Preferred name: Epitrix papa
Authority: Orlova-Bienkowskaja
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Coleoptera: Chrysomelidae
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Notes on taxonomy and nomenclature EPPO Categorization: A2 list
EU Categorization: Emergency measures
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EPPO Code: EPIXPP

E. papa is associated with solanaceous hosts, as is the case for all other Epitrix species, the adults feeding on the foliage and the larvae on the roots (Doguet, 1994). The adults of E. papa may feed temporarily on plants from other botanical families when they do not have access to their solanaceous hosts, but no records exist on the possibility of larval development on non-solanaceous plants.

The most economically important host for E. papa is potato (Solanum tuberosum). In Portugal E. papa has also been observed on aubergine crops (Solanum melongena) but damage on this crop is not important and only leaves are affected (Boavida et al., 2013). Other solanaceous host plants include common weeds such as black nightshade (Solanum nigrum), jimsonweed (Datura stramonium) (Boavida et al., 2013) and cutleaf nightshade (Solanum triflorum) (Boavida & Germain, 2009). All these secondary host plant species are important food sources for the survival of E. papa populations when potato is not available (Boavida et al., 2019), and the same applies to plants from different botanical families where the adults may feed temporarily, such as Chenopodium sp. (Amaranthaceae) recorded by Oliveira et al. (2008). 

However, these different host plant species are not equally suitable for the multiplication of E. papa, as demonstrated in laboratory experiments. In these experiments, E. papa produced the highest number of offspring on potato and on black nightshade, followed by aubergine and jimsonweed, with the lowest number of offspring produced on tomato (Solanum lycopersicum), and no reproduction on sweet pepper (Capsicum annuum) (Boavida et al., 2013). 

Host list: Chenopodium sp., Datura stramonium, Solanum lycopersicum, Solanum melongena, Solanum nigrum, Solanum triflorum, Solanum tuberosum

The origin and native distribution of E. papa are unknown (Orlova-Bienkowskaja, 2015). In Portugal, E. papa is supposed to have been introduced around 2004 in the North of Portugal (Oporto), but remained unnoticed until 2008, when it was detected in two important potato cropping zones in the centre of Portugal (Centro and Lisboa e Vale do Tejo) (Oliveira et al., 2008; Boavida & Germain, 2009). In Spain, E. papa was first detected in 2008 in Galicia, close to the Portuguese border (Boavida & Germain, 2009).

EPPO Region: Portugal (mainland, Azores, Madeira), Spain (mainland)

The life cycle of E. papa is similar to those of the economically important American tuber flea beetle species, E. tuberis and E. yanazara (Hoerner & Gillette, 1928; Hill & Tate, 1942; Alcázar, 1997). The adults overwinter in and around the fields where they developed, buried in the soil or under leaf litter and other debris. They become active at the end of winter, when the temperature warms up, leave their winter refuges and start feeding on alternative host plant species available, until the potato plants develop. The emergence of the overwintered adults is gradual, and may start in early March (Boavida et al., 2019) or later in April (MAPAMA, 2017) depending on the climate. When they find a potato plantation, the overwintered adults settle on the potato plants, feed, and mate. After a pre-oviposition period, the female lays eggs below the soil surface, close to the stems of the potato plants. After the eggs hatch, the larvae move to the roots for feeding. When fully-grown, larvae stop feeding, move away from the root zone, to build a pupation chamber with soil particles in which the insect transforms into an adult. After emerging from the soil, the adults of the first generation feed on the foliage of the potato or other host-plants and multiply, to produce the second generation. 

The biology of E. papa was studied in the laboratory at different temperatures. The development time from egg to adult was 102 days at 15ºC, 48 days at 20ºC, 34 days at 25ºC and 30 days at 30ºC (Boavida et al., 2019). The mean preoviposition period ranged from 20 to 7 days, the oviposition period from 115 to 44 days, and the females fecundity from 64 to 190 eggs, at 15ºC and 25ºC respectively.

From these data, a degree-day model of developmental rates as a function of temperature was calculated, allowing an estimation of the lower limit for completion of one E. papa generation as 625 degree-days above 8.1 °C (Boavida et al., 2019). Based on this model, three complete generations per year and a partial fourth are possible in most cropping zones of Portugal. The first generation of E. papa is expected to develop from egg to adult in a minimum of 7 weeks, and the following generations will develop much faster, in 4-5 weeks. The first generation larvae develop from April to late May, mostly on seed potatoes, small immature tubers and roots of early planted crops, while the larvae of the second generation develop from mid June onwards, hence developing mostly on maturing tubers of mid- and late season crops. The second larval generation is more damaging than the first one, because the second generation larvae are more abundant and also because the feeding wounds caused by the larvae on the maturing tubers in the process of skin suberization are deeper and remain conspicuous until harvest, whereas the lesions caused on small developing tubers are frequently blurred into the skin during the process of tuber growth. The larvae of the third generation develop on alternate hosts from mid August onwards, a period when most of the potato crops have been harvested, and therefore the larvae of this generation do not represent in most cases a threat for potato production.

