Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Rhagoletis pomonella
(apple maggot)

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Datasheet

Rhagoletis pomonella (apple maggot)

Summary

  • Last modified
  • 27 September 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Natural Enemy
  • Preferred Scientific Name
  • Rhagoletis pomonella
  • Preferred Common Name
  • apple maggot
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Uniramia
  •         Class: Insecta
  • Summary of Invasiveness
  • R. pomonella is an important pest in apple production and its invasion of a new apple production area would have large economic and environmental impacts, both due to control efforts and likely export restriction...

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Pictures

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PictureTitleCaptionCopyright
Rhagoletis pomonella; adult fly on surface of an apple.
TitleAdult
CaptionRhagoletis pomonella; adult fly on surface of an apple.
CopyrightAndrew A. Forbes
Rhagoletis pomonella; adult fly on surface of an apple.
AdultRhagoletis pomonella; adult fly on surface of an apple.Andrew A. Forbes
Cross section of apples damaged by larval stages of Rhagoletis pomonella.
TitleDamaged fruit
CaptionCross section of apples damaged by larval stages of Rhagoletis pomonella.
CopyrightAndrew A. Forbes
Cross section of apples damaged by larval stages of Rhagoletis pomonella.
Damaged fruitCross section of apples damaged by larval stages of Rhagoletis pomonella. Andrew A. Forbes
Rhagoletis pomonella; adult fly on surface of an apple.
TitleAdult
CaptionRhagoletis pomonella; adult fly on surface of an apple.
CopyrightAndrew A. Forbes
Rhagoletis pomonella; adult fly on surface of an apple.
AdultRhagoletis pomonella; adult fly on surface of an apple.Andrew A. Forbes
Rhagoletis pomonella; close-up of thoracic region of an adult fly on surface of an apple.
TitleAdult
CaptionRhagoletis pomonella; close-up of thoracic region of an adult fly on surface of an apple.
CopyrightAndrew A. Forbes
Rhagoletis pomonella; close-up of thoracic region of an adult fly on surface of an apple.
AdultRhagoletis pomonella; close-up of thoracic region of an adult fly on surface of an apple.Andrew A. Forbes
Damaged apple with a 3rd instar Rhagoletis larvae (arrowed).
TitleDamaged fruit
CaptionDamaged apple with a 3rd instar Rhagoletis larvae (arrowed).
CopyrightAndrew A. Forbes
Damaged apple with a 3rd instar Rhagoletis larvae (arrowed).
Damaged fruitDamaged apple with a 3rd instar Rhagoletis larvae (arrowed).Andrew A. Forbes
Rhagoletis puparium with the parasitic Braconid wasp Diachasma alloeum emerging from it.  This species is a parasitoid of R. pomonella.  Adult wasps oviposit in third instar larvae of the fly. The eggs then develop after the larvae have pupated and the larval wasps then devour the fly larvae and overwinter inside the fly puparia.
TitleNatural enemy
CaptionRhagoletis puparium with the parasitic Braconid wasp Diachasma alloeum emerging from it. This species is a parasitoid of R. pomonella. Adult wasps oviposit in third instar larvae of the fly. The eggs then develop after the larvae have pupated and the larval wasps then devour the fly larvae and overwinter inside the fly puparia.
CopyrightAndrew A. Forbes
Rhagoletis puparium with the parasitic Braconid wasp Diachasma alloeum emerging from it.  This species is a parasitoid of R. pomonella.  Adult wasps oviposit in third instar larvae of the fly. The eggs then develop after the larvae have pupated and the larval wasps then devour the fly larvae and overwinter inside the fly puparia.
Natural enemyRhagoletis puparium with the parasitic Braconid wasp Diachasma alloeum emerging from it. This species is a parasitoid of R. pomonella. Adult wasps oviposit in third instar larvae of the fly. The eggs then develop after the larvae have pupated and the larval wasps then devour the fly larvae and overwinter inside the fly puparia. Andrew A. Forbes
Adult female
TitleLine artwork
CaptionAdult female
CopyrightCAB International
Adult female
Line artworkAdult femaleCAB International
Rhagoletis pomonella; Head capsule, orb s = orbital seta.
TitleLine artwork
CaptionRhagoletis pomonella; Head capsule, orb s = orbital seta.
CopyrightCAB International
Rhagoletis pomonella; Head capsule, orb s = orbital seta.
Line artworkRhagoletis pomonella; Head capsule, orb s = orbital seta.CAB International
Rhagoletis pomonella: Aculeus, dorsal view of apex.
TitleLine artwork
CaptionRhagoletis pomonella: Aculeus, dorsal view of apex.
CopyrightCAB International
Rhagoletis pomonella: Aculeus, dorsal view of apex.
Line artworkRhagoletis pomonella: Aculeus, dorsal view of apex.CAB International

Identity

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Preferred Scientific Name

  • Rhagoletis pomonella Walsh

Preferred Common Name

  • apple maggot

Other Scientific Names

  • Rhagoletis symphoricarpi
  • Spilographa pomonella (Walsh)
  • Trypeta pomonella
  • Zonosema pomonella (Walsh)

International Common Names

  • English: blueberry maggot; maggot, apple; railroad worm
  • Spanish: mosca de las manzanas
  • French: larve de la pomme; mouche de la pomme; ver-chemin-de-fer

Local Common Names

  • Denmark: Æbleflue
  • Germany: Apfelfliege; Apfelfruchtfliege; Fliege, Apfel-; Fruchtfliege, Apfel-
  • Italy: Mosca delle mele
  • Norway: epleflue
  • Sweden: Äpplefluga

EPPO code

  • RHAGPO (Rhagoletis pomonella)

Summary of Invasiveness

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R. pomonella is an important pest in apple production and its invasion of a new apple production area would have large economic and environmental impacts, both due to control efforts and likely export restrictions. R. pomonella is an important threat to apple production areas in temperate Europe, East Asia, and New Zealand that all lack apple-infesting tephritid pests. The only known invasion is the colonization of the West Coast of the USA with a recent spillover into parts of British Columbia. The means by which R. pomonella first arrived in the Pacific Northwest are speculative, but could range from natural spread via yet-undiscovered native populations to unintended human transport via larvae in infested fruit or pupae in soil. Its restricted host-use make the apple maggot an easier target for monitoring than extremely polyphagous species such as medfly [Ceratitis capitata], but its natural host, hawthorn [Crataegus monogyna] is widespread in all temperate environments both as a native and ornamental species and could provide a difficult-to-monitor reservoir.

