Anastrepha fraterculus (South American fruit fly)

Pictures

Picture	Title	Caption	Copyright
Title Wing Caption Anastrepha fraterculus, wing markings and venation. Copyright USDA-ARS	Wing	Anastrepha fraterculus, wing markings and venation.	USDA-ARS
Title Genitalia Caption Anastrepha fraterculus, genitalia. Copyright USDA-ARS	Genitalia	Anastrepha fraterculus, genitalia.	USDA-ARS
Title Genitalia. Caption Anastrepha fraterculus, genitalia. Copyright USDA-ARS	Genitalia.	Anastrepha fraterculus, genitalia.	USDA-ARS
Title Genitalia. Caption Anastrepha fraterculus, genitalia. Copyright USDA-ARS	Genitalia.	Anastrepha fraterculus, genitalia.	USDA-ARS
Title Adult Caption Anastrepha fraterculus, adult female. Copyright USDA-ARS	Adult	Anastrepha fraterculus, adult female.	USDA-ARS

Identity

Preferred Scientific Name

• Anastrepha fraterculus (Wiedemann)

Preferred Common Name

• South American fruit fly

Other Scientific Names

• Acrotoxa fraterculus (Wiedemann)
• Anastrepha braziliensis Greene
• Anastrepha costarukmanii Capoor
• Anastrepha fraterculus var. soluta Bezzi
• Anastrepha lambayecae Korytkowski & Ojeda
• Anastrepha peruviana Townsend
• Anastrepha pseudofraterculus Capoor
• Anastrepha scholae Capoor
• Anthomyia frutalis Weyenburgh
• Dacus fraterculus Wiedemann
• Tephritis mellea Walker
• Trypeta fraterculus (Wiedemann)
• Trypeta unicolor Loew

International Common Names

• English: fruit fly, South American
• Spanish: mosca de la ciruela; mosca de la fruta suramericana; mosca sudamericana de la fruta
• French: mouche des fruits sud-américaine
• Portuguese: mosca das frutas sul-americana

Local Common Names

• Germany: Fruchtfliege, Suedamerikanische

EPPO code

• ANSTFR (Anastrepha fraterculus)

Summary of Invasiveness

A. fraterculus has a broad host range, particularly in the family Myrtaceae, but it is also a pest of citrus and apples [Malus domestica] in some areas. It is the most important pest species of Anastrepha in subtropical areas of South America, thus it and Anastrepha ludens may be more of a threat of introduction to other subtropical areas of the world than other species of Anastrepha. It is invasive in the Galapagos Islands. As it is probably a complex of cryptic species whose ranges and delimitation remain unresolved, there is also the threat of introduction of particular cryptic species to other areas within the range of the complex. It is considered an A1 quarantine pest by EPPO.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Diptera
•                         Family: Tephritidae
•                             Genus: Anastrepha
•                                 Species: Anastrepha fraterculus

Notes on Taxonomy and Nomenclature

This is probably a complex of cryptic species, which has not yet been studied in sufficient detail to permit clear delimitation of the individual species. Data of various types, including isozymes, karyotypes, morphometric analysis of morphology, mating incompatability and pest status (e.g. Steck, 1991, 1999; Alberti et al., 2002; Hernández-Ortiz et al., 2004; Selivon et al., 2005; Vera et al., 2006), indicate that certain populations (e.g. Andean and lowland populations in Venezuela; sympatric populations in southern Brazil) are likely to be distinct species, but comprehensive analysis is needed to resolve the status of other populations from throughout the range of the complex.

The oldest name pertaining to the complex is Dacus fraterculus Wiedemann, 1830. The current combination was proposed by Wulp (1899). Numerous names are currently recognized as synonyms of A. fraterculus, but remain available and may become valid if the complex is split into multiple species.

Description

For a general description of the genus, see the datasheet on Anastrepha.

Adult

As in most other Anastrepha spp., the adults of A. fraterculus are easily separated from those of other tephritid genera by a simple wing venation character; vein M, the vein that reaches the wing margin just behind the wing apex, curves forwards before joining the wing margin. Furthermore, most Anastrepha spp. have a very characteristic wing pattern; the apical half of the wing has two inverted 'V'-shaped markings, one fitting within the other; and a stripe along the forward edge of the wing, which runs from near the wing base to about half-way along the wing length.