E. papa adults disperse by flight, jumping and walking.

Symptoms

Both larvae and adults have chewing mouthparts. The adults riddle the leaves with small circular holes (1.0-1.5 mm diameter) that produce the characteristic ‘shot-hole’ symptom in the potato foliage, which is common to all flea beetles. The adult insects can be detected on the foliage, and jump promptly when approached. On windy days, they are less active.

The types of tuber injury caused by larval feeding are similar to those caused by E. tuberis. The larva may tunnel underneath the skin, producing winding superficial trails, called ‘worm-tracks’ or ‘serpentines’ (Gentner, 1944; Boavida et al., 2013). They may also feed from the outside, burrowing into the flesh, almost at a right angle to the surface, causing a dark splinter full of corky material which mostly penetrates up to 3 mm but may reach 9 mm (Boavida et al., 2013). This type of injury is similar to the one described for E. tuberis in the USA as a ‘sliver’ (Gentner, 1944; Morrison et al., 1967). ‘Slivers’ may show on the tuber’s surface as a black point, or a raised rugose elevation in the skin (‘pimples’). Rough skin, and scab-like lesions are sometimes observed in association with the larval attack of E. papa. Tuber flea beetle lesions have been claimed to favour the penetration of different pathogens, and Schaal (1934) demonstrated that E. tuberis larvae could transmit the common scab fungus (Streptomyces scabies) from the soil into the tubers. This may also be the case for E. papa.

Morphology

The genus Epitrix is a group of small flea beetles with uniform appearance which can be recognized by the presence of elytral punctures arranged into rows, and characteristic rows of erect setae on the intervals (Döberl, 2000; EPPO, 2017). The morphological identification to species is made by specialists, on the basis of the habitus and genitalia of the adult insects. The identification keys and illustrations presented in EPPO Standard PM 7/109 (2) (EPPO, 2017) and Orlova-Bienkowskaja (2015) allow E. papa to be distinguished from the related potato species E. cucumeris, E. tuberis and E. subcrinita.

Eggs

The eggs are elliptical, white, with a reticulate surface, approximately 0.5 mm in length and 0.2 mm in width.

Larva

The newly hatched larva is white in colour, threadlike, and approximately 1.0 mm long. The full-grown larva is white, with the head and thoracic shield light brown, and approximately 5 mm in length.

Pupa

The pupa is pearly white and approximately 2.5 mm long and 1.5 mm wide.

Adult

The adults are small black beetles with a weak bronze reflection, rows of short white hairs along the elytra, 1.7-2.2 mm long. The hind femurs are enlarged, adapted to jumping. 

Detection and inspection methods

Detection is made by visual inspection of the foliage of potato or other host plants, looking for shot-hole symptoms and adult flea beetles. On potato, the tubers are inspected visually for symptoms of larval injury (EFSA, 2019). The ‘worm-track’ type of injury is the most easily recognizable. The ‘slivers’ are best detected if the potato tubers are peeled with a knife.

The identification of the species requires the collection of insect specimens for analysis. Adult specimens may be collected with a sweep-net or with a mouth aspirator. The larvae are very difficult to detect and collect because of their small size and translucent colour, and also because of their feeding behaviour. When present at potato harvest, some larvae may be hidden inside the ‘worm tracks’, and others may expose the terminal part of their abdomens protruding outside the tuber, while feeding.

The identification of all E. papa stages can be made reliably by non-specialists, using molecular methods (DNA barcoding on cytochrome c oxidase subunit I (COI) gene) (Germain et al., 2013; Mouttet et al., 2019). The reference sequences of these species are available in EPPO-Q-bank and BOLD databases.

The origin of E. papa and the pathway for its introduction in Portugal are unknown. The adults disperse naturally by flight, walking and jumping, but long distance spread is through the commercial transport of seed or ware potato tubers, when associated with soil and plant debris (EPPO, 2016; 2017). 

When potatoes are harvested from an infested field, adults and pupae of E. papa may be present in the stubble and soil, and larvae in the tubers. Adult beetles may be carried passively on the surface of potatoes, or with the soil adhering to potato tubers. This possibility would be higher in exports of seed potatoes, because potatoes are not washed. At harvest, larvae present inside well suberized ‘worm-tracks’ may be transported with the tuber, however no data exists on the possibility of these larvae surviving and completing development. By contrast, larvae feeding outside the tuber escape rapidly and hence will not be transported. 

Economic impact

The ‘worm-track’ lesions caused by the larvae of E. papa are mostly superficial and do not affect the tuber’s quality, but have a marked negative visual impact in certain trade markets, which may result in the rejection or the commercial downgrading of the potato exports (Oliveira et al., 2008; Vernon & Herk, 2017). When present, ‘slivers’ oblige deeper peeling of the potatoes before consumption, and may cause some production losses. In Canada, a potato lot is commercially downgraded when more than 5% of the tubers are injured by E. tuberis (EPPO, 2011). To prevent economic damage, the crops are treated with insecticides, which increases the production costs (Vernon & Herk, 2017). In the countries where E. papa is reported, official eradication and containment measures are implemented, which include insecticide treatments targeting specifically Epitrix species, and brushing / washing the harvested tubers to remove the pest and the soil (EU, 2018). The related costs represent an additional burden to the crop’s production, and the recommended early season insecticide sprays pose a risk to the pollinating fauna.

