Popillia japonica
(Japanese beetle)

In its native country of Japan, Popillia japonica is a minor pest because natural enemies suppress populations and the terrain is generally unsuitable for larval development. P. japonica was first discovered near Riverton, New Jersey, USA in 1916. It was found at a nursery and was likely transported as larvae on imported rhizomes of the Japanese iris before 1912, when plant materials were first examined. Its westward expansion has been successful due to favourable groundcover (turfgrass) for larval development, adequate rainfall and limited natural enemies, though human-assisted movement likely played a role. The loss of the chlorinated hydrocarbon insecticides and the end of the Federal quarantine on nursery stock, has allowed beetles to move westward at a rapid rate. Additionally, P. japonica was found on Terceira Island, Azores, Portugal in the 1970s and extensive turf allowed establishment of the beetles and infestation of the island. P. japonica has moved considerably outside of the climatic conditions in its native range and is a pest of quarantine concern throughout many parts of the world. Information about quarantines and regulations for P. japonica in the USA can be found here: https://www.aphis.usda.gov/aphis/ourfocus/planthealth/plant-pest-and-disease-programs/pests-and-diseases/japanese-beetle/japanese-beetle.

Popillia japonica originates from northeastern Asia where it is native in northern Japan and in the far east of Russia (Fleming, 1972). Fleming’s (1972) report of P. japonica in China and Korea was likely incorrect and probably referred to closely-related species (Ping, 1988; Reed et al., 1991).

In Japan, the beetle is most abundant in northern Honshu and all of Hokkaido where grasslands occur, but it does not reach the high population densities that occur in the USA. It is common, but not abundant in Kyushu, Shikoku and southern Honshu. It was not considered to be a pest in Japan until the increase in golf courses and is still not the major scarab pest species. The distribution in Japan may be influenced by other species of Popillia, or other scarabs, competing for limited resources.

The distribution of P. japonica in the USA is far south of the beetle distribution in its native Japan. In the USA, P. japonica is established in all states east of the Mississippi River, with the exception of Florida and the states bordering the Mississippi River immediately to the west, with the exception of Louisiana. Mississippi is considered to have a partial infestation (Shanovich et al., 2019). Several western states have partial infestations of the beetle. Pest survey data are submitted to NAPIS by participating USA states in the Cooperative Agricultural Pest Survey (CAPS) with USDA, APHIS and PPQ and the resulting distribution of P. japonica in the USA is mapped from 2011 to the present (2020) and can be found here at CERIS (2020). Note that this is survey data and the accuracy of this data relies on state participation. It is interesting to note that unlike the weevils, no scarab has established on the opposite side of the equator from its native land (Jackson and Klein, 2006).

In Russia, the last report of P. japonica restricted it to the South Kuril region of Sakhalin, on the island of Kunashir (Chebanov, 1977). An accidental introduction from a US air base led to the establishment of P. japonica on Terceira Island, part of the Azores Islands of Portugal (Simoes, 1984). Since then, the islands of Faial, Flores, Graciosa, Pico, Sao Jorge and Sao Miguel have become infested (EPPO, 2019b). P. japonica was detected in Italy in 2014, which was its first report in mainland Europe (EPPO, 2014), and Switzerland in 2017 (EPPO, 2017). Damage to plants (vineyards in Switzerland; vineyards, field crops, fruit trees, small fruits and ornamentals in Italy) was observed in 2020 for the first time since introduction to these countries; however, official measures are being taken to eradicate the pest from mainland Europe.

Popillia japonica is an A2 quarantine organism for EPPO (EPPO, 2019a), which means the pest is present in the region but not widely distributed. Other regional plant protection organizations (RPPOs) that list P. japonica as an A2 quarantine pest include APPPC and COSAVE. P. japonica is on the A1 list for the CAHFSA, CAN and OIRSA RPPOs as well as several African, Asian, South American and European countries, meaning the pest is not yet present in these areas but is of quarantine concern. In North America, P. japonica is considered a quarantine pest that is being officially controlled. Within the USA, P. japonica is the object of a USDA/APHIS quarantine that restricts interstate movement by aircraft from regulated airports to nine western states (USDA/APHIS, 2016). The interstate shipment of plant material is covered by the US Domestic Japanese Beetle Harmonization Plan (National Plant Board, 2016). Very few of the P. japonica infestations in states west of the Mississippi River have been associated with movement of beetles by aircraft. Many isolated reports in western states were associated with parks, golf courses, or lawns.

