EPPO Global Database

Rhagoletis indifferens(RHAGIN)

EPPO Datasheet: Rhagoletis indifferens

Last updated: 2021-10-21

IDENTITY

Preferred name: Rhagoletis indifferens
Authority: Curran
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Diptera: Tephritidae
Other scientific names: Rhagoletis cingulata indifferens Curran
Common names in English: western cherry fruit fly
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Notes on taxonomy and nomenclature

Rhagoletis indifferens and R. cingulata (Loew) are very closely related allopatric species, occurring respectively in the western and eastern parts of North America. Before 1966, only R. cingulata was generally recognized, and most pre-1966 literature did not make any distinction between the two species, even though distinct morphological differences between flies from the east and west were recognized in 1955 (Blanc & Kiefer, 1955). As a result, all records of R. cingulata in western North America refer to R. indifferens.

EPPO Categorization: A1 list
EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: RHAGIN

HOSTS 2021-10-08

The principal cultivated hosts of R. indifferens are sweet cherry (Prunus avium) and tart cherry (P. cerasus). The native host of the fly is bitter cherry (Prunus emarginata) (Curran, 1932; Foote & Blanc, 1963; Bush 1966; Yee et al., 2011, 2015a). Cherry plum (Prunus cerasifera), cherry laurel (Prunus laurocerasus), mahaleb cherry (Prunus mahaleb), and bird cherry (Prunus padus) are also host plants that appear commonly attacked. Rare hosts are black hawthorn (Crataegus douglasii), cascara buckthorn (Frangula purshiana), Chinese crab apple (Malus spectabilis), apricot (Prunus armeniaca), and chokecherry (Prunus virginiana). Pin cherry (Prunus pensylvanica), Japanese plum (Prunus salicina), and Klamath plum (Prunus subcordata) are also host plants, but how commonly they are attacked is unclear (Frick et al., 1954; Ellertson, 1961; Yee, 2008; Yee & Goughnour, 2005a; 2008; Yee & Klaus, 2013; Yee et al., 2010; 2018a). In the EPPO region, P. avium and P. salicina would be the main potential hosts. Under laboratory conditions, R. indifferens oviposits in and larvae can develop in mango (Mangifera indica), common plum (Prunus domestica), and nectarine (Prunus persica) (Yee & Goughnour, 2017a).

Host list: Crataegus douglasii, Frangula purshiana, Malus spectabilis, Prunus armeniaca, Prunus avium, Prunus cerasifera, Prunus cerasus, Prunus emarginata, Prunus laurocerasus, Prunus mahaleb, Prunus padus, Prunus salicina, Prunus subcordata, Prunus virginiana

GEOGRAPHICAL DISTRIBUTION 2021-10-08

Rhagoletis indifferens is found in western North America, from California in the United States north to British Columbia, Canada (Bush, 1966; Yee et al., 2014a). According to Foote et al. (1993), R. indifferens is found in nine states in the United States: California, Colorado, Idaho, Montana, New Mexico, Oregon, Utah, Washington, and Wyoming. In the Pacific Northwest states of Washington and Oregon where the sweet cherry industry in the United States is concentrated, the fly is found almost exclusively in bitter cherry or in unmanaged sweet and tart cherry trees in yards and roadsides, and not in commercial orchards, which if properly managed are usually free of the fly (Smith 2005). Previous records of R. indifferens in the EPPO region were based on misidentifications of R. cingulata (Augustinos et al., 2019).

North America: Canada (British Columbia), United States of America (California, Colorado, Idaho, Montana, New Mexico, Oregon, Utah, Washington)

BIOLOGY 2021-10-08

Eggs are laid below the skin of the host fruit and, in cherries, hatch after 5-8 days (Frick et al., 1954). Larvae feed exclusively inside fruit. The first instar stage lasts 2-5 days; the second instar averages 4 days; the third instar averages 8 days. Pupariation is in the soil under the host plant, where puparia overwinter. A prolonged chilling period is required to terminate diapause and for pupae to develop into adults. Adults eclose from puparia in soil in late spring or summer. Flies feed indiscriminately on leaf and fruit surfaces, ingesting leachates that may contain sugars, bacteria, yeasts, amino acids, and minerals. Males use fruit as territories for mating (there is no true courtship) and defend them against other males. Females reach reproductive maturity and begin ovipositing about 1 week post-eclosion. Adult R. indifferens may live 15-30 days under field conditions in central Washington (Frick et al., 1954).

DETECTION AND IDENTIFICATION 2021-10-08

Symptoms 

Attacked cherries have punctures caused by stinging by the females’ ovipositor. In advanced stages of larval infestation, cherries become discolored and soft. Larval respiration holes and exit holes are commonly seen when larvae are at the third instar stage or have left fruit, respectively. 