Taxonomic Tree

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

Description

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Eggs

The eggs are elliptical, semi-opaque and creamy white, with both ends slightly yellow and more opaque, about 0.9 mm long and 0.23 mm wide.

Larvae

The legless larva when fully grown are usually 6.5-8 mm long and 1.5-2 mm wide at the widest point. The cream coloured body consists of 11 apparent segments.

Pupae

The oval, yellow-brown pupae are approximately 5 mm long and 2.3 mm wide.

Adults 

The adult is about 2-4 mm long, a little smaller than the housefly, easily recognizable by four irregular or zig-zag black bands on the wings with the three distal bands forming an F-shape. The body is generally black with a yellowish head and legs, and greenish eyes. The male has three white bands on the abdomen and the female has four similar white bands and is considerably larger. These characteristics do also describe other closely related Rhagoletis species. Apple maggots are members of a complex of cryptic species and adults cannot be diagnostically distinguished from these taxa by morphological characters alone (Berlocher, 2000). R. pomonella may be distinguished from the snowberry maggot, R. zephyria, in most but not all cases based on genital morphology (Westcot, 1982) and morphometric analyses may hold some promise for distinguishing R. pomonella from other taxa (Bi et al., 2007). But even detailed genetic studies have not revealed any fixed differences between R. pomonella and the blueberry maggot, R. mendax, and R. zephyria making the application of conventional barcoding improbable (Xie et al., 2008). Instead, using multilocus genotypes to assign single individual specimens of unknown taxonomic status to one of the described taxa holds the most promise (Schwarz et al., 2005; Michel et al., 2007).

 

Distribution

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In addition to the data in the Distribution table, this species is present in Alberta, Canada, where it is said to be 'very widespread in the Edmonton area' (Alberta Agriculture and Food, Canada: Alberta Insect Pest Report, 2006, archived document held by Alberta Agriculture and Food, Canada and CABI). See also CABI/EPPO (1998, No. 137).

An erroneous record of R. pomonella in Pakistan published in previous versions of the Compendium has been removed.

Distribution Table

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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.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

AfghanistanAbsent, invalid recordEPPO, 2014

North America

CanadaRestricted distributionEPPO, 2014
-British ColumbiaRestricted distributionIntroduced Invasive NAPPO, 2007; NAPPO, 2013; EPPO, 2014; NAPPO, 2015
-ManitobaPresentNative Not invasive EPPO, 2014
-New BrunswickPresentNative Not invasive EPPO, 2014
-Nova ScotiaPresentNative Not invasive EPPO, 2014
-OntarioPresentNative Not invasive EPPO, 2014
-Prince Edward IslandPresentNative Not invasive EPPO, 2014
-QuebecPresentNative Not invasive EPPO, 2014
-SaskatchewanPresentNative Not invasive EPPO, 2014
MexicoPresentNative Not invasive Rull et al., 2006; Muñiz-Reyes et al., 2011; EPPO, 2014Central Highland and Sierra Madre Oriental
USAWidespreadEPPO, 2014
-ArkansasPresentNative Not invasive EPPO, 2014
-CaliforniaWidespreadEPPO, 2014
-ColoradoWidespreadNative Not invasive EPPO, 2014
-ConnecticutWidespreadNative Not invasive EPPO, 2014
-DelawareWidespreadNative Not invasive EPPO, 2014
-FloridaWidespreadNative Not invasive EPPO, 2014
-GeorgiaWidespreadNative Not invasive EPPO, 2014
-IdahoPresentEPPO, 2014
-IllinoisWidespreadNative Not invasive EPPO, 2014
-IndianaWidespreadNative Not invasive EPPO, 2014
-IowaPresentEPPO, 2014
-KansasPresentEPPO, 2014
-MaineWidespreadNative Not invasive EPPO, 2014
-MarylandWidespreadNative Not invasive EPPO, 2014
-MassachusettsWidespreadNative Not invasive EPPO, 2014
-MichiganWidespreadEPPO, 2014
-MinnesotaWidespreadNative Not invasive EPPO, 2014
-MississippiWidespreadNative Not invasive EPPO, 2014
-MissouriWidespreadNative Not invasive EPPO, 2014
-MontanaPresentYee et al., 2015
-NebraskaPresentEPPO, 2014
-New HampshireWidespreadNative Not invasive EPPO, 2014
-New JerseyWidespreadNative Not invasive EPPO, 2014
-New YorkWidespreadNative Not invasive EPPO, 2014
-North CarolinaWidespreadNative Not invasive EPPO, 2014
-North DakotaWidespreadNative Not invasive EPPO, 2014
-OhioWidespreadNative Not invasive EPPO, 2014
-OregonWidespreadIntroduced1977 Invasive EPPO, 2014
-PennsylvaniaWidespreadNative Not invasive EPPO, 2014
-Rhode IslandWidespreadNative Not invasive EPPO, 2014
-South CarolinaWidespreadNative Not invasive EPPO, 2014
-South DakotaPresentNative Not invasive EPPO, 2014
-TexasWidespreadNative Not invasive EPPO, 2014
-UtahRestricted distribution Not invasive EPPO, 2014
-VermontWidespreadNative Not invasive EPPO, 2014
-VirginiaWidespreadNative Not invasive EPPO, 2014
-WashingtonPresentIntroduced Invasive EPPO, 2014; Mattsson et al., 2015
-West VirginiaWidespreadNative Not invasive EPPO, 2014
-WisconsinWidespreadNative Not invasive EPPO, 2014
-WyomingPresentEPPO, 2014

