Crop Protection Compendium report - cerasi (European cherry fruit ) Page 1 of 12

Crop Protection Compendium

Selected sections for: Rhagoletis cerasi (European cherry fruit fly) Identity Taxonomic Tree Notes on and Nomenclature Description Distribution Distribution Table Risk of Introduction Hosts/Species Affected Host Plants and Other Plants Affected Growth Stages Symptoms List of Symptoms/Signs Biology and Ecology Plant Trade Notes on Natural Enemies Natural enemies Impact Detection and Inspection Similarities to Other Species/Conditions Prevention and Control References Pictures

Datasheet Type(s): Pest

Identity

Preferred Scientific Name Rhagoletis cerasi Linnaeus

Preferred Common Name European cherry fruit fly

Other Scientific Names Musca cerasi Linnaeus Rhagoletis cerasi fasciata Rohdendorf Rhagoletis cerasi nigripes Rohdendorf Rhagoletis cerasi obsoleta Hering Rhagoletis obsoleta Hering Spilographa cerasi Tephritis cerasi Trypeta signata Meigen Urophora cerasorum Dufour Urophora liturata Robineau-Desvoidy Zonosema cerasi (L.)

International Common Names

English European cherry fly, fruit fly, cherry

Local Common Names

Denmark kirsebærflue

Finland kirsikkakärpänen

France mouche des cerises

Germany Fruchtfliege, Kirschen-, Kirschen-Fruchfliege, Kirschen-Made, Made, Kirschen-

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Italy mosca delle ciliege

Netherlands Kersenvlieg

Norway kirsebærflue

Spain mosca de la cereza

Sweden körsbärsfluga

Turkey kiraz sinegi

EPPO code RHAGCE (Rhagoletis cerasi)

Taxonomic Tree

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

Notes on Taxonomy and Nomenclature

The synonyms listed are mostly only of historical interest and have never been in regular use, at least since 1900. Some workers refer to R. obsoleta as a distinct species. These authors may well be describing a distinct species but the name obsoleta does not belong to such a distinct species and is a synonym of cerasi. The type specimen of R. cerasi obsoleta was collected at the same time and place as other specimens that Hering did identify as cerasi. Therefore the name obsoleta only refers to an aberrant form (lacking an accessory costal crossband), rather than a true species.

Populations associated with spp. used to be regarded as R. cerasi but are now known to be a distinct species, R. berberidis Jermy; see Kandybina (1977) for larval differences and

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Richter (1970) for adult differences.

Description Adult

The generally dark body (most other European species pale) and the form of the wing markings (the small mark across cells R1 and R2+3 [accessory costal crossband] is often absent in small individuals) and the lack of a basal dark mark on the scutellum, will separate this species from most others (R. berberidis being the exception).

Larva

Description of third-instar larva by M.M. Elson-Harris (White and Elson-Harris, 1994):

Larvae medium-sized, length 5.0-6.0 mm; width 1.2-1.5 mm.

Head: Stomal sensory organs rounded, with 2 small sensilla; preoral teeth large, sclerotised, with 6 strong sharply pointed teeth; oral ridges not discernible; mouthhooks heavily sclerotised, each with a long, slender curved apical tooth and a much smaller preapical tooth on concave surface. Thoracic and abdominal segments: T1 with 3-4 rows of spinules ventrally but none dorsally and laterally; T2 and T3 with 3-5 rows of spinules dorsally and ventrally, but none laterally; A1 with 2-3 rows dorsally and 4-5 rows ventrally; A2-A8 with very few spinules dorsally but 9-12 rows of stout spinules ventrally; A8 with intermediate lobes well developed.

Anterior spiracles: 12-16 tubules.

Posterior spiracles: Each spiracular slit 4-5 times as long as broad with a thin, sclerotised rima. Dorsal and ventral hair bundles of 6-7 long (about as long as a spiracular slit) sometimes branched hairs, lateral bundles of 3-5 similar hairs.

Anal area: Lobes large, protuberant, with a discontinuous row of small spinules anteriorly and a small concentration of spinules just below anal opening.

For description of genus, see data sheet on Rhagoletis.

