Rhagoletis completa (walnut husk fly)

Pictures

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Picture	Title	Caption	Copyright
Title Line drawing of adult R. completa Caption Copyright ©CABI BioScience	Line drawing of adult R. completa		©CABI BioScience

Identity

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Preferred Scientific Name

• Rhagoletis completa Cresson

Preferred Common Name

• walnut husk fly

Other Scientific Names

• Rhagoletis suavis completa Cresson
• Rhagoletis suavis var. completa Cresson

International Common Names

• English: husk maggot
• French: mouche des brous du noyer

Local Common Names

• : husk maggot
• Germany: Amerikanische Walnussschalen-Fliege; Fliege, Amerikanische Walnussschalen

EPPO code

• RHAGCO (Rhagoletis completa)

Taxonomic Tree

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

Notes on Taxonomy and Nomenclature

Top of page R. completa was originally described as a subspecies of R. suavis but these have been recognized as separate species since the 1930s (see Foote et al., 1993).

Description

Top of page Adult

Diagnostic features of the genus are as follows (characters extracted from key to North American genera of Tephritidae by Foote et al., 1993): Head with two pairs orbital setae; posterior pair reclinate. Gena with only short anterior setae. First flagellomere (third antennal segment) at least slightly pointed at the apex. Thorax with dorsocentral setae closer to level of anterior supra-alar setae than transverse suture. Scutellum not swollen or shiny. Wing with cells bm and bcu of similar depth; bcu with a short acute extension. Crossvein R-M near middle of cell dm.

This species may be identified using the Diptera key in the Crop Protection Compendium taxonomic identification aid. For full details of its separation from other North American species, see Foote et al. (1993).

The main features of R. completa are as follows: thorax and abdomen predominantly pale yellow to orange. Wing with a distinct subbasal crossband; discal and preapical crossbands usually separate. Mediotergite dark marked (either entirely dark brown or with a pair of brown stripes). For more comprehensive details see Foote et al. (1993).

Larva

Diagnosis of genus by Elson-Harris (White and Elson-Harris, 1994): Antennal sensory organ with a short basal segment and cone-shaped distal segment; maxillary sensory organ flat, with well defined sensilla surrounded by small cuticular folds; stomal sensory organ rounded, with a peg-like sensilla; large, preoral teeth near base of stomal sensory organ; no preoral lobes; oral ridges in 5-13 short, unserrated rows; no accessory plates. Stout spinules forming discontinuous rows on almost all segments. Anterior spiracles with 7-35 stout tubules. Posterior spiracular slits 3-8 times as long as broad, with 3-16 short, branched spiracular hairs. Anal lobes large, protuberant with well defined tubercles and sensilla.

There is no modern description of the larva of this species (in the sense of SEM studies being applied). However, Steyskal (1973) provided a key for the separation of the larvae of three species found in walnut. Any Rhagoletis larvae found in walnuts and having the following features is likely to be this species: 16-21 tubules, in each anterior spiracle; upper and lower slits of the posterior spiracles at about 60 degrees to each other. See key to larvae in White and Elson-Harris (1994), which used a combination of host and fragmentary morphological data.

Distribution

Top of page R. completa is native to southern and central USA; adventive in western USA since the 1920s (Bush, 1966). Also adventive in southern Europe since the early 1990s (Ciampolini and Trematerra, 1992; Merz, 1994; Seljak and Zezlina, 1999).

Harris (1989), Foote et al. (1993) and CABI (1997) all provide distribution maps.

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/Region	Distribution	Last Reported	Origin	First Reported	Invasive	Reference	Notes
North America
Mexico	Restricted distribution					Foote, 1981; CABI/EPPO, 2014; EPPO, 2014
USA	Present					CABI/EPPO, 2014; EPPO, 2014
-Arizona	Present					CABI/EPPO, 1997; CABI/EPPO, 2014; EPPO, 2014
-California	Present, few occurrences					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Colorado	Present					NHM, 1989; CABI/EPPO, 2014; EPPO, 2014
-Idaho	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Iowa	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Kansas	Present					Berlocher, 1984; Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Minnesota	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Mississippi	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Missouri	Present					CABI/EPPO, 2014; EPPO, 2014
-Nebraska	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Nevada	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-New Mexico	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Oklahoma	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Oregon	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Texas	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Utah	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
-Washington	Present					Foote et al., 1993; CABI/EPPO, 2014; EPPO, 2014
Europe
Austria	Present, few occurrences					CABI/EPPO, 2014; EPPO, 2014
Bosnia-Hercegovina	Present					Ostojic et al., 2014
Croatia	Present					Bjelis, 2008; CABI/EPPO, 2014; EPPO, 2014
France	Restricted distribution					EPPO, 2011a; CABI/EPPO, 2014; EPPO, 2014
Germany	Restricted distribution					CABI/EPPO, 2014; EPPO, 2014
Hungary	Restricted distribution					Tuba et al., 2012; IPPC, 2013; CABI/EPPO, 2014; EPPO, 2014
Italy	Restricted distribution					Ciampolini and Trematerra, 1992; CABI/EPPO, 2014; EPPO, 2014
Netherlands	Present, few occurrences					NPPO of the Netherlands, 2013; EPPO, 2014; EPPO, 2016; IPPC, 2016
Slovenia	Restricted distribution			1997		Seljak and Zezlina, 1999; CABI/EPPO, 2014; EPPO, 2014
Switzerland	Widespread			1986		Merz, 1994; CABI/EPPO, 2014; EPPO, 2014
UK	Absent, confirmed by survey					EPPO, 2014
Oceania
New Zealand	Absent, confirmed by survey					EPPO, 2014