Central America and Caribbean

Costa RicaAbsent, unreliable recordEPPO, 2014

South America

ColombiaAbsent, unreliable recordEPPO, 2014

Europe

NetherlandsAbsent, confirmed by surveyNPPO of the Netherlands, 2013; EPPO, 2014

Oceania

New ZealandAbsent, confirmed by surveyEPPO, 2014

History of Introduction and Spread

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R. pomonella was first detected in Oregon (Portland area), USA in 1977 (Aliniazee and Penrose, 1981), but nothing is known about the introduction history. Following this initial detection, the apple maggot was subsequently also recorded in (and most likely spread to) Washington and California, USA and is now established in the fruit production areas of the Pacific Northwest. In 2006, it was recorded for the first time in British Columbia, Canada, which it presumably reached via natural spread from Washington, USA. So far the apple maggot has not been detected in the interior fruit production areas of that province. The apple maggot could have reached Oregon via unintended human transport (fruit or soil) or it could have spread from localized, to date unknown, native populations in hawthorn [Crataegus monogyna]. A detailed phylogeographic study is needed to elucidate the origin of the Northwestern apple maggots. While genetic data favours the hypothesis of an introduction (McPheron, 1990) in the Pacific Northwest, these former populations appear to be unrelated to isolated populations in Utah and Colorado, USA. The Utah and Colorado populations are strongly isolated from one another and could either be introductions or isolated native populations (McPheron, 1990).

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
British Columbia 2006 No No NAPPO (2007)
California >1977 Yes No
Colorado Yes No McPheron (1990) Could represent native population
Oregon 1977 Yes No Aliniazee and Penrose (1981)
Utah Yes No McPheron (1990) Could represent native population
Washington >1977 Yes No

Risk of Introduction

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R. pomonella has already shown its capacity to spread from its original range in eastern North America, to western states of the USA since 1979 (Foote et al., 1993) and it represents the most serious potential new tephritid pest for many apple producing temperate areas. Canada considers it as an internal quarantine pest (absent from the fruit-producing areas of British Columbia). R. pomonella is of quarantine significance for COSAVE, EPPO and OIRSA.

Consignments of apples from countries where R. pomonella 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 R. pomonella does not occur, or from a place of production found free from the pest by regular inspection for 3 months before harvest.

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

Fruits may also be treated, but specific treatment schedules have mostly not been developed for Rhagoletis spp. Chloropicrin, Telone II, and the two in combination could be used as fumigants for killing pupae and preventing emergence of R. pomonella. The following cold storage treatment is applied in Canada (http://www.inspection.gc.ca/plants/plant-protection/directives/horticulture/d-00-07/eng/1323819375916/1323819810662) for effective treatment of R. pomonella in apples:

Cold storage treatment

"The fruit was inspected at time of shipment and is apparently free of apple maggot and has been continuously maintained at a maximum temperature of 0.6°C (33°F) for a minimum of 42 days."

or

"The fruit was inspected at time of shipment and is apparently free of apple maggot and has been continuously maintained at a maximum temperature of 3.3°C (38°F) for a minimum of 90 days."

Irradiation

150 Gy irradiation (Follett et al., 2007); 57 Gy irradiation (Hallman, 2004). Significantly less is required if prevention of eclosion rather than prevention of pupation is desired (Hallman and Thomas, 1999). The USDA treatment manual requires 60 Gy minimum absorbed dose (USDA, 2012).

Habitat List

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CategoryHabitatPresenceStatus
Terrestrial-managed
Cultivated / agricultural land Present, no further details Harmful (pest or invasive)
Managed forests, plantations and orchards Present, no further details Harmful (pest or invasive)
Urban / peri-urban areas Present, no further details
Terrestrial-natural/semi-natural
Natural forests Present, no further details Natural

Hosts/Species Affected

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The main commercial host of R. pomonella is apple (Malus domestica), which was first introduced to eastern North America (New England) some 200 years before the first report of apple being attacked by this fly (Bush, 1966). The original native host of R. pomonella was almost certainly hawthorn (Crataegus spp.). Apple was introduced to Mexico in 1522, about 100 years earlier than to New England. Mexican and north-eastern USA populations on apple closely match regional varieties of wing patterning found in hawthorn-associated populations in those areas, indicating that colonization of apple probably occurred independently in each region (Bush, 1966, 1992). Recent studies have revealed strong geographic subdivison of Mexican R. pomonella populations by the trans-Mexican volcanic belt that could be interpreted as species-level differences. Populations in the Sierra Madre Oriental are more closely related to north American R. pomonella than to populations south-west of the volcanic belt (Rull et al., 2006; Michel et al. 2007). Apple fruits mature about 1 month earlier than those of hawthorn. Correspondingly, the apple race flies emerge about 1 month earlier than the hawthorn race flies and that severely limits the potential for gene flow between the races (Bush, 1969; Smith, 1988). Bush (1969) suggested that the populations on apples were initially founded by a few flies that emerged early and that within a few generations a race of early emerging flies with a preference for ovipositing on apples evolved in sympatry with the original hawthorn race. Similar variation is still evident in the response of both host races to host volatiles (Linn et al., 2005). During the relatively short period since the colonization of apple, the apple and hawthorn populations have diverged genetically to form distinct apple and hawthorn races ( Bush, 1969; McPheron et al., 1988b; Feder et al., 1989; 1990a; 1990b; Berlocher et al., 1993; Berlocher and McPheron, 1996). The two host races are also clearly differentiated by heritable preference for fruit volatiles of their natal hosts and active avoidance of non-natal host odours (Linn et al., 2003; Dambroski et al., 2005, Forbes et al., 2005).