Distribution R. cerasi has two races which are referred to as northern and southern. The southern race is found in Italy, Switzerland, southern Germany, south-western France and southern parts of Austria. The northern race is found north of those areas from the Atlantic to the Black Sea (CIE, 1989). There is a unidirectional incompatibility between the races, such that southern females and northern males are interfertile, but crosses between southern males and northern females are sterile (Boller et al., 1976; Boller, 1989). The recently established population in Crete provides an example of how the races can be identified. When southern males were crossed with Cretan females the eggs produced were all sterile, but northern males and Cretan females produced fertile eggs; the Cretan population therefore belongs to the northern race (Neuenschwander et al., 1983). The possibility of using this one way incompatibility as a basis for control (the incompatible technique) has been investigated (Boller et al., 1976; Blümel and Russ, 1989).

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Distribution Table

Last First Country Distribution Origin Invasive References Notes Reported Reported

ASIA Georgia (Republic Present, no CIE, 1989; of) further details EPPO, 2009 Iran Present, no CIE, 1989; further details EPPO, 2009 Kazakhstan Present, no Foote, 1984; further details EPPO, 2009 Kyrgyzstan Present, no Foote, 1984; further details EPPO, 2009 Tajikistan Present, no Foote, 1984; further details EPPO, 2009 Turkey Present, no Boller & Bush, further details 1974; EPPO, 2009 Turkmenistan Present, no Foote, 1984; further details EPPO, 2009 Uzbekistan Present, no Foote, 1984 further details Austria Present, no Boller & Bush, further details 1974; EPPO, 2009 Belgium Present, no EPPO, 2009 further details Bulgaria Present, no Boller & Bush, further details 1974; EPPO, 2009 Croatia Present, no Boller & Bush, further details 1974 Czechoslovakia Present, no EPPO, 2009 (former) further details Denmark Present, no Ravn et al., 1997 further details Estonia Present, no EPPO, 2009 further details France Present, no Boller & Bush, further details 1974; EPPO, 2009 Germany Present, no Boller & Bush, further details 1974; EPPO, 2009 Greece Present, no Boller & Bush, further details 1974; EPPO, 2009 -Crete Present, no EPPO, 2009 further details Hungary Present, no Boller & Bush, further details 1974; EPPO,

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2009 Italy Present, no Boller & Bush, further details 1974; EPPO, 2009 -Sardinia Present, no EPPO, 2009 further details -Sicily Present, no EPPO, 2009 further details Latvia Present, no Dirlbek, 1982; further details EPPO, 2009 Lithuania Present, no Dirlbek, 1982; further details EPPO, 2009 Moldova Present, no Kiskin et al., 1981 further details Netherlands Present, no Boller & Bush, further details 1974; EPPO, 2009 Norway Present, no Jaastad, 1994; further details EPPO, 2009 Poland Present, no Boller & Bush, further details 1974; EPPO, 2009 Portugal Present, no CIE, 1989; further details EPPO, 2009 Romania Present, no Beratlief et al., further details 1981; EPPO, 2009 Russian Federation Present, no EPPO, 2009 further details -Russia (Europe) Present, no EPPO, 2009 further details -Russia (Europe) Present, no EPPO, 2009 further details -Russia (Europe) Present, no EPPO, 2009 further details - Present, no Foote, 1984; further details EPPO, 2009 Serbia Present, no EPPO, 2009 further details Spain Present, no Boller & Bush, further details 1974; EPPO, 2009 Sweden Present, no EPPO, 2009 further details Switzerland Present, no Boller & Bush, further details 1974; EPPO, 2009 Ukraine Present, no Matvievskii, 1983; further details EPPO, 2009 Yugoslavia (Serbia Present, no Stamenkovic et and Montenegro) further details al., 1996a

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Risk of Introduction R. cerasi constitutes a serious plant quarantine risk to any cherry growing regions from which it is absent. Its absence from the UK suggests that it may have some undocumented climatic limits; plant quarantine measures alone are unlikely to account for its absence from the UK.

Hosts/Species Affected R. cerasi is the only serious tephritid pest in central and northern Europe and its status in different countries was reviewed by Fischer-Colbrie and Busch-Petersen (1989). Recorded hosts are black cherry (Prunus serotina), mahaleb cherry (P. mahaleb), sour cherry (P. cerasus) and sweet cherry (P. avium) (Hendel, 1927; Séguy, 1934; Thiem, 1934).

