Popillia japonica

Current scientific name: Popillia japonica Newman, 1841 Class: Insecta Order: Coleoptera Family: Scarabaeidae Subfamily: Rutelinae Tribe: Anomalini Genus: Popillia Species: Popillia japonica EPPO Code:  POPIJA  Common name: Japanese beetle Taxonomic rank: species

Popillia japonica is native to northern Japan and in the far east of Russia and is a pest of a great variety of trees, shrubs and herbaceous plants, which could be both cultivated and wild conditions. It is a clearly distinguished species among others of the same genus.

Popillia japonica is a Union quarantine pest listed in Annex II Part B (Section C – Insects and mites) of  Commission Implementing Regulation (EU) 2019/2072 . This part of the Annex contains the list of Union quarantine pests known to occur in EU territory.

Popillia japonica is also listed as a priority pest under  Commission Delegated Regulation (EU) 2019/1702 , for which annual surveys are required by the MSs. Popillia japonica is a highly polyphagous pest. The introduction into the EU of the potential host commodities of P. japonica and soil from third countries is either prohibited or regulated (Annex VI and Annex VII Commission Implementing Regulation (EU) 2019/2072). Special requirements for P. japonica are laid down in Commission Implementing Regulation (EU) 2019/2072 for the introduction of plants for planting from third countries (Annex VII, Point 4.2) and also for the movement of plants for planting within the EU (Annex VIII, Point 2.1).

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 .

The Japanese beetle originates from north-eastern Asia where it is native to Japan and the far east of Russia (Fleming, 1972). It was introduced into North America in 1911 and has become a more serious pest in the USA than in its area of origin ( EPPO, 2006 ).

In the EU, the pest occurs in the Azores (Portugal) where it was detected in the early 1970s, and in northern Italy (Pavesi, 2014) where it was initially found in the Ticino Valley Natural Park between the Lombardy and Piedmont regions in 2014 ( EPPO, 2014 ). Since then, the outbreak in Italy has spread to other areas ( EPPO, 2022b ), and as a result from this outbreak in Italy, P. japonica is also present with restricted distribution in Switzerland ( EPPO, 2021 ). Additionally, one female was caught in a trap in Sardinia in 2021 near the main airport ( EPPO, 2022b ).

In 2018, a dead female beetle was intercepted in a pheromone trap located at Schiphol airport, in the Netherlands ( EPPO, 2019 ). Recently, one specimen was trapped in Germany, close to a railway track in Baden-Wuerttemberg ( EPPO, 2022c ).

Note: the information included in this section is aligned with the EPPO map updated on 03-11-2022

Popillia japonica normally has one generation per year but, at the northern edge of its range, it could take up to two years to complete its life cycle ( EPPO, 2022a ). Kistner-Thomas (2019) projected that in many areas where it has a biennial life cycle, it will transition to an annual life cycle by 2050 as a result of climate change.

The life cycle illustrated in the figure in the right panel indicates the seasonality of the different life stages of the pest. Larval development, adult emergence, subsequent mating and oviposition vary with latitude and year according to the temperature (Fleming, 1972). Thus, Member States must take into consideration the climatic conditions of the area under surveillance. In fact, the reported life cycle in northern Italy is anticipated several weeks earlier than in the US.

In northern Italy, adults emerge in late spring (end of May to the beginning of June) and climb or fly onto the foliage at the top of low-growing hosts before later moving to feed on trees. The average life span of the adult P. japonica is 30–45 days and the adults are present between June and September. The population peak of adults is mid-July, following which, a substantial decline of the population (to negligible) occurs by the end of the month (Gilioli et al., 2021). Aggregation of the adults to feed and mate on individual host plants causes some hosts to be heavily infested while nearby hosts may remain uninfested.