Identification to species is more difficult. In particular, for positive identification it is essential to dissect the aculeus (the distal, piercing part of the ovipositor that is normally retracted into the oviscape) of a female specimen. A. fraterculus adults are difficult to separate from those of Anastrepha sororcula, Anastrepha zenildae and Anastrepha turpiniae, and to a lesser extent Anastrepha obliqua and Anastrepha suspensa, and several other species of the fraterculus group; if necessary, specimens should be referred to a specialist.

The body is predominantly yellow to orange-brown, and the setae are red-brown to dark-brown.

Head: yellow except ocellar tubercle brown. Facial carina, in profile, concave. Frons with three or more frontal setae, two orbital setae. Antenna not extended to ventral facial margin.

Thorax: mostly yellow to orange-brown, with the following areas yellow to white and often contrasting: postpronotal lobe; single medial and paired sublateral vittae on scutum, the slender medial vitta extended nearly full-length of the scutum, slightly broadened posteriorly, ovoid; sublateral vitta extended from transverse suture almost to posterior margin, including intra-alar seta; scutellum; propleuron; dorsal margin of anepisternum; dorsal margin of katepisternum; katepimeron; and most of anatergite and katatergite. Area bordering scutoscutellar suture medially usually with dark-brown spot. Subscutellum and mediotergite dark-brown laterally. Scutum entirely microtrichose or at most with small presutural, medial bare area.

Wing: vein M strongly curved apically. Vein R₂₊₃ nearly straight. Pattern mostly orange-brown and moderate brown. C-band and S-band usually connected along vein R₄₊₅, but sometimes separated; marginal hyaline spot (or end of band) present in cell r₁ at apex of vein R₄₊₅. S-band with middle section between costa and vein Cu₁ largely yellow to orange with narrow brown margins, darkening distally; distal section of band relatively narrow, well-separated from apex of vein M. V-band with distal arm usually complete and connected to proximal arm; proximal arm extended to vein R₄₊₅, not connected to S-band.

Abdomen: tergites yellow to orange-brown, without dark-brown markings.

Male terminalia: lateral surstylus moderately long, in posterior view slightly tapered, somewhat truncate apically. Phallus 2.7-3.2 mm long; ratio to mesonotum length 0.90-1.10. Glans with basolateral membranous lobe, mostly membranous medially, with isolated, T-shaped apical sclerite.

Female terminalia: oviscape straight, 1.40-2.15 mm long; ratio to mesonotum length 0.59-0.75. Dorsobasal scales of eversible membrane numerous, hook-like, in triangular pattern. Aculeus length 1.50-1.95 mm; tip 0.20-0.30 mm long, 0.12-0.15 mm wide, gradually tapering, but with slight constriction proximal to serrate part, distal 0.50-0.67 serrate. Three spermathecae ovoid.

Immature Stages

Larva: it is very difficult, and in some cases impossible, to identify larvae of Anastrepha species from morphological characteristics. The key by Steck et al. (1990) and the interactive key by Carroll et al. (2004) are the best tools for larval identification. Descriptions of A. fraterculus larvae are provided by Weems (1980), Steck et al. (1990) and White and Elson-Harris (1994). White and Elson-Harris (1994) described the third-instar larva as follows:

Larvae: medium-sized; 8.0-9.5 mm long; 1.4-1.8 mm wide.

Head: stomal sensory organ rounded, protuberant, with two to three peg-like sensilla; 7-10 oral ridges; accessory plates small; mandible heavily sclerotised, with a large slender curved apical tooth.

Thoracic and abdominal segments: anterior margin of T1 with a broad, encircling band of 4-11 discontinuous rows of small, sharply pointed spinules; T2 and T3 with three to seven rows of smaller spinules encircling each segment. Dorsal spinules occasionally on A1-A3, but absent from A4-A8. Creeping welts with 7-12 rows of small spinules. A8 with dorsal and sensilla well-developed; intermediate areas obvious, with large sensilla; ventral sensilla present.

Anterior spiracles: with 14-18 tubules.

Posterior spiracles: spiracular slits about three times as long as broad, with heavily sclerotised, dark-brown rimae. Spiracular hair bundles large; dorsal and ventral bundles of 12-16 long hairs, many branched in apical third; lateral bundles of six to nine hairs similarly branched.

Anal area: lobes large, protuberant, not grooved, grooved, or bilobed; surrounded by two to four discontinuous rows of small, sharp spinules.