R. pomonella is a serious pest of apple (Malus domestica), which is also recorded from Chickasaw plum (Prunus angustifolia), peach (Prunus persica) and Siberian crabapple (Malus baccata); larvae have also been found in pear (Pyrus communis), but no adults emerged (Bush, 1966). In New England (USA), R. pomonella utilizes the hips (fruits) of Japanese rose (Rosa rugosa) and R. carolina (as R. virginiana) as alternative hosts (Prokopy and Berlocher, 1980). Recently, R. pomonella has adapted to attacking apricot (Prunus armeniaca), chokeberry (Prunus virginiana), crabapple (Malus spp.), mahaleb (Prunus mahaleb), pyracantha (Pyracantha coccinea), ornamental hawthorn (Crataegus monogyna and C. mollis), plum (Prunus americana), river hawthorn (C. douglasii), sweet cherry (Prunus avium) and sour cherry (Prunus cerasus) in Utah (USA) where it has not been reported from cultivated apple (Jorgensen et al., 1986; McPheron et al., 1988a; Messina, 1989; Alldred and Jorgensen, 1993), and there is also a record from apricot in New York (USA) (Lienk, 1970). Ornamental hawthorns (Crataegus spp.) may also be attacked by the hawthorn race.

The major natural hosts from which the pest populations have evolved are hawthorns (Crataegus spp.); R. pomonella is also recorded from some Amelanchier, Aronia and Cotoneaster spp. (all Rosaceae) (Bush, 1966).

Records from rowan (Sorbus aucuparia) (Pickett and Neary, 1940) require confirmation. Records from black huckleberry (Gaylussacia baccata), cranberry (Vaccinium macrocarpon), cultivated plum (presumably P. domestica), highbush blueberry (Vaccinium corymbosum), lowbush blueberry (Vaccinium angustifolium), mountain cranberry (Vaccinium vitis-idaea), tomato (Lycopersicon esculentum) and wintergreen (Gaultheria procumbens) (Pickett, 1937; Pickett and Neary, 1940) were almost certainly based on misidentifications of Rhagoletis mendax and other species.

Rhagoletis flies with the taxonomic designation Rhagoletis pomonella that infest flowering dogwood (Cornus florida) are widespread throughout eastern North America. Flies on flowering dogwood, however, show strong genetic and behavioural isolation from apple- or hawthorn-infesting R. pomonella (Berlocher, 1999; Dambroski et al., 2005). Much less well documented is the 'mayhaw fly' that appears to be strongly temporally isolated from other R. pomonella flies by infesting spring fruiting Crataegus ser. aestivalis in the southeastern USA (Berlocher, 2000).

Host Plants and Other Plants Affected

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Plant nameFamilyContext
Amelanchier (serviceberries)RosaceaeWild host
Aronia (chockeberry)RosaceaeWild host
Cornus florida (Flowering dogwood)CornaceaeWild host
CotoneasterRosaceaeWild host
Cotoneaster apiculatusRosaceaeOther
Cotoneaster coriaceusRosaceaeOther
Cotoneaster integerrimusRosaceaeOther
Crataegus (hawthorns)RosaceaeWild host
Crataegus crus-galli (Cockspur hawthorn)RosaceaeWild host
Crataegus douglasii (black hawthorn)RosaceaeWild host
Crataegus laevigataRosaceaeWild host
Crataegus mollisRosaceaeOther
Crataegus monogyna (hawthorn)RosaceaeWild host
Crataegus suksdorfiiRosaceaeOther
Malus (ornamental species apple)RosaceaeOther
Malus baccata (siberian crab apple)RosaceaeOther
Malus domestica (apple)RosaceaeMain
Prunus (stone fruit)RosaceaeWild host
Prunus americana (American plum)RosaceaeOther
Prunus angustifolia (Mountain cherry tree)RosaceaeOther
Prunus armeniaca (apricot)RosaceaeOther
Prunus avium (sweet cherry)RosaceaeOther
Prunus cerasifera (myrobalan plum)RosaceaeOther
Prunus cerasus (sour cherry)RosaceaeOther
Prunus domestica (plum)RosaceaeOther
Prunus emarginata (Bitter cherry tree)RosaceaeOther
Prunus mahaleb (mahaleb cherry)RosaceaeOther
Prunus persica (peach)RosaceaeOther
Prunus salicina (Japanese plum)RosaceaeOther
Prunus virginiana (common chokecherrytree)RosaceaeOther
Pyracantha coccinea (Scarlet firethorn)RosaceaeOther
Pyrus communis (European pear)RosaceaeOther
Pyrus pyrifolia (Oriental pear tree)RosaceaeOther
Rosa (roses)RosaceaeWild host
Rosa rugosa (rugosa rose)RosaceaeOther
Rosa virginiana (Virginia rose)RosaceaeOther
Sorbus aucuparia (mountain ash)RosaceaeOther
Sorbus scopulinaRosaceaeOther
Vaccinium corymbosum (blueberry)EricaceaeOther

Growth Stages

Top of page Fruiting stage

Symptoms

Top of page R. pomonella burrow in all directions through the flesh of apples feeding on the pulp and leaving brown channels. When a single fruit is infested with several larvae, the pulp will be honeycombed with their burrows until it finally breaks down. Infested fruit are usually misshapen. Attacked fruit are pitted by oviposition punctures, around which some discoloration usually occurs.