Risk of Introduction

Top of page R. completa poses a small quarantine risk for temperate regions. However, now that it is established in Switzerland and Italy, this species has been removed from the European and Mediterranean Plant Protection Organization (EPPO) A1 list. However, there are no practical measures to prevent its spread and it is not considered to be a very important pest, so EPPO recently decided not to add it to its A2 list. It has not been individually considered to be a quarantine pest by any other Regional Plant Protection Organization.

Habitat

Top of page Areas with suitable hosts and climate.

Hosts/Species Affected

Top of page R. completa is mainly associated with Juglans species. It is also known to attack Prunus persica (peach) (Bush, 1966).

Host Plants and Other Plants Affected

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Plant name	Family	Context
Juglans californica (california walnut)	Juglandaceae	Main
Juglans hindsii (californian black walnut)	Juglandaceae	Main
Juglans nigra (black walnut)	Juglandaceae	Main
Juglans regia (walnut)	Juglandaceae	Main
Prunus persica (peach)	Rosaceae	Other

Growth Stages

Top of page Fruiting stage

Symptoms

Top of page Attacked fruit will be pitted by oviposition punctures, around which some discoloration usually occurs.

List of Symptoms/Signs

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Sign	Life Stages	Type
Fruit / discoloration
Fruit / extensive mould
Fruit / gummosis
Fruit / internal feeding
Fruit / lesions: black or brown
Fruit / lesions: scab or pitting
Fruit / obvious exit hole
Fruit / odour
Fruit / ooze

Biology and Ecology

Top of page Most Rhagoletis species have a similar biology as detailed by Christenson and Foote (1960): eggs are laid below the skin of the host fruit and hatch after 3-7 days; the larvae usually feed for 2-5 weeks; pupariation is in the soil under the host plant and this is the normal overwintering stage; adults may live for up to 40 days under field conditions. In Oregon, adults emerge from late June to mid-August or sometimes early September; peak oviposition is in late August (Kasana and Aliniazee, 1996).

For development rates at various temperatures see Kasana and AliNiazee (1994).

Natural enemies

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Natural enemy	Type	Life stages	Specificity	References	Biological control in	Biological control on
Biosteres sublaevis	Parasite	Larvae
Coptera occidentalis	Parasite
Trybliographa sp.	Parasite	Larvae

Notes on Natural Enemies

Top of page The braconid, Biosteres sublaevis, and a eucoilid of the genus Trybliographa, were found to cause varying degrees of natural parasitism in New Mexico (Legner and Goeden, 1987).

Means of Movement and Dispersal

Top of page Adult flight and the transport of infected fruit are the major means of movement and dispersal to previously uninfected areas. However, Rhagoletis species are not known to fly more than a short distance (Fletcher, 1989). In international trade, the major means of dispersal to previously uninfested areas is the transport of fruit containing live larvae. There is also a risk from the transport of puparia in soil or packaging with plants which have already fruited.

Pathway Vectors

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Vector	Notes	Long Distance	Local	References
Clothing, footwear and possessions	Fruit in case or handbag.	Yes
Containers and packaging - wood	Of fruit cargo.	Yes
Land vehicles	Lorries, aeroplanes and perhaps ships, with fruit cargo.	Yes
Mail	Fruit in post.	Yes
Soil, sand and gravel	Risk of puparia in soil.	Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transport	Pest stages	Borne internally	Borne externally	Visibility 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

Top of page In North America, R. completa is a pest of various Juglans species but it has rarely been recorded on European walnut (J. regia). In Switzerland, it attacks the mesocarp of J. regia, and in the case of severe infestation may also damage the pericarp and the nut itself (R. Mani, Switzerland [address available from CABI], personal communication, 2001). It therefore becomes a problem for walnut fruit production. In 1991, 50% of harvested walnuts in some Italian orchards were infested by R. completa (Ciampolini and Trematerra, 1992). In Oregon, Kasana and Aliniazee (1996) recorded up to 95% infestation on untreated trees.