Distribution

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Introductions

Risk of Introduction

EPPO lists A. fraterculus as an A1 quarantine pest (OEPP/EPPO, 1983) within the broad category 'non European Trypetidae'; it is also of quarantine significance to APPPC, CPPC and NAPPO. A. fraterculus, like the other Anastrepha spp., derives from tropical wet forest habitats and therefore represents a high risk to similar areas.

Consignments of fruits of Annona, Citrus, Fortunella, Malus, mango [Mangifera indica], peach [Prunus persica] and guava [Psidium guajava] from countries where A. fraterculus occurs should be inspected for symptoms of infestation and those suspected should be cut open in order to look for larvae. For example, EPPO recommends that such fruits should come from an area where A. fraterculus does not occur, or from a place of production found free from the pest by regular inspection for 3 months before harvest. Fruits may also be treated in transit by cold treatment (e.g. 13, 15 or 17 days at 0.5, 1 or 1.5°C, respectively) or, for certain types of fruits, by vapour heat (for example, keeping at 43°C for 4-6 h) (USDA, 1994), or by hot water immersion (Nascimento et al., 1992). Ethylene dibromide was previously widely used as a fumigant, but is now generally withdrawn because of its carcinogenicity. Carneiro and Salles (1994) showed that an entomopathogenic fungus (Paecilomyces fumosoroseus isolate CG 260) could be used to treat larvae entering soil, which then die upon pupariation.

Plants of host species transported with roots from countries where A. fraterculus occurs should be free from soil, or the soil should be treated against puparia, and should not carry fruits. Such plants may be prohibited for importation.

Habitat

Habitat List

Hosts/Species Affected

Pest status varies among populations of the fraterculus complex. The populations in Mexico and Central America are less significant pests (e.g. of guava [Psidium guajava], rose apple [Syzygium jambos] and occasionally peach [Prunus persica] and mango [Mangifera indica], but not citrus or apple [Malus domestica]) than some populations in the Andes, southern Brazil, and Argentina that also attack apples, citrus and a variety of other crops (even blackberries [Rubus fruticosus]). Some populations range into subtropical areas in southern Brazil and Argentina and temperate elevations in the Andes, and are pests in those zones.

The complex as a whole is broadly polyphagous (Norrbom, 2004a), but the preferred hosts are Myrtaceae, particularly the native American guava (P. guajava). Other cultivated mytaceous hosts include other Psidium spp., Campomanesia spp., rose apple, Horn of plenty [Feijoa sellowiana], Surinam cherry [Eugenia uniflora] and other Eugenia spp. Prunus spp., especially peach, and loquat [Eriobotrya japonica] are commonly reported hosts. The most frequent introduced hosts in Mexico are S. jambos and Terminalia catappa [Indian-almond] (Hernandez-Ortiz, 1992). Apple, pear, kumquat [Fortunella spp.], peach, loquat and various  Citrus spp. are among the cultivated crops attacked in southern Brazil, although most of the primary hosts are Myrtaceae (Salles, 1995b). Guava, Surinam cherry, grapefruit [Citrus paradisi], cherimoya [Annona cherimola], apricot [Prunus armeniaca], plum [Prunus domestica] and peach are significant hosts in Argentina (Ovruski et al., 2003; Segura et al., 2006).

In common with other polyphagous and difficult to identify species, many host records cannot be substantiated and only records confirmed by Norrbom (2004a) or subsequent reliable sources have been accepted here.

Host Plants/Plants Affected

Growth Stages

Symptoms

Symptoms List

Biology and Ecology

A. fraterculus eggs are laid below the skin of the host fruit. Many Anastrepha spp. lay their eggs deeper inside the fruit or in the seeds. The life cycle includes: the egg, three larval stages, pupa and adult. Salles (2000) presented a table showing the length of development at temperatures from 15-30°C. At 25°C the eggs hatch in 2.6-3.2 days and the larvae feed for another 11-14 days (up to 34.5 days at 15°C). Pupariation is in the soil under the host plant and the adults emerge after 10-15 days (43.2 days at 15°C) and may live up to 161 days in laboratory conditions. Salles (2000) reported that females can produce 278-437 eggs. The adults occur throughout the year (Christenson and Foote, 1960). They have no winter diapause or quiescence in more temperate areas such as southern Brazil (Salles, 1993). Reproductive behaviour in the laboratory and field has been studied by Lima et al. (1994).