List of Symptoms/Signs

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SignLife StagesType
Fruit / internal feeding

Biology and Ecology

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In most cases R. pomonella has only one generation a year, but diapause is facultative (Feder et al., 1997) and emergence without diapause by a small proportion of apple maggot pupae has been documented in the field (Chen et al., 2002). Females lay their eggs singly beneath the skin of the fruit. The larvae hatch 3-7 days later and tunnel into the fruit pulp. They complete their development within the fruit, taking anywhere from 2 weeks to several months to mature. Very rarely will larvae exit from hanging fruit. The infested fruit usually drops to the ground. Larvae remain in the dropped fruit until reaching maturity when they make an exit hole in the skin of the fruit and wriggle to the ground. Larval emergence from fruit may continue into early December. Larvae then enter the soil where pupation occurs. They enter the soil to a depth of 2-5 cm, usually beneath the host plant. Pupae stay dormant over winter, and they may persist in the soil for several years. Adult emergence is in late June or July and they may feed on insect honeydew and bird dung, reaching sexual maturity 7-10 days after emergence. As the flies mature and mate they respond more to oviposition-site stimuli, i.e. fruit shape and fruit odour (Prokopy and Papaj, 2000; Linn et al., 2003). After mating, a single female fly is capable of laying more than 200 eggs in her lifetime. Adults usually die after 3-4 weeks, but may live up to 40 days under field conditions.

Climate

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ClimateStatusDescriptionRemark
C - Temperate/Mesothermal climate Preferred Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C
Cf - Warm temperate climate, wet all year Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Cs - Warm temperate climate with dry summer Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Preferred Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)
D - Continental/Microthermal climate Preferred Continental/Microthermal climate (Average temp. of coldest month < 0°C, mean warmest month > 10°C)
Df - Continental climate, wet all year Preferred Continental climate, wet all year (Warm average temp. > 10°C, coldest month < 0°C, wet all year)
Ds - Continental climate with dry summer Tolerated Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)
Dw - Continental climate with dry winter Preferred Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
50 28 0 0

Air Temperature

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Parameter Lower limit Upper limit
Absolute minimum temperature (ºC) -40 0
Mean annual temperature (ºC) 0 21
Mean maximum temperature of hottest month (ºC) 21 37
Mean minimum temperature of coldest month (ºC) -20 15

Rainfall

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ParameterLower limitUpper limitDescription
Mean annual rainfall3803000mm; lower/upper limits

Rainfall Regime

Top of page Bimodal
Summer
Uniform
Winter

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Amara aenea Predator
Biosteres melleus Parasite Larvae
Carabidae Predator Larvae/Pupae
Diachasma alloeum Parasite Larvae
Diachasma ferrugineum Parasite
Formica fusca Predator
Harpalus affinis Predator
Opius downesi Parasite
Opius lectoides Parasite Larvae
Opius lectus Parasite Larvae
Phygadeuon wiesmanni Parasite Pupae Ontario apples
Pterostichus melanarius Predator
Salticidae Predator Adults
Trochosa terricola Predator

Notes on Natural Enemies

Top of page Up to 90% of larvae may be parasitized in Crataegus fruits (Gut and Brunner, 1994) in Washington State, USA. However, in a comparative study of parasitism levels in Crataegus and apple in Michigan, USA, Feder (1995) found only 46% and 13% parasitism, respectively. Allen and Hagley (1989) reviewed predators found in an orchard in Ontario, Canada, but indicated that the impact was probably very low.

Means of Movement and Dispersal

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Natural Dispersal

Self-propelled natural dispersal appears to be the likely mode for the spread of the apple maggot in the Pacific Northwest. In the absence of suitable hosts the long-lived adults (several weeks) can spread > 1 km in a single day if forced by the absence of suitable host fruit. Native or introduced hawthorns [Crataegus monogyna] could serve as reservoirs.

Accidental Introduction

No cases of introduction via accidental human transport have been reported. However, transport via infested fruit (commercial shipments or transport by individual travellers) or as pupae in soil via the nursery trade, are likely pathways.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Self-propelledPacific northwest Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Clothing, footwear and possessionsFruit in case or handbag. Yes
Containers and packaging - woodOf fruit cargo. Yes
Land vehiclesAeroplanes and boats, with fruit cargo. Yes
MailFruit in post. Yes
Soil, sand and gravelRisk of puparia in soil. Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Fruits (inc. pods) eggs; larvae Yes Pest or symptoms usually visible to the naked eye
Growing medium accompanying plants pupae Yes Pest or symptoms usually visible to the naked eye
Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Leaves
Roots
Seedlings/Micropropagated plants
Stems (above ground)/Shoots/Trunks/Branches
True seeds (inc. grain)
Wood

Impact Summary

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CategoryImpact
Economic/livelihood Negative
Environment (generally) Negative

Impact

Top of page R. pomonella, which primarily attacks apples, is the most serious fruitfly pest in North America, except for introductions of Ceratitis capitata (EPPO/CABI, 1996).

Economic Impact

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In principle, all major apple production areas outside the USA and eastern Canada are endangered by the introduction of the apple maggot. These include temperate regions in Europe, East Asia, New Zealand, and South America. Currently, at greatest risk are the interior apple-growing regions of British Columbia, due to their close spatial proximity to populations in the Pacific Northwest and reports from coastal British Columbia. Introduction overseas would have to occur via unintended transport by humans. The fact that such transport represents a real possibility has been documented by the recent establishment of the American cherry fruit fly, Rhagoletis cingulata, in Europe (EPPO, 2004).