Adult activity is at its peak on warm sunny days, with optimum temperatures for flying in the US between 29°C and 35°C (Kreuger and Potter, 2001). However, if disturbed, the adults will fly at 21°C (Fleming, 1972). Following mating, the females burrow up to 10 cm into the soil for oviposition.  EPPO (2016)  highlighted the importance of the oviposition sites for the females with a preference for moist grassland and turf. After laying eggs the females exit the soil to feed and then return to oviposit in the soil again. A female will usually lay between 40 and 60 eggs in total (Campbell et al., 1989). The eggs are not cold hardy and viability decreases at temperatures below 10°C, while seven days at 0°C led to 100% egg mortality (Fleming, 1972). Depending on temperature, the eggs usually hatch after about 2 weeks and then larvae develop through three instars. In northern Italy, the eggs are present from mid-June to the end of August. The first instar (L1) develops in 2–3 weeks followed by the second instar (L2) in 3–4 weeks. The third instar (L3) overwinters 10–20 cm below ground and will only move towards the turf and start feeding on roots in the spring, before pupation ( EPPO, 2022a ). Adults emerge at the end of May to the beginning of June to repeat the cycle (Ciampitti and Buonopane, 2017). In a physiologically based model predicting larval diapause termination and adult emergence of P. japonica in the outbreak area of Lombardy in Italy, the soil temperature threshold that triggered diapause termination was found to be 12.8°C (Gilioli et al., 2022). The abundance of P. japonica larvae is higher in cool soils and they are less likely to occur in soils with extremely humid conditions (Simonetto et al., 2022)

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., 2020). 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 P. japonica within the EU is proposed in  Section 2.5 .

Popillia japonica is a highly polyphagous species, and the adults can be found feeding on a wide range of wild, cultivated and ornamental plant species ( EPPO, 2016 ). According to the USDA (2016), the pest has a host range of more than 300 plants in 79 plant families. CABI (2020) and  EPPO (online)  provide an exhaustive list of host plant species reported so far worldwide. Following exclusion and inclusion criteria, ANSES (2022) selected 131 main host plants from 39 different families that are associated with a higher phytosanitary risk.

Popillia japonica can cause significant damage to seedbeds, orchards, field crops, landscape plants, turf and garden plants due to the larval feeding. The main species attacked by larvae within the grassland belong to the genera Festuca, Poa and Lolium ( EPPO, 2016 ).

In northern Italy, the plant species, and their respective categories attacked, are illustrated in the table below (Servizio Fitosanitario Regione Lombardia, 2022).

In the Azores (Portugal), the adult beetles were reported to feed on a wide range of hosts: Acer spp. (maples), Asparagus officinalis (asparagus), Glycine max (soybean), Malus spp. (apples), Medicago sativa (alfalfa), Phaseolus vulgaris (pea), Populus spp. (poplar), Prunus spp. (stone fruits including plums and peaches), Quercus spp. (oaks), Rosa spp. (roses), Rubus spp. (blackberry, raspberry), Tilia spp. (lime trees), Ulmus procera (English elm), Vitis spp. (grapes) and Zea mays (maize) (Vieira, 2008).

Given the polyphagous nature of P. japonica, detection surveys should target the most abundant host crops in the area, while in high-risk areas (see  Section 2.4 ) all the host plants should be considered. The information available from the outbreaks in northern Italy and the Azores (Portugal) shows that Vitis spp., Prunus spp., Zea mays, Glycine max and Rosa spp. are very attractive hosts and therefore, if present, these should be prioritised in detection surveys.

In the event of an outbreak, all the known host plants of P. japonica should be included in delimiting surveys. The MSs should evaluate their territory and identify whether P. japonica exhibits any preference for specific host plants. In northern Italy, wild Vitis spp., Rosa spp., Tilia spp., Parthenocissus spp. and Carpinus spp., which are widely present as ornamentals, are inspected with particular attention in delimiting surveys, as they have been found to be very attractive plants for P. japonica (Servizio Fitosanitario Regione Lombardia, 2022).

Soil moisture and temperature are the key parameters that may limit the potential establishment of the Japanese beetle in new areas. In North America, P. japonica distribution has been described as being adapted to regions where the mean soil temperature is between 17.5°C and 27.5°C during the summer and above -9.4°C in the winter (Fleming, 1972).

