Rhagoletis pomonella

Current scientific name: Rhagoletis pomonella (Walsh) Class: Insecta Order: Diptera Family: Tephritidae Genus: Rhagoletis Species: Rhagoletis pomonella (Walsh) Synonym(s): Trypeta pomonella Walsh 1867; Spilographa pomonella (Walsh), Zonosema pomonella (Walsh) EPPO Code:  RHAGPO  Common name: apple maggot fly, apple maggot Taxonomic rank: species

The family Tephritidae consists of a vast number of species and includes many species that are significant agricultural pests. In particular, the genus Rhagoletis contains 77 described species that are distributed throughout Europe, Asia and America and includes several species of economic importance ( EFSA PLH Panel, 2020 ). Rhagoletis pomonella was first reported after the species expanded its natural host range from fruit of the hawthorn (Crataegus spp.) to fruit of domesticated apple trees when this fruit crop was introduced into North America (Bush, 1993).

Rhagoletis pomonella is part of a group of closely related species – the pomonella species group or complex – which originally comprised the sibling species R. pomonella, R. mendax, R. zephyria and R. cornivora (Bush, 1966). The undescribed flowering dogwood fly is also considered to be part of this species complex (Berlocher, 1999). These species have a very similar morphology but have distinct host plant affiliations. Moreover, several allozyme loci display frequency patterns that are useful in discriminating the species (Berlocher, 2000). In addition, the species R. pomonella has been differentiated into host races (apple and hawthorn-infesting populations). The exact taxonomic status of the entities in the pomonella complex is somewhat uncertain. However, sequence data analysis has shown that R. cornivora is clearly distinct from the other species, but neither nuclear nor mtDNA loci resolved the phylogenetic relationships among populations of R. pomonella, R. mendax, R. zephyria and flowering dogwood fly in the USA (Xie et al., 2008). Despite this complexity and uncertainty, R. pomonella can be considered a clearly defined entity given its capacity to infest apples (i.e. because of their host fidelity a finding of Rhagoletis larvae in apples would be a very strong indication of the presence of R. pomonella).

Rhagoletis pomonella is a Union quarantine pest listed in Annex II of  Commission Implementing Regulation (EU) 2019/2072 .

Rhagoletis pomonella is also listed as a priority pest under  Commission Delegated Regulation (EU) 2019/1702  implying the obligation for annual surveys of the pest.

Special import requirements are laid down in Annex VII of Commission Implementing Regulation (EU) 2019/2072 regarding the fruit of Malus to ensure pest freedom from R. pomonella. In addition, this Annex lays down special import requirements for growing medium in general that would also mitigate the risk for entry of pupae of R. pomonella should plants for planting of hosts be imported.

Plants for planting of the main host plants of the genera Malus and Crataegus are included in the list of high-risk plants under  Commission Implementing Regulation (EU) 2018/2019 .

The general requirements for survey of quarantine pests in the EU territory are laid down in  Regulation (EU) 2016/2031  and  Commission Implementing Regulation (EU) 2020/1231 .

Rhagoletis pomonella is endemic to eastern North America from Canada via the USA to Mexico (CABI, 2019; Yee et al. 2014a; Michel et al. 2007; Rull et al. 2006;  EPPO, online ). The species shifted from its native hawthorn host (Crataegus spp.) to domesticated apple in the mid-1800s (Hood et al. 2013). Nowadays, the species is also present in the western United States. Overall, R. pomonella is currently distributed in several states of the US, Canada and Mexico. No outbreaks have been reported in the EU so far.

Note: the information included in this section is aligned with the EPPO map updated on 17-06-2021

Rhagoletis pomonella is a univoltine species, meaning that one generation of flies complete their life cycle in a single year (Dean and Chapman, 1973). Flies overwinter in an obligate pupal diapause under the surface in the top 5 cm of soil beneath the host trees (mainly Malus spp. and Crataegus spp.), but can sporadically overwinter on the soil surface (within fallen leaves and dry grasses) or in fallen fruit. A small proportion of pupae may yield adults within the same season. Occasionally, flies delay emergence from the pupae in the soil for one or two years, while a few pupae may refrain from entering diapause causing flies to emerge before the winter in the same year.