The reduction of the leaf area by adult feeding is not expected to have an important impact on yield, because it can be compensated for by the fast growth of the potato plants, as demonstrated experimentally by Senanayake et al. (1993) for E. cucumeris.

Control

There are no published records of efficient natural enemies of E. papa.

Without control measures, and with favourable climatic conditions, E. papa can multiply rapidly to damaging population levels (Oliveira et al., 2008), in particular in zones with an extended potato growing season, allowing the development of two complete generations in its preferred host (Boavida et al., 2019). In Portugal and Spain, the populations of E papa were drastically reduced after the pest was identified and control measures were implemented. The control strategy is based on the IPM program carried out in Canada against E. tuberis (Vernon & Herk, 2017). This program combines cultural measures, for reducing the population of overwintered adults, with insecticide treatments. The cultural measures are the cornerstone of the strategy and include the destruction of overwintering places, the rotation with non-solanaceous crops, and when feasible, the adaptation of the planting schedules (Hoerner & Gillette, 1928; Vernon & Herk, 2017). A 3-year potato rotation is recommended to avoid the on-site overwintering of the beetles, together with the destruction of potato culls and volunteers. In Canada, the need for insecticide treatments against the related species E. tuberis is decided on the basis of weekly estimations of the population density of the adults on the plants, by visual inspection of the foliage until the plants are 30 cm tall and later with a sweep net (Vernon & Herk, 2017). Based on experience, a national regulatory control system for Epitrix species damaging potato tubers was developed (EPPO, 2016). No damage thresholds exist yet for E. papa and the mandatory treatments in the demarcated areas of Portugal and Spain stipulated by the Commission Implementing Decision 2012/270/EU of 16 May 2012 (EU, 2018) are recommended to start very early in the season, as soon as the overwintered beetles start colonizing the early potato crops (DGAV, 2018; 2019; MAPAMA, 2019). The negative impact of these early season treatments on beneficial insects can be mitigated if the treatments are directed to specific spots or rows infested by the beetles, avoiding spraying the entire field. Indeed, in well rotated fields the overwintered colonizing beetles tend to settle and feed initially on the border rows of the crop (Cusson et al., 1990). 

Phytosanitary risk

The present distribution of E. papa in Portugal and Spain indicates that the species could establish in at least the Mediterranean Basin (EPPO, 2011). Distribution models based on climatic variables of the currently known distribution of E. papa indicate that the species would not find suitable climatic conditions in northern parts of the EPPO region, namely in Norway (VKM, 2019). However, according to a degree-day model of developmental rates as a function of temperature (Boavida et al., 2019), the area potentially at risk of establishment would be larger, and would include a few regions located in southern Norway (VKM, 2019).

Since E. papa can be controlled chemically, its presence could lead to a generalized use of insecticides on potato, rather than the occasionally targeted use against Leptinotarsa decemlineata, as at present in most EPPO countries. The problem would arise even more acutely in countries where L. decemlineata has not been introduced (EPPO, 2011). Furthermore, the control of E. papa could be critical in several EPPO countries, namely in a majority of the EU countries, where insecticides used in North America are no longer authorized.

The import of seed potatoes from third countries is prohibited in several EPPO Countries, namely in the EU (EU, 2016), but sometimes authorized under derogation procedures, e.g. from Canada into the EU (EU, 2003). 

Following the risks identified in a Pest Risk Analysis carried out by EPPO on Epitrix species damaging to potato tubers (EPPO 2011), specific requirements related to E. cucumeris, E. papa, E. subcrinita and E. tuberis are recommended in the EPPO potato Standard PM 8/1 (EPPO, 2017b) for the international trade of seed (except micropropagative material and minitubers) and ware potatoes. This Standard recommends that seed potatoes should be washed or brushed so that they are free from plant debris and have no more than 0.1% w/w of soil remaining, and where appropriate subject to transitional arrangements (pest-free area for E. papa and origin from a pest-free potato production and distribution system for the pest, according to EPPO Standard PM 3/61 (2) (EPPO, 2019)). For ware potatoes this Standard recommends that either (a) measures as described in EPPO Standard PM 9/22 (EPPO, 2016) for E. papa should have been implemented to ensure that there is no risk of spreading this pest, or (b) that there should be absence of plant debris and no more than 0.1% w/w of soil present.

Additional requirements are recommended for soil or growing medium attached to rooted host plants from countries where E. papa occurs (removal of soil and growing media, or production in a pest free area, or in a pest-free place under protected conditions, or production under screened greenhouse conditions with appropriate monitoring in the framework of a bilateral agreement) (EPPO, 2011).

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This datasheet was prepared in 2020 by Conceição Boavida (Instituto Nacional de Investigação Agrária e Veterinária, I.P., Portugal). Her valuable contribution is gratefully acknowledged.

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