In California it causes two types of damage. In populations causing normal or late-season infestations, larval feeding causes the whole husk or large portions of it to turn black, seriously reducing the value of nuts sold in the shell although the kernel is undamaged. Attack by populations involved in early infestations impedes the maturation of the kernel and results in shrivelled nuts or empty shells (Hislop et al., 1981).

Diagnosis

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EPPO (2011) describes a diagnostic protocol for R. completa infesting walnuts.

Detection and Inspection

Top of page Traps have been developed which capture both sexes, based on visual, 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 (see Riedl et al., 1989), or spherical and dark-coloured to represent a fruit (green spheres are best, see Riedl and Hislop, 1985); 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. See Boller and Prokopy (1976) and Economopoulos (1989) for a discussion of these traps.

Similarities to Other Species/Conditions

Top of page This species should not be mistaken for any other provided the diagnostic notes (see Morphology) are applied carefully. If in doubt consult Foote et al. (1993). R. suavis is an eastern USA species which is also associated with Juglans species, and in the past has been confused with R. completa (see Distribution Section).

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) note 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; and juvenile hormone analogues which can be applied to the soil (Boller and Prokopy, 1976). The IPM of walnut pests, including R. completa, was discussed by Haley and Baker (1982). Early harvest can be used to avoid attack (Yokoyama and Miller, 1996). Some varieties may be more susceptible to attack than others. Shelton and Anderson (1990) compared four varieties and found that Hartley suffered less damage than early leafing varieties.

Consignments of fruits from countries where these pests occur should be inspected for symptoms of infestation and those suspected should be cut open in order to look for larvae. European and Mediterranean Plant Protection Organization (EPPO) recommended (OEPP/EPPO, 1990), when only the North American origin was under consideration, that such fruits should come from an area where R. completa does not occur or from a place of production subject to growing season inspection. Fruits may also be treated in transit by cold treatment (for example, 40-42 days at -0.6°C) (FAO, 1983); however, Yokoyama and Miller (1996) found that low temperature storage could not be used as a quarantine treatment alone for some crops (e.g. walnuts) because the fly tolerated the treatment better than the host. Ethylene dibromide was previously widely used as a fumigant but is now generally withdrawn because of its carcinogenicity. Treatment methods against fruit flies are currently under review within EPPO and as part of an inter-RPPO programme.

Plants of host species transported with roots from countries where these pests occur should be free from soil, or the soil should be treated against puparia. The plants should not carry fruits. Such plants may indeed be prohibited from importation.

References

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Armstrong JW; Couey HM, 1989. Control; fruit disinfestation; fumigation, heat and cold. In: Robinson AS, Hooper G, eds. Fruit Flies; their Biology, Natural Enemies and Control. World Crop Pests. Amsterdam, Netherlands: Elsevier, 3(B):411-424.

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.

Bjelis M, 2008. Fruit flies from the family Rhagoletis (Tephritidae) in Croatia. (Vocne muhe iz roda Rhagoletis (Tephritidae) u Hrvatskoj.) Glasilo Biljne Zastite, 8(1):25-28.

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.

CABI/EPPO, 1997. Rhagoletis completa Cresson. Distribution Maps of Plant Pests, No. 337, rev. ed. Wallingford, UK: CAB International.

CABI/EPPO, 1998. Distribution maps of quarantine pests for Europe (edited by Smith IM, Charles LMF). Wallingford, UK: CAB International, xviii + 768 pp.

CABI/EPPO, 2014. Rhagoletis completa. [Distribution map]. Distribution Maps of Plant Pests, No.December. Wallingford, UK: CABI, Map 337 (2nd revision).

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

Ciampolini M; Trematerra P, 1992. Widespread occurrence of walnut fly (Rhagoletis completa Cresson) in northern Italy. Informatore Agrario, 48(48):52-56

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, 1990. Specific quarantine requirements. EPPO Technical Documents, No. 1008. Paris, France: European and Mediterranean Plant Protection Organization.

EPPO, 2011. EPPO Reporting Service. EPPO Reporting Service. Paris, France: EPPO. http://archives.eppo.org/EPPOReporting/Reporting_Archives.htm

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

EPPO, 2016. EPPO Global database (available online). Paris, France: EPPO. https://gd.eppo.int/

European and Mediterranean Plant Protection Organization, 2011. Diagnostics: Rhagoletis completa. Bulletin OEPP/EPPO Bulletin, 41(3):357-362. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2338

FAO, 1983. International plant quarantine treatment manual. FAO Plant Production and Protection Paper No. 50. Rome, Italy: FAO.

