they are sexually mature. These flies can live up to six months under favourable, cool conditions. Adult flies are often associated with plants other than their host plant, using nearby plants as hiding, resting or overwintering sites, and are also frequently seen consuming honeydew produced by hemipteran insects. Plants with extra-floral nectaries also attract adults. The adults are the overwintering phase. They sometimes congregate in numbers in protected areas during the colder winter months when host plants are not available. However, in modern climates, when host plants are available, they continue to develop throughout the winter month (e.g. in greenhouses and tunnels).
Natural enemies
At least one parasitic wasp, the braconid Fopius bevisi (Brues), is known to attack the larvae of Dacus ciliatus in South Africa. This natural enemy is, however, ineffective in keeping pumpkin fly numbers below threshold.
Management
Pumpkin fly numbers take a long time to build up to economic levels (their life cycles usually last about two months). Plantings between December and February suffer more severe losses than those planted earlier. To lessen the build-up of fly populations within gardens, it is crucial that all infested fruit be removed and destroyed. Deep burial is sometimes the only way to prevent larvae from maturing in discarded produce. In areas with prevailing high ambient temperatures and low humidity, infestations are usually less severe.
Several insecticides are available for control of pumpkin flies, of which baits are the most effective as they target the adult flies before they can attack fruit. Flies can only lay eggs after maturing for a period of 1-3 weeks, during which they feed extensively on sweet liquids and are then more likely to be attracted to poisoned sweet baits. These baits can also be applied to other plants or surfaces and are effective when sprayed in areas where overwintering populations occur. Preventative control is possible and it is advisable to be on the lookout for adults even before a cucurbit crop is planted. Apart from preventative spraying before cucurbits are planted, the first in-field sprays should be timed to coincide with the appearance of flowers. Whatever control measure is used, it is critical that young, small fruit be protected as pumpkin flies cannot puncture old fruit, and fruit larger than 100 mm is usually less attractive. Larger fruit with visible lesions is common, but this is a result of an earlier infestation when fruit was much smaller and younger.
Pumpkin fly, Dacus sp. A sunken area on a young pumpkin, indicating an oviposition site just beneath the skin of the fruit. - D. Visser, ARC
Pumpkin fly, Dacus sp. Larvae infesting a pumkin fruit. - D. Visser, ARC
Jointed pumpkin fly, Dacus vertebratus. Adult - G. Goergen, IITA_2
Mediterranean fruit fly
Ceratitis capitata
Other common names: medfly; Mediterreense vrugtevlieg (A); mosca-do-Mediterrâneo (P)
Marula fruit fly
Ceratitis cosyra
Other common names: mango fruit fly, maroela-vrugtevlieg (A); mosca-da-fruta-da-manga (P)
Natal fruit fly
Ceratitis rosa
Other common names: Natal fly; Natalse vrugtevlieg (A); mosca-da-fruta-do-Natal (P)
Adults: Ceratitis rosa (illustrated) is recognized by its characteristic pattern of brown wing bands, three black areas on the apical half of the scutellum, and by the male having feathering of the mid tibia and no feathering on the mid femur. The female of C. capitata (illustrated) can be separated by the yellow wing pattern and the apical half of the scutellum being entirely black; the male can be separated from other species by the black, pointed expansion at the apex of the anterior pair of orbital setae. Ceratitis cosyra (illustrated) can easily be separated from other species by the characteristic pattern of yellow wing bands, and by three black areas in the apical half on the scutellum.
Origin and distribution
Fruit flies in the genus Ceratitis MacLeay are predominantly an Afrotropical group and the three species treated here are widely distributed in sub-Saharan Africa, including southern Africa.
Host plants
These fruit flies are highly polyphagous. Ceratitis capitata and C. rosa have been recorded from more than 300 and 100 cultivated and wild hosts respectively, while C. cosyra has also been recorded from a large number of hosts in a variety of plant families. In southern Africa the marula, Sclerocarya birrea (Anacaridaceae) is an important wild host of C. cosyra. An annotated list of the host plants of Ceratitis species is provided De Meyer et al. (2002).
Damage
Damage (illustrated) begins when the female fly punctures the skin of the fruit and lays eggs underneath it. Decay is caused by the larvae feeding in the flesh of the fruit, which renders the fruit unmarketable. Ceratitis cosyra and Ceratitis rosa are the dominant species in mango orchards. Mango fruit are not infested during the early stages of fruit development but are markedly more prone to attack closer to harvest. Fruit that ripen on the tree and are picked for local markets are more prone to attack than mature but green fruit picked for export. Fruit flies are important quarantine pests and indirect losses from quarantine restrictions that are imposed by importing countries, to prevent entry and the possible establishment of unwanted fruit fly species.