Some wild cherries (Prunus spp.) are reservoir hosts for R. cerasi. It may also attack wild (Lonicera spp.) (Hendel, 1927). The phenology of R. cerasi differs between cherry and honeysuckle associated populations (Haisch and Chwala, 1979) and the honeysuckle population is either a well differentiated host race or possibly a distinct species (G.L. Bush, University of Michigan, USA, personal communication, 1991).

Hendel (1927) also recorded it from berberis (Berberis vulgaris), but that was probably based on a misidentification of R. berberidis (White and Elson-Harris, 1994), which is a very similar looking species.

Records from Barbary matrimony vine (Lycium barbarum) and bilberry (Vaccinium myrtillus) (Phillips, 1946) were derived from 19th century data and are likely to have been based on casual observation rather than rearing; Thiem (1934) listed those plants as being free from attack.

Host Plants and Other Plants Affected

Plant name Context Lonicera xylosteum (Fly honeysuckle) Wild host Prunus avium (sweet cherry) Main Prunus cerasus (sour cherry) Main Prunus mahaleb (mahaleb cherry) Main Prunus serotina (black cherry) Main

Growth Stages

Fruiting stage

Symptoms Fruits attacked by R. cerasi will be pitted by oviposition punctures, around which some discoloration usually occurs.

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List of Symptoms/Signs

Sign Fruit internal feeding obvious exit hole

Biology and Ecology Eggs (ca 200) are laid below the skin of the host fruit (normally one per fruit) and they hatch after 6-12 days. The larvae usually feed for about 6 weeks. Pupariation is in the soil under the host plant and this is the overwintering stage. Adults may live for up to 1-2 months under field conditions (Christenson and Foote, 1960). In Serbia adult activity peaked in May-June (Stamenkovic et al., 1996a). The oviposition deterring pheromone was analysed by Aluja and Boller (1992a).

Plant Trade

Plant parts liable to carry the Pest Borne Borne Visibility of pest or pest in trade/transport stages internally externally symptoms eggs; Pest or symptoms usually Fruits (inc. pods) Yes No larvae visible to the naked eye Growing medium accompanying Pest or symptoms usually pupae Yes No plants 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

Notes on Natural Enemies The parasitoids of R. cerasi were studied and reviewed by Hoffmeister (1992) who showed that in cherry associated populations Phygadeuon wiesmanni had the greatest impact (up to 48% of puparia were parasitized). Parasitoid species only found in association with Lonicera populations of R. cerasi are Opius magnus, Halticoptera laevigata, Cremnodes atricapillus, Phaelophus unifasciatus and Trichopria cf. sociabilis (Hoffmeister, 1992).

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Natural enemies

Life Biological Biological Natural Enemy Type Specificity References Stages Control in control on Aneuropria Parasite foersteri Cremnodes Parasite Austria; Lonicera atricapillus Switzerland xylosteum Halticoptera Parasite Switzerland Lonicera laevigata xylosteum Opius magnus Parasite Larvae Italy Prunus mahaleb Opius Parasite Larvae rhagoleticola Phygadeuon Parasite Switzerland Lonicera elegans xylosteum Phygadeuon Parasite Pupae scaposus Phygadeuon Parasite Pupae wiesmanni

Impact R. cerasi is the only serious fruit fly pest in western and central Europe. In some cultivars of sweet cherry up to 80% of fruits may be attacked if not adequately controlled (Stamenkovic et al., 1996b).

Detection and Inspection Traps that capture both sexes and are based on visual, or visual plus odour, attraction are used. 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. Vertical traps are more effective than inverted 'V'-shaped tent traps (Casagrande et al., 1995). The odour comes from protein hydrolysate or other substances emitting ammonia, such as ammonium acetate. For further information, see Boller and Prokopy (1976) and Economopoulos (1989).

Similarities to Other Species/Conditions

R. berberidis has very similar looking adults and is best separated by knowledge of the host plant and, if possible, confirmed by the larval differences. It has distinct oral ridges (Kandybina, 1977).

The following separation of the adults derives from Richter (1970):

R. cerasi: Arista black; scutum with 3 microtrichose stripes (described by Richter as 3 brownish- grey coated stripes); apical band of wing extending back beyond vein M.