A new generation of adults emerges from early June (Mattsson et al., 2015) onwards to September and adults live for approximately 30 to 40 days (Dean and Chapman, 1973). After emergence, they feed for 7 to 10 days before reaching sexual maturity. Adults feed on a variety of food sources, including honeydew, pollen and liquid from the plant glands, wounds and oviposition stings (Boller and Prokopy, 1976). Adults mate on or near the host fruit and the female lays a single fertilised egg just under the outer skin of ripe fruit on the tree. A single R. pomonella female can lay more than 20 eggs during her life. Eggs hatch after 3 to 7 days, while the emerging larvae take about 2 to 3 weeks to develop within the fruit (Christenson and Foote, 1960), undergoing three larval instar stages. Development times depend on the host species, fruit softness and temperature (Christenson and Foote, 1960; Messina and Jones, 1990; Dean and Chapman, 1973). The larvae tunnel through the flesh of the fruit while feeding, leaving a brown trail and causing the fruit to deteriorate. This often results in the premature abscission of infested fruit. Mature larvae emerge from the fruit to pupate after it has dropped to the ground or emerge from the fruit while still on the tree. The larvae burrow into the soil to pupate and enter the diapause.

This section provides the information needed to characterise the population of host plants to target in a survey, as described in the  ‘General guidelines for statistically sound and risk-based surveys of plant pests’  (EFSA et al., 2020a). This includes the pest’s host range and main hosts in the EU ( Section 2.1 ), the suitability of EU environments to the pest’s establishment ( Section 2.2 ), the ability of the pest to spread ( Section 2.3 ), and the identification of risk factors associated with an increased probability of presence ( Section 2.4 ).

Once the above parameters have been defined, the target population can be structured in multiple levels. At level 1 is the survey area, which corresponds to the entirety or part of the Member State. At levels 2 and 3 are the epidemiological units that can be distinguished within the survey area. Epidemiological units can be chosen as administrative regions (e.g. EU NUTS areas or Member State-level regions) if they are homogeneous, or further subdivided into the environments where host plants are present using a land-use categorisation (e.g. urban, agricultural and natural areas, nurseries). At level 4, if risk factors are identified, the risk areas are defined around the risk locations. At level 5 are the inspection units, the elementary subdivisions of the target population that are inspected for the detection of the pest (e.g. host plants), depending on the pest detection method ( Section 3 ). For the definitions of the target population, epidemiological units and inspection units, see also the  glossary  of terms available at the end of this document.

The hierarchical structure of the target population should be tailored to the situation in each Member State. A possible structure of the target population for surveys of R. pomonella within the EU is proposed in  Section 2.5 .

Rhagoletis pomonella has been reported to attack a number of host plants, several of which are agricultural hosts. Hawthorn species are its native host plants. The most heavily infested hosts are species of the Malus and Crataegus genera, which are largely distributed across the EU, while many species are considered incidental hosts. Yee et al. (2014a) consider that only apple (M. domestica) and various hawthorn species (C. aestivalis, C. brachyacantha, C. crus-galli, C. douglasii, C. flabellate, C. flava, C. gracilior, C. greggiana, C. holmesiana, C. macrosperma, C. mexicana, C. mollis, C. monogyna, C. opaca, C. pruinosa, C. punctate, C. rivularis, C. rosei, and C. viridis) are the most important potential host species. Species in the genera Amelanchier, Aronia, Cotoneaster, Prunus, Pyracantha, Pyrus, Rosa and Sorbus can also be infested, but are considered to be of low importance (Yee et al., 2014a), whereas Pyrus pyrifolia (Asian pear) is considered to be of medium importance. For example, Bush (1966) indicates that larvae of R. pomonella have been found in pears (Pyrus communis), but that no adults have emerged.

The main commercial host is Malus domestica, in which the pest completes its life cycle and causes severe damage (CABI, 2019). In the EU, apples are cultivated on a large scale and these host trees are the main target for detection surveys. The existence of native Crataegus species in the EU, including C. laevigata, C. monogyna, and C. orientalis, and introduced ornamental ones (e.g. C. crusgalli, C. pedicellata and C. persimilis) highlights the importance of conducting survey activities in areas where those species are present. These species can be found in (semi-)natural conditions or urban areas but can also be found as a hedge species in agricultural areas across all temperate environments in the EU. Crataegus is very likely to become infested should R. pomonella be introduced but is a more challenging target for detection surveys given the difficulties of localising the scattered locations of these trees and shrubs. Nonetheless, for delimiting surveys, Crataegus spp. should be included as a target for surveillance.

Rhagoletis pomonella is currently present in a considerable part of North America across a range of ecoclimatic conditions that closely resemble the climatic conditions in large parts of the EU. The pest seems to have a preference for moderate temperatures and high precipitation (WSDA et al., 2016).