Morphology 

Separation of R. indifferens and R. cingulata larvae and adults (Blanc and Kiefer 1955, Bush, 1966) is difficult morphologically and should be referred to a specialist. 

Egg

The egg is white and elongated.

Larva 

Larvae are whitish or creamy, legless, maggot-like and the last instar is about 8 mm long, see Phillips (1946) and Frick et al. (1954). Rhagoletis indifferens larvae can be separated from R. cingulata larvae by the numbers of papillae on the thoracic spiracles, with R. indifferens having 10-18 while R. cingulata has 21-31; in addition, R. indifferens larvae have a single row of papillae while R. cingulata larvae have at least two rows (Blanc and Kiefer 1955). 

Adult 

Adult females average about 5.2 mm in length with a wingspan of 3.7 mm while males average 4.4 mm in length with a wingspan of 3.3 mm (Yee et al., 2011).

Head: Three pairs of frontal setae; genae usually less than one-quarter eye height; ocellar setae long, usually similar in length and strength to orbital setae; two pairs of orbital setae; 1st flagellomere usually with a small antero-apical point. 

Thorax: Scutum predominantly black, with four longitudinal bars of tomentum that form grey stripes; scutum with dorsocentral setae based close to a line between the anterior supra-alar setae; scutum with dorsocentral setae and presutural supra-alar setae; anatergite without long pale hairs, at most with a fine pubescence; scutellum flat and with four marginal setae (one basal and an apical pair), black at base and sides, with basal and lateral black areas broadly joined; basal scutellar setae based well within black area.

Black shading on the posterior surface of coxa I separates R. indifferens from R. cingulata adults and all other members of the cingulata species group (Bush, 1966). 

Wing: Vein Sc abruptly bent forward at nearly 90°, weakened beyond this bend and ending at subcostal break; vein R1 with dorsal setulae; vein R4+5 usually without dorsal setulae, except sometimes at the base of the vein (except in some aberrant individuals); apex of vein M meeting C with a distinct angle; cup extension short, never more than one-fifth as long as vein A1+Cu2, and vein CuA2 straight along anterior edge of cup extension; cell cup always considerably broader than half depth of cell bm, and usually about as deep as cell bm; cells r1 and r2+3 without any markings between the discal and preapical crossbands; apical crossband usually only divided at apex, leaving an oblique hyaline stripe across the apex of cell r4+5; apical cross band adjoining vein C. Length 3-4 mm. 

Rhagoletis indifferens usually has no apical wing spot (found in only 1.4% of individuals) while R. cingulata usually has an apical wing spot (present in 65.8% to 75.8% of individuals) (Bush, 1966). 

Abdomen: Predominantly black; female with an ovipositor (aculeus) about 0.83 mm long (Bush, 1966) that is shorter than the wing length, and straight. 

Detection and inspection methods

Traps already in use within the EPPO region for the European cherry fruit fly R. cerasi should be suitable for monitoring any invasion of R. indifferens. These traps capture both sexes and are based on visual, or visual plus odour, attraction. They are coated with sticky material. Traps are usually either flat-surfaced and coloured various shades of yellow (panels) to elicit a supernormal foliage response, or spherical and dark-coloured to represent a fruit. The odour comes from protein hydrolysate or other substances emitting ammonia, such as ammonium acetate or carbonate. Burditt (1988) evaluated different traps for R. indifferens in British Columbia, Canada, and Yee (2013, 2014b, 2016, 2017b, 2018b, 2019) has evaluated traps against R. indifferens in Washington State in the USA.

PATHWAYS FOR MOVEMENT 2021-10-08

Adult flight and the transport of infested fruits are probably the major means of movement and dispersal of R. indifferens to previously non-infested areas. However, in general, R. indifferens is not known to fly long distances. In mark-release-recapture studies in Washington State, R. indifferens dispersed 67 m to 171 m (Frick et al., 1954; Jones & Wallace, 1955). In British Columbia, 96% of released R. indifferens were captured within 100 m of their release point (Senger, 2007). In international trade, the major means of dispersal to previously non-infested areas is presumably the transport of fruits containing live larvae. There may also be a risk from the transport of puparia in soil or packaging with plants that have borne fruit. R. cingulata, another cherry fruit fly originating in the Eastern USA, has been introduced and spread into Europe in the 2000s (EFSA PLH Panel, 2014).