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R. berberidis: Arista yellow at base; scutum without microtrichose stripes (described as lustrous black without coating); apical band of wing not extending beyond vein M. [The lack of microtrichose stripes is likely to be an error based on only seeing poor quality specimens; these characters need checking against long reared series.]

A number of electrophoretic differences are apparent from the data given by Berlocher and Bush (1982).

Prevention and Control 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, killing eggs, larvae and adults. 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; and juvenile hormone analogues which can be applied to the soil (Boller and Prokopy, 1976).

Biological control has so far not been successful (Boller and Prokopy, 1976; Wharton, 1989). The host marking pheromone is a potential management tool (Aluja and Boller, 1992b) and the sterile insect technique has been tested in Austria with limited success (Russ, 1976).

References

Aluja M, Boller EF, 1992a. Host marking pheromone of Rhagoletis cerasi: foraging behaviour in response to synthetic pheromonal isomers. Journal of Chemical Ecology, 18(8):1299-1311

Aluja M, Boller EF, 1992b. Host marking pheromone of Rhagoletis cerasi: field deployment of synthetic pheromone as a novel cherry fruit fly management strategy. Entomologia Experimentalis et Applicata, 65(2):141-147

Beratlief C, Ionescu C, Mustatea D, 1981. Observations on the effectiveness of the visual traps in the monitoring of treatments against the cherry fly (Rhagoletis cerasi L.). Bulletin de l'Academie des Sciences Agricoles et Forestieres, No. 10:93-102

Berlocher SH, Bush GL, 1982. An electrophoretic analysis of Rhagoletis (Diptera: Tephritidae) phylogeny. Systematic Zoology, 31:136-155.

Blümel S, Russ K, 1989. Control; manipulation of races. In: Robinson AS, Hooper G, eds. Fruit ; Their Biology, Natural Enemies and Control. World Crop Pests, 3(B):387-389. Amsterdam, Netherlands: Elsevier.

Boller EF, 1989. Genetics; cytoplasmic incompatibility in Rhagoletis cerasi. In: Robinson AS, Hooper G, eds. Fruit Flies; Their Biology, Natural Enemies and Control. World Crop Pests, 3 (B):69-74. Amsterdam, Netherlands: Elsevier.

Boller EF, Bush GL, 1974. Evidence for genetic variation in populations of the European cherry

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fruit fly, Rhagoletis cerasi (Diptera:Tephritidae) based on physiological parameters and hybridization experiments. Entomologia Experimentalis et Applicata, 17(2):279-293

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.

Boller EF, Russ K, Vallo V, Bush GL, 1976. Incompatible races of European cherry fruit fly, Rhagoletis cerasi (Diptera: Tephritidae), their origin and potential use in biological control. Entomologia Experimentalis et Applicata, 20(3):237-247

Casagrande E, Molinari F, Cravedi P, Bertonazzi C, 1995. Evaluation of new attractants and traps for monitoring of the cherry fruit fly, Rhagoletis cerasi L. Bulletin OILB/SROP, 18(2):31-34

Christenson LD, Foote RH, 1960. Biology of fruit flies. Annual Review of Entomology, 5:171-192.

CIE, 1989. Rhagoletis cerasi (Linnaeus) [Diptera: Tephritidae] cherry fruit fly. CAB International Institute of Entomology, Distribution Maps of Pests, series A (Agricultural), (65), revised, 1-3. Wallingford, UK: CAB International.

Dirlbek J, 1982. Fruit-flies (Diptera, Tephritidae) from Latvia and Lithuania. (Part I: Subfamily Trypetinp). Folia Facultatis Scientiarum Naturalium Universitatis Purkynianp Brunensis, Biologia, 23(7):33-35

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, 2009. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. www.eppo.org.

Fischer-Colbrie P, Busch-Petersen E, 1989. Pest status; temperate Europe and west , In: Robinson AS, Hooper G, eds. Fruit Flies; Their Biology, Natural Enemies and Control. World Crop Pests, 3(A):91-99. Amsterdam, Netherlands: Elsevier.

Foote RH, 1984. Tephritidae (Trypetidae). In: Soos A, Papp L, eds. Catalogue of Palaearctic Diptera, 9. Budapest, Hungary: Akadémiai Kiadó, 66-149.