Based on the present distribution in North America, Geng et al. (2011) used CLIMEX 3.0 to determine the potential distribution of R. pomonella in China. Hot and dry summers were found to have a negative effect on pest prevalence in the model. Geng et al. (2011) suggested that the determining factor for the predicted distribution was the environmental conditions (e.g. temperature, humidity) that the pupae experience, whereas eggs and larvae are protected from environmental fluctuations inside the host fruit. Kumar et al. (2016) used both MaxEnt and CLIMEX models, which indicated that most parts of central and southern Europe were highly favourable for the establishment of R. pomonella. Large parts of Scandinavia and the northern edges of the UK were estimated to be unsuitable for establishment ( EFSA PLH Panel, 2020 ). Establishment is conditional on the presence of suitable host plants, which are largely absent from the areas considered unsuitable for R. pomonella. Overall, most or all areas of the EU in which apple and hawthorn species grow are at risk for the establishment of R. pomonella.

Natural spread

Rhagoletis pomonella is not considered to be a long-distance flier. The flies normally travel relatively short distances when food resources and breeding sites are abundant. However, they may travel longer distances when this is not the case. All dispersal studies that have been carried out under field conditions were conducted in areas with abundant host plants. Release–recapture studies have found maximum flight distances up to approximately 1.5 km (Maxwell and Parsons, 1968), but when apple trees are more abundant nearby, reported maximum flight distances are much shorter (7 665 m) (Maxwell, 1968; Neilson, 1971; Bourne et al., 1934; WSDA et al., 2016).

Based on expert knowledge elicitation,  EFSA (2019)  estimated that the maximum distance expected to be covered in one year by R. pomonella is approximately 230 m (with a 95% uncertainty range of 24 m to 2.3 km).

Human-assisted spread

The most likely human-assisted spread of R. pomonella is through the transport of infested fruit (imports of fruit commodities or fruit in passenger luggage) because the development of eggs and larvae takes place in the fruit, making the infestation difficult to detect. Despite the fact that around 4,500 interceptions were generally attributed to Tephritidae specimens in the period 1995–2022 (EUROPHYT, online; TRACES, online), no interceptions or outbreaks of R. pomonella have been reported in the EU so far.

The likelihood of importing adults can be considered negligible. The main pathway would be the introduction of immature life stages of R. pomonella through infested fruit, but this would not result in outbreaks in the majority of cases. This is because, even if eggs or larvae survive the transport, larvae still need to pupate and survive the long dormancy period before reaching the adult stage. Adult females subsequently need to locate both a suitable mate and a suitable host plant with fresh fruit in order to lay eggs for the next generation of flies. Note that in general, any findings of adults or larvae in locally grown fruit should thus be related to an introduction in the previous year.

Pupae may also be transported in the soil or other growing medium with the host plants. However, the import of plants for planting of the main host genera (Malus and Crataegus) is currently prohibited as these genera are included in the list of high-risk plants under  Commission Implementing Regulation (EU) 2018/2019 . The risk for entry of pupae of R. pomonella in growing medium (i.e. other than soil, consisting in whole or in part of solid organic substances) is also mitigated by the general import requirements for growing medium under  Commission Implementing Regulation (EU) 2019/2072 .

Identification of risk factors and their relative risk estimation are essential for performing risk-based surveys. A risk factor is a biotic or abiotic factor that increases the probability of infestation by the pest in the area of interest. The risk factors that are relevant for surveillance need to be characterised by their relative risk (should have more than one level of risk for the target population) and the proportion of the overall target population on which they apply. The identification of risk factors needs to be tailored to the situation of each Member State. This section presents examples of risk factors for R. pomonella and is not necessarily exhaustive. 

For the identification of risk areas, it is first necessary to identify the activities that could contribute to introduction or spread of R. pomonella. These activities should then be connected to specific locations. Around these locations, risk areas can be defined, knowing that their size depends on the spread capacity of the target pest and the availability of host plants around these locations.  

The Member States can opt to utilise the information available on the EU Platforms of TRACES Interceptions, EUROPHYT Interceptions and EUROPHYT Outbreaks. The information available, in particular, relating to the country of origin, type of commodity and hosts of intercepted or outbreak reports can be extracted from such platforms for specific harmful organisms. This information can allow Member States to identify potential pathways of introduction from previous historical findings. Thus, Member States might consider focusing their surveillance efforts around activities and locations related to previous interceptions and outbreaks.  

Such information should only be considered as indicative and given the possible dynamic changes, it should be reviewed and analysed periodically.  

Example 1: Entry points, packing and sorting stations for apples imported from regions where the pest is present

Despite the fact that the import of apples is subject to special import requirements, the risk of introduction of R. pomonella via the import of infested fruit cannot be excluded. Entry points (e.g. seaports, airports) of apple commodities, the packing and sorting stations, and processing industries that handle apples originating from areas where R. pomonella is present would be locations with a higher probability of finding the pest. Risk areas are then the areas in the vicinity of those risk locations where Malus and Crataegus host plants are present.