In Simonetto et al. (2022), soil and weather variables were the main factors in driving the presence of P. japonica larvae in northern Italy. Popillia japonica larvae showed a preference for less acidic soil, especially with sandy skeletal particles, and were found in high densities in soils with medium organic carbon content. Long drought periods or high precipitation levels reduce the probability of the presence of P. japonica (Simonetto et al., 2022).

A review of the thermal requirements of P. japonica for climate mapping was summarised from rearing experiments by Korycinska et al. (2015, table below).

Based on Régnière et al. (1981), the sum of degree days the beetle might need to complete its development into an adult is one or two years. In places with degree days above 1,422 and a threshold of 10°C the insect can complete its life cycle in one year, whereas in places with degree days above 711 and the same threshold, the life cycle is completed in two years (figure in the right panel). It is important to note that soil moisture – which corresponds with rainfall – is not considered in the figure in the right panel, but it is a relevant factor, since precipitation and soil moisture should be taken into account when considering establishment of P. japonica. In fact, despite the projection illustrated in the figure in the right panel, P. japonica completes its life cycle in one year in the current outbreak in Canton Ticino (Switzerland) (C. Marazzi, personal communication).

Given the polyphagous nature of P. japonica, many hosts are widely available throughout the EU MSs ( EFSA PLH Panel, 2018 ) and thus host availability is not a limiting factor for pest establishment. Therefore, it is expected that P. japonica could become established in all Member States where climatic conditions are suitable. The beetle is already established in the Azores (Portugal), Switzerland and northern Italy, and a high risk of spread to other countries with favourable conditions is assumed.

According to Bourke (1961) the Mediterranean region is not suitable for the establishment of the beetle due to the lack of summer rainfall, while in northern Europe, establishment was predicted to be less likely because summer temperatures are lower. In central Europe the climatic conditions for establishment were assumed to be most suitable, since summer rainfall is abundant and the temperature is favourable. In addition, extensive irrigation could increase suitability in some areas of southern Europe ( EFSA PLH Panel, 2018 ).

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

Popillia japonica can be detected in the field either by visual examination for the presence of adults on the host plants and/or the symptoms caused by the larvae and adults, and by setting up traps.

Trapping the adults is the preferred method to be used in detection surveys, i.e. in pest-free areas, possibly integrated with visual examination for the presence of adults or the symptoms caused by them. In the event of an outbreak, delimiting surveys should rely on visual examination for the adults and symptoms, while traps should not be used to avoid further spread of the beetles to pest-free areas. Soil sampling for larvae detection should be conducted if significant turf damage is evident.

3.1.1. Visual examination

Pest

The larvae live in the fibrous root zone of the plants and, therefore, can be detected only by soil sampling (refer to the section "Symptoms and signs"). The figure below shows a typical C-shaped creamy white grub of P. japonica in the soil. A distinctive morphological characteristic of P. japonica larva is the ventral side of the tenth abdominal segment which bears two medial rows, usually of six to seven spines (four to nine may be possible) in a characteristic V shape ( EPPO, 2022d ). They may be seen with a hand lens and if they are not present, the larva belongs to a species other than P. japonica (CFIA, 2017). Further microscopic identification in the lab might be needed to distinguish P. japonica larvae from closely related species ( EPPO, 2016 ).

Adults of P. japonica can be detected by visual examination of the leaves, flowers and petals and fruits of host plants (figures below). Adult beetles feed in groups initially at the top of the plant and move downwards (Vieira, 2008). The adults are more visible on the vegetation during cooler times of day. For visual examination of adult beetles, it should be kept in mind that odour and sun exposition are very important factors for plant selection by the P. japonica. The Japanese beetle tends to feed on full-sun plants with a top-down feeding pattern (Rowe and Potter 1996; Zavala, et al., 2009).