Climate

Latitude/Altitude

Natural Enemies

Notes on Natural Enemies

Means of Movement and Dispersal

There is evidence that adults of Anastrepha spp. can fly up to 135 km (Fletcher, 1989) and therefore natural movement can be an important means of spread.

In international trade, the major means of dispersal to previously uninfested areas is the transport of fruit containing live larvae. For most regions, the most important fruits liable to carry A. fraterculus are guavas [Psidium guajava] and other Myrtaceae; Citrus, Malus and Prunus are attacked in some areas. There is also a risk from the transport of puparia in soil or packaging with plants that have already fruited.

Pathway Causes

Pathway Vectors

Plant Trade

Impact Summary

Impact

Anastrepha spp. are the most serious fruit fly pests in the tropical Americas (Norrbom and Foote, 1989), with the possible exception of introduced Ceratitis capitata (EPPO/CABI, 1996). A. fraterculus is an important pest of guavas [Psidium guajava] (and locally significant Myrtaceae) and mangoes [Mangifera indica], and also to some extent of Citrus and Prunus spp. (Hernandez Ortiz, 1992; White and Elson Harris, 1994). Some populations in South America, particularly in southern Brazil to northern Argentina, and in the Andean countries, are considered more significant pests than those in Mexico and Central America, and these probably represent different cryptic species.

Risk and Impact Factors

Impact outcomes

• Host damage
• Negatively impacts agriculture
• Negatively impacts livelihoods

Invasiveness

• Abundant in its native range
• Capable of securing and ingesting a wide range of food
• Has a broad native range
• Has high genetic variability
• Has high reproductive potential
• Highly adaptable to different environments
• Is a habitat generalist
• Proved invasive outside its native range
• Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc

Likelihood of entry/control

• Difficult to identify/detect as a commodity contaminant
• Difficult to identify/detect in the field
• Difficult/costly to control
• Highly likely to be transported internationally accidentally
• Highly likely to be transported internationally illegally

Detection and Inspection

No male lures have yet been identified for Anastrepha spp. However, they are captured by traps emitting ammonia. McPhail traps are usually used for the capture of Anastrepha spp. (White and Elson-Harris, 1994) and possible baits are ammonium acetate (Hedstrom and Jimenez, 1988), casein hydrolysate (Sharp, 1987) and torula yeast (Hedstrom and Jiron, 1985). The number of traps required per unit area is high. In a release and recapture test, Calkins et al. (1984) placed 18 traps per 0.4 ha and only recovered approximately 13% of the released flies.

Some studies have shown that egg morphology can be used to separate closely related species found in host fruits (Souza et al., 1983; Murillo and Jiron, 1994). The larvae of some species may also be differentiated using cuticular hydrocarbons (Sutton and Carlson, 1993). Neither method has yet been generalized for application outside of very specific circumstances.

Similarities to Other Species/Conditions

Identification of the fraterculus complex and closely related species is very difficult and is based mainly on measurements and subtle differences in the shape of the aculeus and its tip (Araujo et al., 1996; Araujo and Zucchi, 2006). The species most likely to be confused with A. fraterculus are Anastrepha obliqua, Anastrepha suspensa, and especially Anastrepha sororcula, Anastrepha zenildae and Anastrepha turpiniae.

A. obliqua differs in having the subscutellum entirely orange, not dark-brown laterally. It also lacks the medial spot on the scuto-scutellar suture that is usually present in the fraterculus complex. The aculeus tip is more serrate and less tapered basal to the serrate part. A. suspensa has the apical part of the S-band (the band on the anterior apical margin of the wing) much broader and touching or almost touching the apex of vein M. The other three species are distinguished from the fraterculus complex by the length of the aculeus and its tip, although there is slight overlap in these characters among these species. A. sororcula has a shorter aculeus, with a shorter, stouter tip, whereas A. zenildae and A. turpiniae have longer aculeus tips.

The larvae of Anastrepha are extremely difficult to identify and specialist help should be sought to confirm critical identifications. The third-stage larva is very similar to those of A. obliqua and A. suspensa, and these species usually cannot be distinguished (Steck et al., 1990). The larvae of A. sororcula, A. zenildae and A. turpiniae have not been described.