Temperature and soil moisture are the main factors limiting potential spread of the beetle into new areas. According to Fleming (1972), P. japonica is adapted to regions were the mean soil temperature at 0.5 to 1 m depth, where the larvae overwinter, is between 17.5 and 27.5^°C during the summer and above -9.4°C in the winter. In addition, precipitation must be adequate and rather uniformly distributed throughout the year, averaging at least 25 cm during the summer. However, these parameters were established before irrigation was prevalent in much of the Midwest and Western USA.

Allsopp (1996) used a computer-generated modified Match Index to analyse climatic suitability and predict the potential worldwide distribution of P. japonica. P. japonica has met or exceeded the North American distribution predicted by Allsopp (1996). It was also predicted that most of Europe, east-central China, the Korean Peninsula and parts of the Caucasus region, Australia, New Zealand, South Africa and South America were suitable. P. japonica is mostly absent from those areas. The results of a bioclimatic niche model developed by Kistner-Thomas (2019) were mostly consistent with Allsopp (1996) and others: extreme low winter temperatures limit the northern distribution of P. japonica and persistent warm, wet conditions are limiting in the southern tropics. Eastern Asia, central Europe, portions of southern and eastern South America, sub-Saharan Africa, the North Island of New Zealand and the eastern coast of Australia are all suitable for the beetle under the current climate. In North America, the current distribution aligns with the predicted suitability under the current climate; however, there is potential for further invasion along the west coast and in the north central states.

The bioclimatic niche model also predicted the distribution in 2050 based on two global climate models (GCMs) and although there is much variability in the predicted suitable area for the two GCMs, some trends are revealed. Globally, the total suitable area for P. japonica does not change from the current climate predictions. However, suitable ranges tend to shift northward for areas in the Northern Hemisphere and contract for most areas in the Southern Hemisphere. Increased heat stress (extended exposure above 34°C) constricts the beetle’s range in portions of eastern Asia and North America below the 40^th Parallel North. Portions of British Columbia, Saskatoon and Manitoba are predicted to meet growing degree-day requirements under the future GCM models and more northern areas of Ontario and Quebec could be invaded with less cold stress. Northern European countries, such as Norway, Sweden, Finland, Ireland and the UK, become suitable by 2050 with these models. The suitable range for P. japonica in South America and Africa is expected to contract due to rising temperatures leading to increased heat stress. Australia may experience a minor reduction in potential range, while New Zealand’s suitable range expands.

In the USA, adult P. japonica have been observed feeding on at least 300 species of plants in 79 plant families (Fleming, 1972). These include small fruits, tree fruits, vegetable and garden crops, field crops, woody and herbaceous ornamentals, shade trees, various weeds and many non-economic species. Economic damage has been recorded on more than 100 species. The beetles are particularly attracted to certain species of Aceraceae [Sapindaceae], Anacardiaceae, Betulaceae, Clethraceae, Ericaceae, Fagaceae, Gramineae [Poaceae], Hippocastanaceae [Sapindaceae], Juglandaceae, Lauraceae, Leguminosae [Fabaceae], Liliaceae, Lythraceae, Malvaceae, Onagraceae, Platanaceae, Polygonaceae, Rosaceae, Salicaceae, Tiliaceae [Malvaceae], Ulmaceae and Vitaceae. The grubs feed on roots of a wide range of vegetable crops, ornamental plants and tender grasses. In Japan, the host range appears to be smaller than in North America.

Within the EPPO region, the host range of P. japonica would be similar. Malus, Prunus, Rubus and Vitis, with their wide distribution and intensive cultivation, would be especially favourable food sources for the adults. Lush pasture and turfgrasses provide a favourable habitat for the grubs.