The actual risk of a location depends on the storage facilities and the waste disposal procedures. If fruit is stored and handled on site while being cooled, and waste is disposed of in closed containers, the risk of introduction at that site will not be high. Because R. pomonella is not considered to be a long-distance flier (i.e. the maximum distance expected to be covered in one year is estimated to be approximately 230 m; see Section 2.3), the risk area will be of relatively limited size. It should, however, be noted that in the local absence of suitable hosts, the flight distance may become longer. The relative risk of the specific area will depend on the nature of the activities that are taking place at the risk location, e.g. the timing and specific origin of the import, and the storage conditions.

Example 2: Urban areas

Given that import of infested fruit constitutes the most likely pathway for introduction, the households that buy apples originating from areas where R. pomonella is present and fresh markets where such fruit is sold would be locations with a higher probability of finding the pest. When apples are damaged by R. pomonella larvae they are likely to be disposed of in containers or compost heaps. Waste collection centres should also be considered as risk locations. The ‘density’ of apple consumption (and thus disposal) would be higher in urban areas than in less densely populated areas and the preferred survey sites would then be locations with cultivated apple trees in or near to urban areas. Surveillance may include Crataegus spp. or crab apples that are grown as ornamental plants.

The figure on the right panel gives examples of the components of a target population for R. pomonella and is not necessarily exhaustive.

Detection of R. pomonella can be performed either by trapping adults or by examining fruit in order to detect oviposition stings and/or immature stages (mainly larvae). Trapping would be the recommended method for surveillance and detection, but when examinations of fruit are already performed to detect other pests, it might be worthwhile to include R. pomonella in that respective surveillance protocol.

3.1.1. Visual examination

Visual examination should focus on the detection of symptoms cause by R pomonella. For completeness, a simplified description of the pest in the CABI datasheet on R. pomonella (CABI, 2019) is given below.

Pest

According to CABI (2019): ‘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. 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. The oval, yellow-brown pupae are approximately 5 mm long and 2.3 mm wide.’ A detailed description of the eggs, larvae and pupae can be found in Bush (1966).

Rhagoletis pomonella can be recognised by four irregular or zig-zag black bands on the wings with the three distal bands forming an F-shape. The body generally has a black colour, while the head and legs are yellowish-brown. The eyes are greenish. The last segment of thorax ‘scutellum’ is white, in contrast to the European cherry fruit fly, R. cerasi. Males and females have three and four white bands on their abdomen, respectively. Adult flies (also of other closely related Rhagoletis species) are about 2 to 4 mm in size and the females are larger than the males (CABI, 2019).

Symptoms and signs

Fruit can be examined to detect the signs that indicate the presence of R. pomonella. When the female flies lay eggs, this leaves a puncture mark (i.e. oviposition sting) on the skin of the apple. Puncture marks can be recognised by a sunken spot on the surface of the fruit. Fruit may become irregular in appearance due to this sunken spot or as a consequence of the feeding of the larvae. Larvae can be detected when opening the fruit as they leave a brown trail while moving through the flesh of the fruit during feeding. Premature abscission of the fruit can be a clear sign of the presence of R. pomonella, causing the fruit to rot on the ground.

3.1.2. Trapping

In general, a wide variety of systems is available to trap R. pomonella, similar to other fruit fly (Tephritidae) species. Most trapping systems are used in combination with a lure (FAO, 2018). For R. pomonella, a common adult trapping system consists of a yellow sticky trap combined with carbonate lures (WSDA et al., 2016). Alternatives include a red sticky sphere with a combination of lures based on fruit volatiles (Reissig et al., 1982; Zhang et al., 1999).

In the western USA, traps baited with ammonium carbonate were more attractive than the fruit volatile blends that were developed specifically for apple and various hawthorn species (Yee et al. 2005, 2014b). Note that in its native range in the eastern USA, there was no added benefit to using ammonium carbonate when traps were baited with the synthetic host fruit odour butyl hexanoate (Rull and Prokopy, 2000). Ammonium carbonate can be applied in capped vials that subsequently release 5–7 mg of ammonia per hour through holes in the cap for a period of about a month (Yee et al. 2005).

Traps should be placed in fruiting host plants and have a limited range of attraction, since R. pomonella is not attracted to traps further away than circa 2 m (WSDA et al., 2016). In practice, this means that flies are attracted from the tree in which the trap is placed. The trapping density for R. pomonella would need to be very high in order to obtain a reasonable reliability on the absence of the fly in an orchard that is being targeted by the survey.