PEST SIGNIFICANCE 2021-10-12

Economic impact

Rhagoletis indifferens is an important quarantine pest of cherries in western North America. Quarantine agreements between the Pacific Northwest states and other US states or countries result in a zero tolerance for cherry fruit fly larvae in packed fruit, leading to rejection of an entire load when a larva is found. The fly is mostly found in unmanaged sweet and sour cherry trees and not in commercial orchards where pest management is applied (Smith, 2005; Yee et al., 2014a).

Control 

Control procedures already established in the EPPO region for R. cerasi and R. cingulata are similar to those used against R. indifferens and could therefore be implemented against any introduction of this species within the EPPO region. If possible, wild and abandoned host plants near commercial cherry orchards should also be removed. Organophosphates, such as malathion and dimethoate, have long been known to be highly effective, killing eggs, larvae and/or adults of R. indifferens (Zwick et al., 1970; 1975). Spinosad in baits and other insecticides have been identified that are highly toxic to R. indifferens (e.g., Yee, 2009; 2010; 2015b; 2020a; Yee & Alston, 2006; 2012) and have been successful in managing the fly (Yee & Alston, 2006). Biological control agents against R. indifferens have also been studied in the laboratory, focusing on nematodes and fungi (Yee, 2003; 2005b; 2020b; Cossentine et al., 2011). These agents have shown promise although their efficacies have yet to be demonstrated in the field. 

To reduce the probability of pest presence in traded fruits, in the Pacific Northwest of the USA, cherries are checked for larvae at the packinghouses before fruit are shipped using the brown sugar flotation method, which has been shown to be highly efficacious in detecting larvae (Yee, 2012; 2014c).

Phytosanitary risk 

R. indifferens is a damaging fruit fly in North America and Prunus species are important crops in the EPPO region. Considering the pest current range in North America, it is likely that this species could establish in part of the EPPO region. Although control measures already applied against other fruit flies in cherry production may limit its impact, it may be needed to adapt IPM procedures to cover a longer period of infestation.

PHYTOSANITARY MEASURES 2021-10-08

Consignments of cherries (Prunus avium, P. cerasus) from regions where R. indifferens occurs should be inspected for symptoms of infestation and those suspected should be cut open in order to look for larvae. Fruits should come from areas where R. indifferens does not occur, or from a place of production found free from the pest by regular trapping before harvest in addition to use of the brown sugar flotation method post-harvest at the packinghouse. Cherries may also be treated effectively using methyl bromide to kill eggs and larvae (Jones & Schuh, 1953; USDA, 2021), but this may reduce cherry shelf life. Irradiation (Burditt & Hungate, 1988) and combined heat and controlled atmosphere treatments (Neven & Rehfield-Ray, 2006) are also effective at controlling R. indifferens in cherries. Similar measures may be considered for fruit of other host plants, but those species either produce fruits that are not widely traded (e.g. P. cerasifera, P. salicina) or are rarely attacked. 

Plants of host plant species transported with roots from regions where R. indifferens occurs should be free from soil. Such plants (see host list) may be prohibited from importation.

REFERENCES 2021-10-08

Augustinos AA, Moraiti CA, Drosopoulou E, Kounatidis I, Mavragani-Tsipidou P, Bourtzis K, Papadopoulos NT (2019) Old residents and new arrivals of Rhagoletis species in Europe. Bulletin of entomological research 109(6),701-712.

Blanc FL, Kiefer HH (1955) The cherry fruit fly in North America. California Department of Agriculture Bulletin 44, 77–88.

Burditt AK Jr. (1988) Western cherry fruit fly (Diptera: Tephritidae): efficacy of homemade and commercial traps. Journal of the Entomological Society of British Columbia 85, 53–57. 

Burditt AK Jr, Hungate FP (1988) Gamma irradiation as a quarantine treatment for cherries infested by western cherry fruit fly (Diptera: Tephritidae). Journal of Economic Entomology 81, 859–862.

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. 

Cossentine J, Jaronski S, Thistlewood H, Yee W (2011) Impact of Metarhizium brunneum Petch Clavicipitaceae (Hypocreales) on pre-imaginal Rhagoletis indifferens (Diptera: Tephritidae) within and on the surface of orchard soil. Biocontrol Science and Technology 21, 1501–1505.

Curran CH (1932) North American Diptera, with notes on others. American Museum Novitates 526, 1–13.

EFSA PLH Panel (EFSA Panel on Plant Health) (2014) Scientific Opinion on the pest categorisation of Rhagoletis cingulata (Loew). EFSA Journal 12(10), 3854, 27 pp. https://doi.org/10.2903/j.efsa.2014.3854

Ellertson FE (1961) New host records for Rhagoletis cingulata indifferens in Oregon. The Pan-Pacific Entomologist 37, 116.