Recent general reviews of P. japonica should be consulted for additional information on this pest (Potter, 1998; Vittum et al., 1999; Potter and Held, 2002; Jackson and Klein, 2006; Shanovich et al., 2019). Fleming (1972) provided a detailed account of the biology of P. japonica. Larvae (mainly third instar) overwinter about 5-15 cm deep in the soil, although a few may be up to 25 cm deep. In early spring, when the soil temperatures increase to about 10°C, the grubs move closer to the surface and resume feeding on plant roots at 2.5 to 5.0 cm depth. Pupation occurs in an earthen cell within the soil, usually after 4-6 weeks of feeding and the adults emerge from mid-May to mid-July, depending on latitude.

Mating begins shortly after emergence and egg laying soon follows. Virgin females produce a volatile sex pheromone (Ladd, 1970), which has been identified and called Japonilure (Tumlinson et al., 1977). Early in the seasonal flight period, aggregations containing several dozen males form on the ground around a single, emerging female. Females re-mate on food plants between bouts of oviposition, with the last male’s sperm being used. The beetles normally feed in groups, usually starting near the top of a plant and working downward (Fleming, 1972; Rowe and Potter, 1996). The adults are attracted to feeding-induced plant volatiles, resulting in aggregation on damaged plants (Fleming, 1972; Loughrin et al., 1996). Females may leave host plants during the day and fly to suitable sites for oviposition, unless the soil adjacent to the host plant is suitable. Areas with moist, loamy soil covered with turf or pasture grasses are preferred (Fleming, 1972; Allsopp et al., 1992). Low organic matter content, reduced tillage systems and sunlit areas are also preferred (Smith et al., 1988; Dalthorp et al., 1999; Dalthorp et al., 2000). Eggs are laid singly or in small clusters (2-4 eggs) in the upper 7.5 cm of soil. The cycle of feeding, mating and oviposition is repeated every few days. The average lifespan of a female is 30-45 days, during which she may lay 40-60 eggs.

Eggs hatch in about 2 weeks and the young larvae begin feeding on fine roots and organic matter. They moult and become second-instars after 2-3 weeks and third instars after 3-4 weeks more. Feeding continues until late autumn, when the grubs move deeper into the soil in response to declining soil temperatures to prepare for overwintering. Normally, there is one generation per year, but at the northern edge of its range a portion of the population may need 2 years to complete the life cycle (Fleming, 1972; Vittum, 1986; Vittum et al., 1999). Kistner-Thomas (2019) projected that many areas with a biannual life cycle will transition to an annual life cycle by 2050.

Several indigenous, generalist predators, especially ants [Formicidae], rove beetles and ground beetles [Carabidae], help to suppress populations of P. japonica by feeding on eggs and grubs (Terry et al., 1993; Zenger and Gibb, 2001). Both adults and larvae are fed upon by various birds including starlings [Sturnidae], crows [Corvus], grackles and gulls [Laridae]. Moles [Talpidae], skunks, raccoons [Procyon lotor] and armadillos [Dasypodidae] feed on the grubs, but cause considerable damage to turf and pastures. No native parasitic insect attacks P. japonica in North America. However, at least three species of imported parasitic insects have become established in eastern and Midwest states (see 'Prevention and Control'). Grubs are susceptible to several naturally-occurring fungal pathogens including Metarhizium anisopliae and Beauveria bassiana, entomopathogenic nematodes including Steinernema and Heterorhabditis species, bacterial pathogens such as Paenibacillus popilliae, the microsporidian, Ovavesicula popilliae and the rickettsia Rickettsiella popilliae. Unfortunately, humans are also susceptible to the rickettsia.

For further information, see reviews by Fleming (1968), Potter and Held (2002) and Jackson and Klein (2006) and the text section on 'Prevention and Control'. Natural enemy records from older literature are presented in the 'Natural Enemy' table and referenced as Fleming (1968).

A diagnostic protocol for P. japonica is given in EPPO (2006).

Adult P. japonica are easily detected by inspecting the most vulnerable plants for aggregations of beetles on foliage, flowers, or fruits (not blueberries (Vaccinium)), or for skeletonized leaves during the beetles’ flight period in early- to mid-summer. Adults are most active on warm days between 10:00 and 15:00. Traps containing the three part food-type lure (phenethyl propionate + eugenol + geraniol) and the sex attractant (Japonilure) (Ladd et al., 1981) are widely used for monitoring and survey purposes and to delineate infestations. Grubs can be detected in sod and field crops by using a spade or golf cup cutter in late summer, autumn, or in early spring and examining the soil and roots to a depth of about 8 cm. For grubs in nursery trees, removal and examination of soil down to 30 cm may be required to get an accurate sample.