Life history
The development rate of these three fruit flies at different temperatures was studied by Grout & Stolz (2007). At 26 ?C the eggs of C. cosyra took about two days to hatch, the larval stage was close to six days when reared on artificial medium while the pupal stage was about 9-10 days. The mean egg to egg development at 26 ?C took 20-24 days.
Natural enemies
Several predators and parasitoids, including unidentified species of Fopius, Psyttalia. Opius (all Braconidae) and Tetrastichus (Eulophidae) found in mango agro-ecosystems can contribute to the suppression of fruit flies. Spiders and ants are examples of predators.
Management
Management practices include the use of commercially available traps and lures for monitoring fruit fly populations (Grové et al. 2009) in addition to the following strategies:
Bait stations, bait sprays and attract and kill: Bait stations placed in mango trees are registered for control of fruit flies in mango orchards. Control with bait sprays is based on the use of hydrolysed proteins in combination with an insecticide. The method targets adult flies, especially females and aims to attract and kill them before they can lay eggs in the fruit. The spray should be targeted to the lower surface of the leaves to enhance the persistence of the bait and reduce exposure to the sun and rain. This applies when monitoring data indicate that fruit flies are present in high numbers. Bait applications can be applied weekly depending on monitoring data. A pheromone attractant in combination with a contact insecticide, which is applied in the form of small droplets to the leaves, is also registered.
Natural enemies: Parasitoids and predators which can contribute to the suppression of fruit flies are present in fruit agro-ecosystems. Efforts to conserve natural enemies in commercial orchards through more efficient management, may contribute to the overall suppression of fruit flies.
Orchard sanitation: Orchard sanitation entails the collection and destruction of all fallen fruit from the ground. This can contribute towards the reduction in fruit fly numbers, by preventing the pupation of the maggots in the soil. Fruit must be destroyed by burying it at a depth of 600 mm or putting it through a hammer mill.
Eradication of alternative host plants: Alternative host plants serve as a breeding ground and source of fruit flies and must be eradicated when found in the vicinity of the orchard. Wild growing guava is an example of a weed that hosts fruit flies.
Marula fruit fly, Ceratitis cosyra. Adult female. - G. Goergen, IITA
Fruit fly larval damage to a mango fruit. - T. Grové, ARC
Fruit fly larvae feeding in a mango fruit. - T. Grové, ARC
Mediterranean fruit fly
Ceratitis capitata
Other common names: medfly; Mediterreense vrugtevlieg (A); mosca-do-Mediterrâneo (P)
Natal fruit fly
Ceratitis rosa
Other common names: Natal fly; Natalse vrugtevlieg (A); mosca-da-fruta-do-Natal (P)
The immature and adult stages of both species are similar, with C. rosa being the slightly larger of the two.
Eggs: Illustrated. White, smooth and banana-shaped, 1 mm in length; laid under the skin of fruit.
Larvae: There are three instars, found only in the host fruit/vegetable. First instar larvae are about 1 mm in length, reaching 7-9 mm (Medfly) and 9-11 mm (Natal fruit fly) in the third instar. First instar larvae are translucent; subsequent instars are white to cream-coloured. Larvae are legless, and the body tapers from a blunt posterior to a pointed anterior end, with black mouth hooks visible in especially the second and third instar.
Pupae: In a cylindrical puparium (illustrated) with rounded ends, 4-6 mm in length, straw coloured initially, turning dark reddish brown after about three days. Pupation usually occurs in the soil.
Adults: Medfly (illustrated) – slightly smaller than a housefly, about 3-5 mm in length. Yellowish-orange in colour with a dark brown tinge, especially on the abdomen, legs and some markings on the wings. The eyes are reddish-purple with a blue fluorescence. The thorax is creamy white to yellow with a characteristic pattern of black blotches. The apical half of the scutellum is inflated and typically shiny black. Wings are patterned with black, brown, and brownish-yellow markings.
Natal fruit fly (illustrated) – about the size of a housefly, up to 8 mm in length. More brown in colour than Medfly. The eyes are reddish-purple, usually with a green fluorescence. The thorax is similar to Medfly, except for the apical half of the scutellum which is characterized by three black areas. The male has black feathering on the mid-tibia. As in Medfly, the wings are also patterned but wing bands are brown and generally darker.
Origin and distribution
Mediterranean fruit fly is thought to have originated in East Africa and is now widely distributed in over 80 countries throughout the world. Natal fruit fly, which was originally described from Mozambique, is endemic to Africa and the Indian Ocean Islands and does not occur elsewhere.