All traps should be inspected at regular intervals (i.e. weekly) and taken to the laboratory for further confirmation, and lures should be replaced at regular intervals.

3.1.3. Sample collection

Living larvae should be collected from infested fruit and then reared to adulthood for confirmation based on adult morphology. Infested fruit should be taken to the laboratory and kept in controlled conditions until the larvae emerge from the fruit to pupate. It should be noted that to obtain adults from larvae that were retrieved from infested fruit, a period of several months might be required. This is because of the obligate diapause that pupae undergo and needs to be terminated following standard protocols. Living larvae can be dissected from infested fruit but only third instar larvae can be easily located. The collection of living larvae is particularly important for an initial finding but would not be needed when dealing with known outbreaks.

Dead larvae from potentially infested fruit should be transferred to 70% ethanol (for morphological identification at the genus level) or to 95% ethanol (for molecular tests to support identification at the genus level).

Apple samples, living larvae, samples stored on ethanol and trapped insects should be taken to the lab for confirmation.

3.1.4. Timing of detection and identification

Because adult trapping is the preferred survey method, the timing of the surveys should coincide with the period in which adult flies are present, which is aligned with the period in which host fruit is present on the host tree. The presence of ripe or ripening fruit greatly increases the probability of trapping an adult at a given survey site, so the timing should be fine-tuned for specific host species, apple cultivars and local conditions.

3.2.1. Morphological identification

Identification of R. pomonella at the species level requires morphological examination of adult flies, as is generally the case for Tephritidae. This implies that larvae should be reared to the adult stage to enable confirmation of their identity. Because of their host fidelity, a finding of Rhagoletis larvae in apples would be a very strong indication of the presence of R. pomonella. Identification should be performed by a taxonomic specialist and, particularly in the case of a first finding, the identity should preferably be confirmed by a specialist from the current distribution area of the species.

Once the collected adult Rhagoletis flies have been taken to the laboratory or have been reared in the laboratory, keys are available for morphological identification to the genus level (e.g. in White and Elson-Harris, 1992; Foote et al., 1993; Bush, 1966). The information in Bush (1966) can be used for identification within the genus Rhagoletis.

Rhagoletis pomonella is part of the pomonella species group or complex. Its members have a very similar morphology but have distinct host plant affiliations. As a consequence, R. pomonella cannot easily be distinguished from the other species in the complex based on morphology alone (Berlocher, 2000; Bi et al. 2007). Particularly, the separation between R. pomonella and R. mendax is considered very difficult based on morphology but becomes quite straightforward when information on the host plant is included. When adult specimens have been collected from a sticky trap, the tree species in which the trap was placed can be considered as a proxy for the host plant given the limited range of attraction. However, if it is a first finding it is recommended that living larvae are sought and collected from apples and reared to the adult stage to have the most accurate identification.

Since all sibling species in the pomonella complex are regulated as Union quarantine pests, the finding of a member of the complex would always warrant phytosanitary action, even if there is uncertainty about the identity. Nevertheless, accurate identification is desirable for a quarantine pest.

3.2.2. Laboratory testing and other methods of identification

A protocol for DNA barcoding based on the cytochrome oxidase I (COI) gene is described in EPPO Standard PM 7/12 on DNA barcoding as an identification tool for a number of regulated pests ( EPPO, 2016 ) and can be used for all life stages. This protocol can provide additional information on a specimen, but molecular identification by DNA sequencing of a mitochondrial locus and several nuclear loci did not provide sufficient resolution to unequivocally resolve the identity of R. pomonella, R. mendax, R. zephyria and the undescribed flowering dogwood fly (Xie et al., 2008).

Information on what, where, when and how to conduct survey activities for R. pomonella is summarised in the Table on the right panel. The identification of the target population needs to be tailored to the situation in each Member State (example shown below).

The figure below shows the next steps after the survey preparation for designing statistically sound and risk-based detection and delimiting surveys of R. pomonella. Guidance on selecting the type of survey, related survey preparation and design, is provided in the the  EFSA general guidelines for pest surveys  on the right panel (EFSA et al., 2020a).

Scroll down the right panel to access the definitions included in the glossary.

 General guidelines for statistically sound and risk-based surveys of plant pests 

 Rhagoletis pomonella – Pest report to support ranking of EU candidate priority pests by the EFSA Working Group on EU Priority Pests 

 Index of EFSA Plant Pest Survey Toolkit 

 Plant Pest Survey Cards Gallery 

 The statistical tool RiBESS+ 

 The RiBESS+ manual 

 The RiBESS+ video tutorial