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Introduction

The destructive potential and economic importance of this pest have led to intensive studies of various means for control. Note that the adults and grubs cause very different types of damage, above ground and below ground. Because the adults can fly considerable distances, controlling one life stage will not necessarily preclude problems with the other.

Control

Host-plant resistance

Fleming (1972) provided a ranking of the extent of feeding by adult P. japonica on 435 plant species in 95 families. Within some generally susceptible genera such as Betula, Malus and Tilia, less susceptible cultivars have been found (Ranney and Walgenbach, 1992; Spicer et al., 1995; Potter et al., 1998). Use of resistant or less susceptible species and cultivars is key to managing adults and replacing damaged plant material can help reduce infestations. Highly susceptible trees such as Sassafras, Prunus cerasifera, Acer platanoides and Tilia spp., or certain wild plants, such as species of Malva, Parthenocissus, Polygonum and Vitis, will attract numerous beetles.

Although tolerance varies, all species of cool-season turfgrasses are susceptible to the grubs (Potter et al., 1992). Infection of tall fescue, Festuca arundinacea, or perennial ryegrass, Lolium perenne, with fungal endophytes (Neotyphodium spp.) does not provide resistance to this pest. Host-plant resistance has been discovered in soyabean (Glycine max) germplasm, though it is unclear whether host-plant resistance is effective for defoliating pests (Hammond et al., 2001).

Physical removal and exclusion

Hand removal may provide some control for small plantings. Beetles on plants are sluggish when the temperature is <21°C and can be killed by dislodging them into a bucket of soapy water (Ladd and Klein, 1982). This is most effective when done before plants have been damaged and the most effective timing is probably in the evening (around 19:00; Switzer and Cumming, 2014). High-value plants such as roses (Rosa) can be protected with fine netting or Reemay fabric around each blossom during the period of beetle activity.

Trapping

Although mass trapping has held isolated populations in check and reduced the regulatory situation at some airports, it has not been effective in reducing established P. japonica infestations. However, traps are an important tool in the identification and delimitation of new P. japonica infestations. California (Potter and Held, 2002) and Oregon monitor thousands of traps each year and both states have eradicated isolated infestations. Other western states utilize traps to a lesser extent. Trapping efforts in Wyoming led to the first confirmation of P. japonica in the state in 2020 (CERIS, 2020). Small-scale trapping may aggravate defoliation damage in landscapes because the traps may attract more beetles than actually enter the traps (Gordon and Potter, 1985). Although beetles can fly up to 5 miles, they rarely do and are not attracted to traps more than 50-100 m away (Lacey et al., 1994).

Cultural Control

Female beetles seek out sites that are most optimal for egg laying and survival (Allsopp et al., 1992). Withholding irrigation during peak beetle flight can help to reduce subsequent grub populations in time of drought and in naturally dry areas (Potter et al., 1996). In contrast, rainfall or irrigation in summer and early autumn, during early instar feeding, promotes tolerance and recovery of grub-damaged turfgrass. Vigorous, well-watered turf can withstand two to three times the normal threshold of grubs (ca. 100/m²) that would destroy a weak, wilted, or starved sward. Raising cutting height and maintaining a balanced fertility regime to promote growth of roots also enhances tolerance of root-feeding by grubs (Crutchfield et al., 1995). UV-blocking plastics may be valuable for reducing damage to horticultural crops by adult P. japonica in high-tunnel and greenhouse systems (Cramer et al., 2019).