Host plants
Medfly and Natal fruit fly are known to infest over 260 species of fruits, flowers, vegetables and even nuts, but thin-skinned, ripe succulent fruits and berries are preferred. In the Western Cape, these include all deciduous fruits and wine and table grapes and a great many other fruits and berries of trees or shrubs, wild or domestic. Examples of fruits readily infested include stone fruit, table grapes, guava, loquat, litchis, mangoes and wild plum (Harpephyllum caffrum), while lemon, avocado and olive are examples of fruit with lower infestation.
Damage
In both species only the larval stages causes damage. Eggs are deposited just under the skin of mostly ripe or ripening host fruits (illustrated); oviposition sites generally resemble a discoloured pin-prick spot on the fruit skin. The resulting larvae feed on the fruit tissue, tunnelling towards the fruit centre. Under high fruit fly infestation situations, even green fruit can be attacked. The feeding activity together with subsequent infection by micro-organisms and/or secondary pests can reduce the fruit to a pulpy mass, as illustrated.
Medfly is one of the world’s most destructive fruit pests, due to its wide distribution, very wide host range, and ability to tolerate cooler climates compared to most fruit fly species. Natal fruit fly has a lower pest status due to its narrower distribution and host range. Both are international quarantine pests. In uncontrolled conditions, crop losses on some fruits by either or both species can reach 100%.
Life history
The life history is similar for both species. Duration of the different life stages is largely governed by temperature and availability of food. Three to about six generations can occur per year. Under favourable conditions female fruit flies become sexually mature and capable of laying eggs about five days after emergence. After mating they actively seek out ripening fruit and deposit their eggs in a small cavity just below the fruit skin. A single female can lay 1-10 eggs in a cavity, but 50 or more eggs from multiple females can be found in one cavity. After 3-7 days the larvae hatch and start feeding on the flesh of the fruit. Larvae reach maturity from about 10-45 days later, after which they leave the fruit, fall to the ground and pupate just below the surface in the soil. About 10-50 days later the adult flies emerge, they crawl up to the soil surface, and the cycle is complete.
During warm conditions in ripe fruit, the life cycle can be completed in as little as 3-4 weeks, but this can increase to about two or three moths in winter or when eggs are laid in greener fruit. Adult flies can live from 2-6 months under favourable conditions, but die within four days if food is unavailable. Fruit flies are present throughout the year, moving from one fruit kind to another, both cultivated and wild, as they ripen in succession. Peak numbers occur in late summer and autumn. Natal fruit fly prefers cooler and more humid conditions, while medfly predominates in hotter, drier conditions.
Natural enemies
These include entomopathogenic bacteria (e.g. Bacillus thuringiensis, Saccharopolyspora siniosa), fungi (e.g. Entomophthora spp., Beauveria bassiana, Metarpizium anisopliae), and nematodes (Steinernema spp., Diplogaster sp.), a microsporidian, Nosema tephritidae, ants and spiders. The largest contribution to biological control is by numerous hymenopterous parasitoids. Elsewhere some species are mass-reared for augmentative releases as part of an integrated, area-wide management approach, including species of the braconid genera Diachasmimorpha and Fopius.
Management
Biological control of fruit flies has not always been regarded as successful when measured by economic returns, due partly to the very low economic threshold for fruit fly damage. Classical biological control is challenged by a low fecundity of parasitoids compared to fruit flies, poor detection of fruit fly populations by parasitoids, and fruit flies having a degree of refuge from parasitoid attack in large or thick-skinned fruit (larvae) or under dense litter (pupae).
Other management practices include monitoring populations with lure-bated traps (on which all decisions on interventions should be based), control of host plants (removal or fruit-stripping), sanitation (cleaning-picking of orchards and vineyards; destruction of infested/fallen fruit), application of fruit fly bait (usually a protein attractant mixed with a synthetic or natural insecticide), the use of bait stations (so-called “attract & kill” technology), augmentative releases of parasitoids, and where justified, use of the sterile insect technique (STI). It is widely recognized that fruit flies are best managed by an area-wide, integrated approach incorporating as many of the above-mentioned practices as possible.
Mediterranean fruit fly, Ceratitis capitata. Eggs, deposited just under the skin of the fruit. - B.N. Barnes, ARC.
Mediterranean fruit fly, Ceratitis capitata. Puparia. - Florida Dept. Agric & Consumer Serv. Bugwood. org
A peach infested with mature fruit fly larvae. - ARC; Infruitec-Nietvoorbij