The adult beetle is brightly coloured metallic green and coppery bronze, oval in shape, and varies in size from 8 to 11 mm in length and 5 to 7 mm wide (figure below). The female is typically larger than the male. There are five lateral tufts of white hair on the abdomen plus one patch of white hair on the pygidium (total six) for each side of the body ( EPPO, 2006 ). Male and female beetles can be differentiated from each other by the shape of the tibia and tarsus on the foreleg. The male tibial spur is more sharply pointed, and the tarsi are shorter and stouter than those of the female ( EPPO, 2006 ).

Further details on how to carry out visual examinations for the adult beetles can be found in Appendix 2 of  EPPO (2016) .

Symptoms and signs

Turf damage is an indication that a large number of larvae could be present in the soil (figure in the right panel). If symptoms of larval damage are observed, soil should be sampled to confirm P. japonica detection. However, damage from larvae has been observed in Italy with a 2–3-year lag (M. Ciampitti, personal communication), thus visual examination for larval damage is not the recommended method for early detection. The larvae cause feeding damage to the roots of host plants and the signs caused are not at all specific ( EPPO, 2006 ). The larvae prefer areas with moist, loamy soil covered with turf or pasture grasses. They feed just below the surface, cutting and consuming the grass roots. Early symptoms include thinning, yellowing and wilting of grass (CABI, 2020).

Symptoms caused by the adults of P. japonica include defoliation and feeding holes in host leaves (figure in the right panel). The leaves can be skeletonised, leaving only the mid-vein intact ( EPPO, 2006 ) but this cannot be considered as confirmation of the presence of P. japonica, as other organisms such as small snails and insects can cause similar symptoms ( EPPO, 2016 ). The adult beetles can also feed on flower petals and cause direct damage by feeding on ripening fruit such as peaches, apples and small fruits (Davis, 1920) (figure below).

On corn, the beetles feed on the maturing silk, preventing pollination; this results in malformed kernels and a reduction in the yield (CABI, 2020). In northern Italy in extreme drought conditions, in addition to damage to the silk, damage inside the corn cobs was also observed (M. Ciampitti, personal communication) (figure in the right panel).

Popillia japonica feeding can facilitate feeding and aggregation of other scarab species. In the US, the green June beetle Cotinis nitida has been observed to aggregate in large numbers, to feed on ripening grapes whose skin has been previously pierced by feeding adults of P. japonica (Hammons et al., 2008). Similarly, in northern Italy the green rose chafer Cetonia aurata can be seen aggregating in high numbers (M. Ciampitti, personal communication). Thus, an increase in aggregation of scarab beetles can indicate the presence of P. japonica (figure in the right panel).

3.1.2. Trapping

Traps are the recommended method for detection surveys and early detection of adults of P. japonica. The combination of sex pheromones and several synthetic floral volatiles produce a synergistic effect (Althoff and Rice, 2022), and thus traps should be baited with a combination of floral attractant (phenethyl propionate, eugenol, and geraniol (PEG)) and a sex attractant ((R,Z)-5-1-decenyl)dihydro-2(3H)-furanone) (Ladd et al., 1981; Ebbenga et al., 2022). In northern Italy, the lures last for one entire summer season (M. Ciampitti, personal communication).

Even though early studies reported beetle attraction to white, green and yellow, recent studies report that solid green traps reduce pollinator capture and trap beetles effectively (Sipolski et al., 2019). It is recommended that traps should be placed in a position so as to receive all-day sun or at least mid-day sun (10:00–15:00) ( EPPO, 2006 ). Traps should be placed 3–7.5 m away from hosts (excluding turf), to ensure that the beetles fall into the trap, rather than landing on the host plant. Traps placed immediately adjacent to tall, bushy plants or other objects could be of lower efficacy since dissemination of the lure may be hindered (USDA, 2016). It is thus recommended that traps are not set up on the hosts themselves but set up on a separate support.

The use of traps is not recommended in buffer zones, as this may contribute to further spread of the beetles from infested areas to previously pest-free areas due to the attractiveness of the traps. Traps in infested areas can be used as sentinel traps to monitor the flight period of the adults in the territory and for mass trapping. However, as a precaution, it is recommended to use the traps at least 1 km inside the boundary of the infested area.