Biological Control

During 1920-1933, the USDA imported about 49 species of parasites of P. japonica and related scarabs from the orient and Australia and released them into infested areas in the USA (Fleming, 1968). Only a few of these became established, the most widely distributed are Tiphia vernalis, or the spring Tiphia, a wasp that parasitizes overwintered grubs in the spring and Istocheta aldrichi, a tachinid fly that parasitizes adults. The spring Tiphia seems to be well-established throughout the beetle-inhabiting areas. I. aldrichi had been restricted to the New England states, but has recently been established in North Carolina, Michigan, Minnesota and Missouri, USA (Jackson and Klein, 2006) and in Quebec, Canada (O’Hara, 2014; Gagnon and Giroux, 2019). A third established parasitoid, Tiphia popilliavora, the fall Tiphia, has not been recovered since 1969, although isolated populations may still be present. Unfortunately, these parasitoids do not usually provide adequate beetle control.

Spores of Paenibacillus (=Bacillus) popilliae, the primary causal agent of milky disease in P. japonica, were widely distributed in colonization programmes around the middle of the last century in eastern USA (Fleming, 1968). Although milky disease is one of the primary natural biological agents reducing populations of P. japonica, the value of augmenting this natural incidence with commercial spore powder has come under question (Redmond and Potter, 1995; Potter and Held, 2002; Jackson and Klein, 2006). Another bacterium, Bacillus thuringiensis - serovar japonensis, strain Buibui, has shown strong larvicidal activity against P. japonica and other grubs (Ohba et al., 1992; Alm et al., 1997), but lacks a commercial product in the USA. A microsporidian pathogen, Ovavesicula popilliae, which has a high specificity to P. japonica, has shown strong activity against larvae in field studies at epizootic sites (Piombino et al., 2020).

Entomopathogenic nematodes in the genera Steinernema and Heterorhabditis are the most commonly used pathogens against P. japonica. A new species, Hexamermis popilliae n. sp., was described parasitizing larvae of P. japonica in Italy (Mazza et al., 2017). Nematodes such as Steinernema glaseri and Heterorhabditis bacteriophora are better-adapted to locate and parasitize the grubs in the soil (Gaugler et al., 1997; Marianelli et al., 2017). Wright et al. (1988) showed that nematodes could be used to control P. japonica grubs in container-grown nursery plants. Effective use of nematodes for biological control of insect pests requires sufficient application rates and appropriate environmental conditions: applications should not be made in direct sunlight and soil needs to be kept moist for weeks after application (Georgis and Gaugler, 1991). Autodissemination of the fungus Metarhizium anisopliae has been used to suppress populations of P. japonica in the Azores and the USA (Klein and Lacey, 1999; Vega et al., 2007).

Chemical Control

Adult beetles have been controlled by treating susceptible plants with carbamates, organophosphates, or more recently, pyrethroid insecticides (Potter, 1998; Potter and Held, 2002). After the banning of long-residual insecticides, grubs were treated with short-residual organophosphates and carbamates. More recently, neonicotinyl (imidacloprid) and moult accelerators (halofenozide) have been used for preventive larval control in turf (Potter and Held, 2002) and may have an effect for more than 1 year (George et al., 2007). Long-lasting insecticide-treated nets, similar to those used for mosquitos, paralyze adult P. japonica with exposures as short as 5 s, though their utility in an IPM programme is yet to be determined (Marianelli et al., 2019).

Phytosanitary Measures

Control of larvae in nursery stock is a far greater problem with quarantine concerns. Approved procedures include dip treatments, drenches, media incorporation, fumigation and pre-harvest soil surface treatments (National Plant Board, 2016; approved chemicals detailed therein). Adult control in nursery stock includes foliage and shipping container (including truck/trailer) insecticide treatments. Adult beetles are usually eliminated from fresh produce by commercial grading. However, grading has failed to remove P. japonica from blueberries (Vaccinium), where adult beetles eat inside the berry and cannot be seen. Movement of beetles by aircraft from infested to protected states is regulated by USDA/APHIS (2016). Compliance agreements require aircraft at regulated airports to be sprayed with an insecticide. In addition, express package services have expended millions of dollars to use physical excluders and teams of beetle spotters to reduce the chance of beetles getting on a plane. Aircraft are examined upon arrival in protected USA states and re-treated if live beetles are found.

19/10/2020 Updated by:

Erin Hodgson, Iowa State University, Department of Entomology, USA

Ashley Dean, Iowa State University, Department of Entomology, USA

27/03/2008 Updated by:

Michael Klein, Ohio Agricultural Research and Development Center, USA