The introduction of the apple maggot would necessitate the implementation of costly new monitoring and control programmes that could interfere with existing IPM programmes. Most importantly, the establishment of the apple maggot in any of the regions listed above is likely to have severe impacts on apple exports as other countries will implement quarantine regimes.

Impact: Biodiversity

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The apple maggot could potentially hybridize with other closely related species. This has been documented in the Pacific Northwest, where hybridization with the snowberry maggot occurred (McPheron, 1990). North American Rhagoletis form a distinct clade from old world or South American Rhagoletis and hybridization with native species in these areas appears to be less likely. The greatest danger in this respect would be the 'contamination' of the genetically distinct and geographically isolated populations of the 'Mexican pomonella', southwest of the Trans-Mexican Volcanic Belt, should 'Northern pomonella' be introduced into that area of Mexico (Michel et al., 2007).

Other environmental impacts would result from increased pesticide use, which is caused by chemical control of introduced apple maggot populations. Eradication attempts are also likely to include the local destruction of apple trees [Malus spp.] and native hawthorn [Crataegus monogyna] plants that could represent alternative hosts.

Social Impact

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The biggest social impacts would result from the economic costs resulting from control and loss of export markets. Human health impacts may result from chemical control efforts.

Risk and Impact Factors

Top of page Invasiveness
  • Invasive in its native range
  • Proved invasive outside its native range
  • Has a broad native range
  • Abundant in its native range
  • Highly adaptable to different environments
  • Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
  • Highly mobile locally
  • Benefits from human association (i.e. it is a human commensal)
  • Has high reproductive potential
  • Has propagules that can remain viable for more than one year
  • Has high genetic variability
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts livelihoods
  • Transportation disruption
Impact mechanisms
  • Herbivory/grazing/browsing
  • Parasitism (incl. parasitoid)
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Uses

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The apple maggot has been a prime study organism for the evolution of new specialist insect pests and basic questions of ecological speciation and adaptation of host specific herbivores and parasites (Berlocher and Feder, 2002). Its establishment in the Pacific Northwest has further provided an example for hybridization of an introduced species with a closely related native taxon (Rhagoletis zephyria, snowberry maggot) (McPheron, 1990). Should the apple maggot be introduced to another region, studying its potential adaptation to new hosts would be of great applied and general interest.

Uses List

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General

  • Research model

Detection and Inspection

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Traps that capture both sexes are based on visual attraction, or visual plus odour attraction. They are coated in sticky material and are usually either flat-surfaced and coloured fluorescent yellow to elicit a supernormal foliage response, or spherical and dark-coloured to represent a fruit; traps which combine both foliage and fruit attraction can also be used. The odour comes from protein hydrolysate or other substances emitting ammonia, such as ammonium acetate; for R. pomonella synthetic apple volatiles are also very effective attractants (Reissig et al., 1985; Stenlinski and Liburd, 2002). See Boller and Prokopy (1976) and Economopoulos (1989) for a discussion of these traps.

Prevention and Control

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Upon detection, fallen and infected fruit must be removed and destroyed. If possible, wild and abandoned host trees should also be destroyed. Boller and Prokopy (1976) noted that systemic organophosphates, such as dimethoate, are highly effective against most species, killing eggs, larvae and adults. Belanger et al. (1985) discussed the use of pyrethroids, but these were only of use when pest activity was low. More environmentally acceptable techniques have been tried; namely bait sprays (insecticide plus ammonia source) which can be applied as a spot treatment; soil application of insecticide to destroy pupae; juvenile hormone analogues which can be applied to the soil (Boller and Prokopy, 1976); pesticide-coated red spheres suspended on apple trees, which visually attract adult R. pomonella (Duan and Prokopy, 1995; Prokopy et al., 2005). However, it should be noted that bait sprays may not work well where natural sources of protein and ammonia abound, for example abundant bird droppings (Prokopy et al., 1993). Bait sprays containing Spinosad have been applied successfully more recently (Reissig, 2003; Pelz et al., 2005). An alternative to insecticide might be the application of kaolin clay films that interfere with visual host finding in the flies (Villanueva and Walgenbach, 2007). An IPM approach is now generally recommended for apple pests in North America (Prokopy et al., 1990), for example Trimble and Solymar (1997) described a programme for Ontario. Monitoring to facilitate IPM of R. pomonella and other apple pests can be facilitated by computer software such as Bugwatch (Yee and Yee, 1990). Averill and Prokopy (1987) demonstrated that the application of the oviposition deterrent pheromone of R. pomonella deterred oviposition for up to 3 weeks, provided it was not rain-washed. Biological control has so far not been successful (Boller and Prokopy, 1976; Wharton, 1989), and Van Driessche et al. (1987) concluded that, of 15 apple pests, R. pomonella was one of only two for which biological control had no potential. Behavioural management (use of oviposition detering pheromones, red spheres) is reviewed by Prokopy (1991).