Further information and details on how to set the traps for detection of adult beetles are provided in Appendix 4 of  EPPO (2016) .

3.1.3. Sample collection

Any beetles found in traps set up for detection surveys should be examined for the distinctive features of P. japonica. Specimens identified should be sent to the laboratory for confirmation ( EPPO, 2016 ). Traps should be checked at least once per month from June to September.

As previously stated, sampling the soil for larvae is ineffective for ensuring early detection, and should only be conducted when turf damage is evident, indicating the possible presence of larvae. The most used method for detecting P. japonica larvae is to extract cubic portions of soil, 20×20×20 cm. After extraction, the soil sample is inspected for the presence of larvae by breaking the soil into a tray using hand tools. Collected larvae should be put in sample tubes containing 70% alcohol and sent to the laboratory for confirmation. For further information on larva sampling refer to Appendix 3 of  EPPO (2016) .

3.1.4. Timing of detection and identification

The exact timing of the survey is dependent on the life cycle of the beetle, which depends on environmental conditions. Therefore, the timing for detection surveys should be dependent on the field conditions and on the life cycle occurring in the different MSs.

Flight activity is initiated on clear days when the temperature is higher than 21°C and the relative humidity is lower than 60%, while colder temperatures, higher humidity and windy days prevent flight (Fleming, 1972). Popillia japonica flies actively mainly during the hottest hours of summer (10:00–16:00), when wind streams are weak (Borgogno Mondino et al., 2022).

Popillia japonica adults feed extensively on clear summer days, when the temperature is between 21°C and 35°C and the relative humidity is above 60%. Adults feed less on cloudy and windy days and do not feed on rainy days (CFIA, 2017).

If the field conditions and life cycle of P. japonica are similar to the situation in northern Italy, it is recommended that visual examination for the adult beetles and the associated damage on the preferred host plants is conducted during June and July (figure below).

Traps should be set up when conditions favour the emergence of the adults. In northern Italy, traps are usually set up from mid-May and kept until the end of September (figure below).

Soil samples for larva detection should be taken when most of the larvae are in the second or third instar and they are nearer to the surface, and if symptoms of turf damage are evident ( EPPO, 2016 ). In northern Italy, soil sampling is conducted from February until May and from mid-August to October (figure below).

3.2.1. Morphological identification

Collected larvae and adults need to be examined in the laboratory under the microscope to identify the distinctive morphological characteristics of the pest. Further details on the morphological identification and a dichotomous key for Scarabaeoidea families and the Popillia genus are provided in Appendix 1 of  EPPO (2006) . ERSAF (2016) recommends morphological identification with a binocular microscope as a diagnostic method. For detailed diagnostics, refer to EPPO Standard PM 7/74(1) ( EPPO, 2006 ).

Risk of misidentification

Popillia japonica larvae and adults are very similar to the pest of European cultivated grasslands Phyllopertha horticola (figure below), which has a similar life cycle and biology (Korycinska et al., 2015). Popillia japonica can be distinguished from the latter by its shiny golden green thorax, and there are five lateral tufts of white hair on the abdomen plus one patch of white hair on the pygidium (total six) (figure in the right panel) on each side of the body ( EPPO, 2006 ).

3.2.2. Laboratory testing and other methods of identification

Molecular identification methods are available to identify P. japonica. Molecular identification can be used to confirm morphological analysis or when there are fragments of larvae or adults that are not well preserved. Molecular analysis consists of PCR testing with universal barcode primers and then sequencing. The sequences obtained can then be compared with standard P. japonica sequences, deposited in international databanks.

A diagnostic protocol for PCR test (LCO1490/HCO2198) has been prepared by Folmer et al. (1994). Rizzo et al. (2022) recently developed a SYBR green-based real-time PCR test for the identification of adults and larvae of P. japonica.

Information on what, where, when and how to conduct survey activities for P. japonica 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 P. japonica. 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., 2020).

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 

 Scientific opinion on the pest categorisation of Popillia japonica 

 Popillia japonica – Pest Report and Datasheet to support ranking of EU candidate 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