Foote RH, Blanc FL (1963) The fruit flies or Tephritidae of California. Bulletin of the California Insect Survey 7, 1–117. 

Foote RH, Blanc FL, Norrbom AL (1993) Handbook of the fruit flies of America north of Mexico. Comstock, Ithaca, USA. 

Frick KE, Simkover HG, Telford HS (1954) Bionomics of the cherry fruit flies in eastern Washington. Washington Agricultural Experiment Stations. Technical Bulletin 13, 66 pp.

Jones SC, Schuh J (1953) Fumigation tests with methyl bromide for control of cherry fruit fly eggs, larvae, and puparia. Journal of Economic Entomology 46, 916–917.

Jones SC, Wallace L (1955) Cherry fruit fly dispersion studies. Journal of Economic Entomology 48, 616–617.

Neven LG, Rehfield-Ray L (2006) Combined heat and controlled atmosphere quarantine treatments for control of western cherry fruit fly. Journal of Economic Entomology 99, 658–663.

Phillips VT (1946) The biology and identification of trypetid larvae. Memoirs of the American Entomological Society 12, 1–161. 

Senger SE (2007) The dispersal of the western cherry fruit fly Rhagoletis indifferens (Diptera: Tephritidae) in structured environments. Ph.D. Dissertation. Simon Fraser University.

Smith TJ (2005) Western cherry fruit fly (Rhagoletis indifferens {Curran}) and its management in the Pacific Northwest United States of America. https://extension.wsu.edu/chelan-douglas/agriculture/treefruit/pestmanagement/cherryfruitfly/ [accessed in October 2021

USDA (2021) Treatment Schedules T101-s-1 Cherry. Treatment Manual. USDA/APHIS, Frederick, USA. https://www.aphis.usda.gov/import_export/plants/manuals/ports/downloads/treatment.pdf [accessed in October 2021].

Yee WL, Lacey LA (2003) Stage-specific mortality of Rhagoletis indifferens (Diptera: Tephritidae) exposed to three species of steinernematid nematodes. Biological Control 27, 349–356

Yee WL, Goughnour RB (2005a) New hosts of western cherry fruit fly, Rhagoletis indifferens (Diptera: Tephritidae), and their relationship to life history characteristics of this fly. Annals of the Entomological Society of America 98, 703–710. 

Yee WL, Lacey LA (2005b) Mortality of different life stages of Rhagoletis indifferens (Diptera: Tephritidae) exposed to the entomopathogenic fungus Metarhizium anisopliae. Journal of Entomological Science 40, 167–177.

Yee WL, Alston, D.G. (2006) Effects of spinosad, spinosad bait, and chloronicotinyl insecticides on mortality and control of adult and larval western cherry fruit fly (Diptera: Tephritidae). Journal of Economic Entomology 99, 1722–1732. 

Yee WL (2008) Host plant use by apple maggot, western cherry fruit fly, and other Rhagoletis species (Diptera: Tephritidae) in central Washington state. The Pan-Pacific Entomologist 84, 163–178. 

Yee WL, Goughnour RB (2008) Host plant use by and new host records of apple maggot, western cherry fruit fly, and other Rhagoletis species (Diptera: Tephritidae) in western Washington state. The Pan-Pacific Entomologist 84, 179–193.

Yee WL (2009) Insecticide, sugar, and diet effects on feeding and mortality in Rhagoletis indifferens (Dipt., Tephritidae). Journal of Applied Entomology 133, 297–306. 

Yee WL, Thistlewood HMA, Klaus MW (2010) Infestation of apricot by Rhagoletis indifferens Curran (Diptera: Tephritidae) in Washington state and British Columbia. The Pan-Pacific Entomologist 86, 100–103

Yee WL (2010) Oviposition in sweet cherry by reproductively mature western cherry fruit fly (Diptera: Tephritidae) fed spinosad and neonicotinoid baits. Journal of Economic Entomology 103, 379–385.

Yee WL, Goughnour RB, Feder JL (2011) Differences in body size and egg loads of Rhagoletis indifferens (Diptera: Tephritidae) from introduced and native cherries. Environmental Entomology 40, 1353–1362. 

Yee WL (2012) Detection of Rhagoletis indifferens (Dipt., Tephritidae) larvae using brown sugar flotation and hot water methods. Journal of Applied Entomology 136, 549–560. 

Yee WL, Alston DG (2012) Behavioral responses, rate of mortality, and oviposition of western cherry fruit fly exposed to malathion, zeta-cypermethrin, and spinetoram. Journal of Pest Science 85, 141–151.