Prevention and Control

Control can be considerably aided by good cultural practices, for example, by gathering all fallen and infected host fruits and destroying them. Insecticidal protection is possible by using a cover spray or a bait spray. Malathion is the usual choice of insecticide for fruit fly control and this is usually combined with protein hydrolysate to form a bait spray (Roessler, 1989). Practical details are given by Bateman (1982). Bait sprays work on the principle that both male and female tephritids are strongly attracted to a protein source from which ammonia emanates. Bait sprays have the advantage over cover sprays in that they can be applied as a spot treatment so that the flies are attracted to the insecticide and there is minimal impact on most natural enemies. However, Nasca et al. (1983) warned that bait sprays could have a substantial effect on Chrysopidae (Neuroptera), which are natural enemies of many pests.

The toxicity to A. fraterculus of different insecticides used in baits was recently compared by Salles (1995) and Lerenzato et al. (1984). They advocated control measures be applied when 0.5-1.0 flies per day per trap were found. Like many fruit flies, shape and colour play a role in host seeking behaviour and Cytrynowicz et al. (1982) found a preference for yellow spheres. The sterile insect technique was tried in Peru (Gonzalez et al., 1971), but has not been applied on a realistic scale.

References

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Bateman MA, 1982. III. Chemical methods for suppression or eradication of fruit fly populations, In: Drew RAI, Hooper GHS, Bateman MA eds. Economic Fruit Flies of the South Pacific Region. 2nd edn. Brisbane, Australia: Queensland Department of Primary Industries, 115-128.

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Deus Eda Gde, Pinheiro Ldos S, Lima CR, Sousa Mdo SMde, Guimarães JA, Strikis PC, Adaime R, 2013. Wild hosts of frugivorous dipterans (Tephritidae and Lonchaeidae) and associated parasitoids in the Brazilian Amazon. Florida Entomologist, 96(4):1621-1625. http://www.fcla.edu/FlaEnt/

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Enkerlin D, Garcia RL, Lopez F, 1989. Mexico, Central and South America. In: Fruit flies: their biology, natural enemies and control, vol. A (World crop pests; 3A) [ed. by Robinson AS, Hooper G] Amsterdam, Netherlands: Elsevier Science Publishers B. V., 83-90.

EPPO, 1983. Data sheets on quarantine organisms. Set 6. EPPO Bulletin, 13(1). unnumbered.

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

Fletcher BS, 1989. Ecology; movements of tephritid fruit flies. In: Robinson AS, Hooper G, eds. Fruit Flies; Their Biology, Natural Enemies and Control. World Crop Pests, 3(B). Amsterdam, Netherlands: Elsevier, 209-219.

Foote RH, 1982. The Tephritidae (Diptera) of the Galapagos Archipelago. Memoirs of the Entomological Society of Washington, 10:48-55.

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Gonzalez BJ, Vargas VC, Jara PB, 1971. Estudios sobre la aplicacion de la tecnica de machos esteriles en el control de la mosca sudamericana de la fruta, Anastrepha fraterculus (Wied.). Revista Peruana de Entomologia, 14:66-86.

Harper JD, Escobar JS, Cereceda G, 1989. Collection of Anastrepha fraterculus on Santa Cruz Island, Galapagos Province, Ecuador. Florida Entomologist, 72(1):205-206

Hedstrom I, Jimenez J, 1988. Field evaluation of attractants in the capture of Anastrepha spp. (Diptera, Tephritidae), pests of fruit trees in tropical America. II. Ammonium acetate and torula with sodium borate. Revista Brasileira de Entomologia, 32(2):319-322.

Hedström I, Jirón LF, 1985. Field evaluation of attractants in the trapping of Anastrepha spp. (Diptera, Tephritidae), pests of fruit trees in tropical America. I. Molasses and torula yeast. Revista Brasileira de Entomologia, 29(3/4):515-520.

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Lima IS de, Howse PE, Salles LAB, 1994. Reproductive behaviour of the South American fruit fly Anastrepha fraterculus (Diptera: tephritidae): laboratory and field studies. Physiological Entomology, 19(4):271-277

Loiacono MS, 1981. Notes on Neotropical Diapriinp (Hymenoptera, Diapriidae). Revista de la Sociedad Entomologica Argentina, 40(1/4):237-241

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Links to Websites

Contributors

27/02/2008 Updated by:

Allen Norrbom, Systematic Entomology Laboratory, USDA, c/o National Museum of Natural History, MRC 168, PO Box 37012, Washington, DC 20013-7012, USA

Distribution Maps

• = Present, no further details
• = Evidence of pathogen
• = Widespread
• = Last reported
• = Localised
• = Presence unconfirmed
• = Confined and subject to quarantine
• = See regional map for distribution within the country
• = Occasional or few reports

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