References

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Aliniazee MT, Penrose RL, 1981. Apple maggot in Oregon: a possible new threat to the northwest apple industry. Bulletin of the Entomological Society of America, 27:245-246

Alldred DB, Jorgensen CD, 1993. Hosts, adult emergence, and distribution of the apple maggot (Diptera: Tephritidae) in Utah. Pan-Pacific Entomologist, 69(3):236-246; 35 ref

Allen WR, Hagley EAC, 1989. Epigeal arthropods as predators of mature larvae and pupae of the apple maggot (Diptera: Tephritidae). Environmental Entomology, 19(2):309-312

Averill AL, Prokopy RJ, 1987. Residual activity of oviposition-deterring pheromone in Rhagoletis pomonella (Diptera: Tephritidae) and female response to infested fruit. Journal of Chemical Ecology, 13(1):167-177

Belanger A, Bostanian NJ, Rivard I, 1985. Apple maggot (Diptera: Trypetidae) control with insecticides and their residues in and on apples. Journal of Economic Entomology, 78(2):463-466

Berlocher SH, 1999. Host race or species? Allozyme characterization of the 'flowering dogwood fly', a member of the Rhagoletis pomonella complex. Heredity, 83(6):652-662

Berlocher SH, 2000. Radiation and divergence in the Rhagoletis pomonella species group: inferences from allozymes. Evolution, 54(2):543-557

Berlocher SH, Feder JL, 2002. Sympatric speciation in phytophagous insects: moving beyond controversy? Annual Review of Entomology, 47:773-815

Berlocher SH, McPheron BA, 1996. Population structure of Rhagoletis pomonella, the apple maggot fly. Heredity, 77(1):83-99; 33 ref

Berlocher SH, McPheron BA, Feder JL, Bush GL, 1993. Genetic differentiation at allozyme loci in the Rhagoletis pomonella (Diptera: Tephritidae) species complex. Annals of the Entomological Society of America, 86(6):716-727

Bi C, Saunders MC, McPheron BA, 2007. Wing pattern-based classification of the Rhagoletis pomonella species complex using genetic neural networks. International Journal of Computer Science and Application, 4(3):1-14

Boller EF, Prokopy RJ, 1976. Bionomics and management of Rhagoletis. In: Smith RF, Mittler TE, Smith CN, ed. Annual review of entomology. Volume 21. Annual Reviews Inc. Palo Alto, California, USA, 223-246

Bush GL, 1966. The taxonomy, cytology and evolution of the genus Rhagoletis in North America (Diptera: Tephritidae). Bulletin of the Museum of Comparative Zoology, 134:431-526

Bush GL, 1969. Sympatric host formation and speciation in frugivorous flies of the genus Rhagoletis. Evolution, 23:237-251

Bush GL, 1992. Host race formation and sympatric speciation in Rhagoletis fruit flies (Diptera: Tephritidae). Psyche (Cambridge, Mass), 99(4):335-357

Chen H, Felland CM, McPheron BA, 2002. Population dynamics of apple maggot (Diptera: tephritidae) in south central Pennsylvania. Journal of Economic Entomology, 95(1):65-71

Dambroski HR, Linn C, Berlocher SH, Forbes AA, Roelofs W, Feder JL, 2005. The genetic basis for fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts. Evolution, 59(9):1953-1964

Driesche RG van, Prokopy RJ, Coli WM, 1987. Potential for increased use of biological control agents in Massachusetts apple orchards. Research Bulletin, Massachusetts Agricultural Experiment Station, No. 718:6-21

Duan JJ, Prokopy RJ, 1995. Development of pesticide-treated spheres for controlling apple maggot flies (Diptera: Tephritidae): pesticides and residue-extending agents. Journal of Economic Entomology, 88(1):117-126

Economopoulos AP, 1989. Control; use of traps based on color and/or shape. In: Robinson AS, Hooper G, eds. Fruit Flies; Their Biology, Natural Enemies and Control. World Crop Pests 3(B): 315-327. Amsterdam, Netherlands: Elsevier

EPPO, 2004. Rhagoletis cingulata occurs in the Netherlands, but not Rhagoletis indifferens. EPPO Reporting Service., 8. http://www.invasive.org/library/eppo/Rse-0406.pdf

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

FAO/IAEA, 2003. Trapping Guidelines for area-wide fruit fly programmes. Vienna, Austria: International Atomic Energy Agency, 47 pp

Feder JL, 1995. The effects of parasitoids on sympatric host races of Rhagoletis pomonella (Diptera: Tephritidae). Ecology, 76(3):801-813; 31 ref

Feder JL, Chilcote CA, Bush GL, 1989. Are the apple maggot, Rhagoletis pomonella, and blueberry maggot, R. mendax, distinct species? Implications for sympatric speciation. Entomologia Experimentalis et Applicata, 51(2):113-123

Feder JL, Chilcote CA, Bush GL, 1990. Regional, local and microgeographic allele frequency variation between apple and hawthorn populations of Rhagoletis pomonella in western Michigan. Evolution, 44(3):595-608

Feder JL, Chilcote CA, Bush GL, 1990. The geographic pattern of genetic differentiation between host associated populations of Rhagoletis pomonella (Diptera: Tephritidae) in the eastern United States and Canada. Evolution, 44(3):570-594

Feder JL, Roethele JB, Wlazlo B, Berlocher SH, 1997. Selective maintenance of allozyme differences among sympatric host races of the apple maggot fly. Proceedings of the National Academy of Sciences of the United States of America, 94(21):11417-11421

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

Follett PA, Yang ManMiao, Lu KuangHui, Chen TseWei, 2007. Irradiation for postharvest control of quarantine insects. Formosan Entomologist, 27(1):1-15

Foote RH, Blanc FL, Norrbom AL, 1993. Handbook of the Fruit Flies (Diptera: Tephritidae) of America North of Mexico. Ithaca, USA: Comstock

Forbes AA, Fisher J, Feder JL, 2005. Habitat avoidance: Overlooking an important aspect of host-specific mating and sympatric speciation? Evolution, 59(7):1552-1559

Gut LJ, Brunner JE, 1994. Parasitism of the apple maggot, Rhagoletis pomonella, infesting hawthorns in Washington. Entomophaga, 39(1):41-49

Hallman GJ, 2004. Irradiation disinfestation of apple maggot (Diptera: Tephritidae) in hypoxic and low-temperature storage. Journal of Economic Entomology, 97(4):1245-1248. http://www.esa.catchword.org