Yee WL (2013) Captures of Rhagoletis indifferens (Diptera: Tephritidae) and non-target insects on red spheres versus yellow spheres and panels. Journal of Economic Entomology 106, 2109–2117.

Yee WL, Klaus MW (2013) Development of Rhagoletis indifferens Curran (Diptera: Tephritidae) in crabapple. The Pan-Pacific Entomologist 89, 18–26. 

Yee WL, Hernandez-Ortiz V, Rull J, Sinclair BJ, Neven LG (2014a) Status of Rhagoletis (Diptera: Tephritidae) pests in the NAPPO countries. Journal of Economic Entomology 107, 11–28. 

Yee WL (2014b) Commercial yellow sticky strips more attractive than yellow boards to western cherry fruit fly (Dipt., Tephritidae). Journal of Applied Entomology 139, 293–301.

Yee WL (2014c) Comparison of the brown sugar, hot water, and salt methods for detecting western cherry fruit fly (Diptera: Tephritidae) larvae in sweet cherry. Florida Entomologist 97, 422–430.

Yee WL, Goughnour RB, Hood GR, Forbes AA, Feder JL (2015a) Chilling and host plant/site-associated eclosion times of western cherry fruit fly (Diptera: Tephritidae) and a host-specific parasitoid. Environmental Entomology 44, 1029–1042. 

Yee WL (2015b) Temperature-mediated kill and oviposition of western cherry fruit fly (Diptera: Tephritidae) in the presence of spinosad. Journal of Economic Entomology 109, 132–142.

Yee WL (2016) Ammonium carbonate loss rates differentially affect trap captures of Rhagoletis indifferens (Diptera: Tephritidae) and non-target flies. The Canadian Entomologist 149, 241–250.

Yee WL, Goughnour RB (2017a) Development in mango (Mangifera indica) and other tropical and temperate fruit by Rhagoletis pomonella and R. indifferens (Diptera: Tephritidae) in the laboratory. Florida Entomologist 100, 157–161.

Yee WL (2017b) Attraction of Rhagoletis indifferens (Diptera: Tephritidae) to white light in the presence and absence of ammonia. Florida Entomologist 100, 21–28.

Yee WL, Liquido NJ, Santamaria J (2018a) Host plant records of the western cherry fruit fly, Rhagoletis indifferens Curran (Diptera: Tephritidae), Version 1.0. Available online at: USDA Compendium of Fruit Fly Host Information (CoFFHI), Edition 3.1, https://coffhi.cphst.org/ [accessed in October 2021].

Yee WL (2018b) Efficacies of Rhagoletis cerasi traps and ammonium lures for western cherry fruit fly (Diptera: Tephritidae). Journal of Insect Science 18, 1–8.

Yee WL (2019) Three-dimensional versus rectangular sticky yellow traps for western cherry fruit fly (Diptera: Tephritidae). Journal of Economic Entomology 112, 1780–1788. 

Yee WL (2020a) Evaluation of cyantraniliprole, spinetoram, and Chromobacterium subtsugae extract in bait for killing and reducing oviposition of Rhagoletis indifferens (Diptera: Tephritidae). Journal of Economic Entomology 113, 1356–1362. 

Yee WL (2020b) Laboratory evaluation of CX-10282 containing Beauveria bassiana (Hypocreales: Cordycipitaceae) strain GHA against adult Rhagoletis indifferens (Diptera: Tephritidae). Phytoparasitica 48, 231–245. 

Zwick RW, Jones SC, Peifer FW, Every RW, Smith RL, Thienes JR (1970) Malathion ULV aerial applications for cherry fruit fly control. Journal of Economic Entomology 63, 1693–1695.

Zwick RW, Fields GJ, Kiigemagi U (1975) Dimethoate for control of western cherry fruit fly on sweet cherry in Oregon. Journal of Economic Entomology 68, 383–385.

ACKNOWLEDGEMENTS 2021-10-08

This datasheet was prepared in 2021 by Wee L. Yee, USDA-ARS, Temperate Tree Fruit & Vegetable Research Unit, Wapato, USA. His valuable contribution is gratefully acknowledged.

How to cite this datasheet?

EPPO (2021) Rhagoletis indifferens. EPPO datasheets on pests recommended for regulation. Available online. https://gd.eppo.int

Datasheet history 2021-10-08

This datasheet was first published in the EPPO Bulletin in 1983 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2021. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1st and 2nd edition). CABI, Wallingford (GB).

EPPO (1983) Data sheets on quarantine organisms No. 41, Trypetidae (non-European). EPPO Bulletin 13 (1). https://doi.org/10.1111/j.1365-2338.1983.tb01715.x