Haisch A, Chwala D, 1979. Host influence on the diapause of Rhagoletis cerasi Linnpus 1758. Bulletin SROP, 2:153-155

Hendel F, 1927. Part 49. Trypetidae. In: Lindner E , ed. Die Fliegen der Palaearktischen Region, 5 (1):1-221. Stuttgart, Germany.

Hoffmeister T, 1992. Factors determining the structure and diversity of parasitoid complexes in tephritid fruit flies. Oecologia, 89(2):288-297

Jaastad G, 1994. First registration of the cherry fruit fly, Rhagoletis cerasi (L.) in western

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Norway; distribution, size and origin of the population. Norwegian Journal of Agricultural Sciences, 8(3/4):203-214.

Kandybina MN, 1977. The larvae of fruit-flies (Diptera, Tephritidae). Keys to the fauna of the USSR No.114. Lichinki plodovykh mykh-pestrokrylok (Diptera, Tephritidae). Opredeliteli po faune SSSR 114. Leningrad, USSR: Nauka, 212 pp.

Kiskin PKh, Lazar' IS, 1981. Perfocartograms for the prognosis of pests of agricultural crops. In: Sem'yanov VP, ed. Noveishie dostizheniya sel'skokhozyaistvennoi entomologii (po materialam USh s"ezda VEO, Vil'nyus, 9-13 oktyabrya 1979 g.) Vilnius, Vsesoyunzoe Entomologicheskoe Obshchestvo USSR, 89-93

Matvievskii AS, 1983. The use of pesticides in orchards in the Ukraine. Zashchita Rastenii, No. 6:25

Neuenschwander P, Bigler F, Delucchi V, Michelakis S, 1983. Natural enemies of preimaginal stages of Dacus oleae Gmel. (Dipt., Tephritidae) in western Crete. I. Bionomics and phenologies. Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', 40:3-32.

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

Ravn HP, Rasmussen AN, Jensen J, 1997. Kirsebaerfluen - en "dognflue" eller den storste trussel mod produktion af sodkirsebaer? Gron Viden, Havebrug, No. 102.

Richter VA, 1970. Part 62. Tephritidae (Trypetidae), In: Bienko GyaBei, ed. Keys to the of the European part of the USSR. Opredeliteli po Faune SSSR, 103(5):132-172.

Russ R, 1976. Untersuchungen uber die praktische Anwendung der `SIT' (sterile insect technique) als Bekampfungsmethode gegen die Kirschfruchtfliege (Rhagoletis cerasi L.) in Osterreich. Pflanzenarzt, 29:56-58.

Séguy E, 1934. Faune de France. 28 DiptFres (BrachycFres) (Muscidae Acalypterae et Scatophagidae). Paris, France.

Stamenkovic S, Garic R, Stamenkovic T, Milenkovic S, Nicolic M, 1996b. Susceptibility of some sweet cherry cultivars to Rhagoletis cerasi L. (Diptera, Tephritidae). Proceedings of the international cherry symposium, Budapest, Hungary, 14-18 June 1993. Acta Horticulturae, 410:555-560.

Stamenkovic S, Milenkovic S, Stamenkovic T, 1996a. Population dynamics of Rhagoletis cerasi L. (Diptera, Tephritidae) in western Serbia. Proceedings of the international cherry symposium, Budapest, Hungary, 14-18 June 1993. Acta Horticulturae. 410:561-565.

Thiem, von H, 1934. BetrSge zur Epidemiologie und BekSmpfung der Kirschfruchtfliege (Rhagoletis cerasi L.). Arbeiten über Physiologische und Angewandte Entomologie aus Berlin- Dahlem, 1:7-79.

Wharton RH, 1989. Control; classical biological control of fruit-infesting Tephritidae, In: Robinson

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AS, Hooper G, eds. Fruit Flies; their Biology, Natural Enemies and Control. World Crop Pests 3 (B). Amsterdam, Netherlands: Elsevier, 303-313.

Pictures

Picture Title Caption Copyright Eggs AgrEvo

Larva AgrEvo

Adult AgrEvo

Date of report: 09/12/2010

© CAB International 2010

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