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

Foote RH, 1981. The genus Rhagoletis Loew south of the United States (Diptera: Tephritidae). Technical Bulletin, Science and Education Administration, United States Department of Agriculture, No. 1607:iv + 75 pp.

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

Haley MJ; Baker L, ed. , 1982. Integrated pest management for walnuts. Integrated pest management for walnuts. University of California Statewide Integrated Pest Management Project Berkeley USA, 96 pp.

Harris EJ, 1989. Pest status; Hawaiian Islands and North America, In: Robinson AS, Hooper G, eds. Fruit Flies; their Biology, Natural Enemies and Control. World Crop Pests. Amsterdam, Holland: Elsevier, 3(A):73-81.

Hislop RG; Riedl H; Joos JL, 1981. Control of the walnut husk fly with pyrethroids and bait. California Agriculture, 35(9/10):23-25

IPPC, 2013. First report of Rhagoletis completa. IPPC Official Pest Report, No. HUN-02/1. Rome, Italy: FAO. https://www.ippc.int/

IPPC, 2016. First suspicion of Rhagoletis completa on Juglans regia in a private garden. IPPC Official Pest Report, No. NLD-46/1. https://www.ippc.int/en/

Kasana A; AliNiazee MT, 1994. Effect of constant temperatures on development of the walnut husk fly, Rhagoletis completa. Entomologia Experimentalis et Applicata, 73(3):247-254

Kasana A; AliNiazee MT, 1996. Seasonal phenology of the walnut husk fly, Rhagoletis completa Cresson (Diptera: Tephritidae). Canadian Entomologist, 128(3):377-390; 29 ref.

Legner EF; Goeden RD, 1987. Larval parasitism of Rhagoletis completa (Diptera: Tephritidae) on Juglans microcarpa (Juglandaceae) in western Texas and southeastern New Mexico. Proceedings of the Entomological Society of Washington, 89(4):739-743

Merz B, 1994. Insecta Helvetica, Fauna, 10: Diptera Tephritidae. Neuchatel, Switzerland; Centre Suisse de Cartographie de la Faune (CSCF), 198 pp.

Ostojic I; Zovko M; Petrovic D, 2014. First record of walnut husk fly Rhagoletis completa (Cresson, 1929) in Bosnia and Herzegovina. (Prvi nalaz orahove muhe Rhagoletis completa (Cresson, 1929) u Bosni i Hercegovini.) Radovi Poljoprivrednog Fakulteta Univerziteta u Sarajevu (Works of the Faculty of Agriculture University of Sarajevo), 59(64(1)):121-126.

Riedl H; Barnett WW; Coates WW; Coviello R; Joos J; Olson WH, 1989. Walnut husk fly (Diptera: Tephritidae): evaluation of traps for timing of control measures and for damage predictions. Journal of Economic Entomology, 82(4):1191-1196

Riedl H; Hislop R, 1985. Visual attraction of the walnut husk fly (Diptera: Tephritidae) to color rectangles and spheres. Environmental Entomology, 14(6):810-814

Rull J; Tadeo E; Aluja M; Guillen L; Egan SP; Feder JL, 2012. Hybridization and sequential components of reproductive isolation between parapatric walnut-infesting sister species Rhagoletis completa and Rhagoletis zoqui. Biological Journal of the Linnean Society, 107(4):886-898. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1095-8312

Seljak G; Zezlina I, 1999. Appearance and distribution of walnut husk fly (Rhagoletis completa Cresson) in Slovenia. Zbornik predavanj in referatov 4. Slovenskega Posvetovanja o Varstvu Rastlin v Portoroz^hacek~u od 3. do 4. Marca 1999., 231-238; 7 ref.

Shelton MD; Anderson JL, 1990. Walnut cultivars: evidence for differential susceptibility to insect pests. Fruit Varieties Journal, 44(4):179-182

Steyskal GC, 1973. Distinguishing characters of the walnut husk maggots of the genus Rhagoletis (Diptera, Tephritidae). Cooperative Economic Insect Report, 23: 522.

Tuba K; Schuler H; Stauffer C; Lakatos F, 2012. First record of the walnut husk fly (Rhagoletis completa Cresson 1929) (Diptera: Tephritidae) in Hungary. (A nyugati dióburok-fúrólégy (Rhagoletis completa Cresson 1929 - Diptera: Tephritidae) megjelenése magyarországon.) Növényvédelem, 48(9):419-424.

White IM; Elson-Harris MM, 1994. Fruit flies of economic significance: their identification and bionomics. Wallingford, UK: CAB International. Reprint with addendum.

Yokoyama VY; Miller GT, 1996. Response of walnut husk fly (Diptera: Tephritidae) to low temperature, irrigation, and pest-free period for exported stone fruits. Journal of Economic Entomology, 89(5):1186-1191; 7 ref.

Distribution Maps

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