Hallman GJ, Thomas DB, 1999. Gamma irradiation quarantine treatment against blueberry maggot and apple maggot (Diptera: Tephritidae). Journal of Economic Entomology, 92(6):1373-1376; 11 ref

Jorgensen CD, Allred DB, Westcott RL, 1986. Apple maggot (Rhagoletis pomonella) adaptation for cherries in Utah. Great Basin Naturalist, 46(1):173-174

Lienk SE, 1970. Apple maggot infesting apricot. Journal of Economic Entomology, 63:1684

Linn C, Feder JL, Nojima S, Dambroski HR, Berlocher SH, Roelofs W, 2003. Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proceedings of the National Academy of Sciences of the United States of America, 100(20):11490-11493

Linn CE, Dambroski H, Nojima S, Feder JL, Berlocher SH, Roelofs WL, 2005. Variability in response specificity of apple, hawthorn, and flowering dogwood-infesting Rhagoletis flies to host fruit volatile blends: implications for sympatric host shifts. Entomologia Experimentalis et Applicata, 116(1):55-64

Mattsson M, Hood GR, Feder JL, Ruedas LA, 2015. Rapid and repeatable shifts in life-history timing of Rhagoletis pomonella (Diptera: Tephritidae) following colonization of novel host plants in the Pacific Northwestern United States. Ecology and Evolution, 5(24):5823-5837. http://onlinelibrary.wiley.com/journal/10.1002/(ISSN)2045-7758

McPheron BA, 1990. Genetic structure of apple maggot fly (Diptera: Tephritidae) populations. Annals of the Entomological Society of America, 83(3):568-577

McPheron BA, Jorgensen CD, Berlocher SH, 1988. Low genetic variability in a Utah cherry-infesting population of the apple maggot, Rhagoletis pomonella. Entomologia Experimentalis et Applicata, 46(2):155-160

McPheron BA, Smith DC, Berlocher SH, 1988. Genetic differences between host races of Rhagoletis pomonella. Nature (London), UK, 336(6194):64-67

Messina FJ, 1989. Host preferences of cherry- and hawthorn-infesting populations of Rhagoletis pomonella in Utah. Entomologia Experimentalis et Applicata, 53(1):89-95

Michel AP, Rull J, Aluja M, Feder JL, 2007. The genetic structure of hawthorn-infesting Rhagoletis pomonella populations in Mexico: implications for sympatric host race formation. Molecular Ecology, 16(14):2867-2878

Muñiz-Reyes E, Lomelí-Flores JR, Sánchez-Escudero J, 2011. Native parasitoids of Rhagoletis pomonella Walsh (Diptera: Tephritidae) in hawthorn in central Mexico. (Parasitoides nativos de Rhagoletis pomonella Walsh (Diptera: Tephritidae) en tejocote Crataegus spp. en el centro de México.) Acta Zoologica Mexicana, 27(2):425-440. http://www1.inecol.edu.mx/azm/AZM27(2)-2011/15.-%20Muniz-Reyes.pdf

NAPPO, 2007. Update on Apple Maggot (Rhagoletis pomonella) in British Columbia, Canada. NAPPO Phytosanitary Alert System. Ottawa, Canada: North American Plant Protection Organization. http://www.pestalert.org/oprDetail.cfm?oprID=250

NAPPO, 2013. Phytosanitary Alert System: Apple Maggot Found in Prince George, British Columbia. NAPPO. http://www.pestalert.org/oprDetail.cfm?oprID=570

NAPPO, 2015. Phytosanitary Alert System: Rhagoletis pomonella (apple maggot) detected in West Kelowna, British Columbia. NAPPO. NAPPO. http://www.pestalert.org/oprDetail.cfm?oprID=638&keyword=Rhagoletis%20pomonella

Pelz KS, Isaacs R, Wise JC, Gut LJ, 2005. Protection of fruit against infestation by apple maggot and blueberry maggot (Diptera: Tephritidae) using compounds containing spinosad. Journal of Economic Entomology, 98(2):432-437

Pickett AD, 1937. Studies on the genus Rhagoletis (Trypetidae) with special reference to Rhagoletis pomonella (Walsh). Canadian Journal of Research, Series D, 15:53-75

Pickett AD, Neary ME, 1940. Further studies on Rhagoletis pomonella (Walsh). Scientific Agriculture, 20:551-556

Prokopy RJ, 1991. Behavioral management of apple maggot flies: an update. Proceedings - Annual Meeting Massachusetts Fruit Growers' Association Inc., 97:107-110

Prokopy RJ, Berlocher SH, 1980. Establishment of Rhagoletis pomonella (Diptera: Tephritidae) on rose hips in southern New England. Canadian Entomologist, 112(12):1319-1320

Prokopy RJ, Cooley SS, Galarza L, Bergweiler C, 1993. Bird droppings compete with bait sprays for Rhagoletis pomonella (Walsh) flies (Diptera: Tephritidae). Canadian Entomologist, 125(3):413-422

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Yee WL, Lawrence TW, Hood GR, Feder JL, 2015. New records of Rhagoletis Loew, 1862 (Diptera: Tephritidae) and their host plants in western Montana, U.S.A. Pan-Pacific Entomologist, 91(1):39-57. http://www.bioone.org/doi/full/10.3956/2014-91.1.039

Links to Websites

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WebsiteURLComment
Parasitoids of Fruit-Infesting Tephritidaehttp://hymenoptera.tamu.edu/paroffit

Contributors

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05/02/2008 Updated by:

Dietmar Schwarz, The Pennsylvania State University, Department of Entomology, 501 ASI Building, University Park, PA 16801, USA

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