Popillia japonica
(Japanese beetle)

The Japanese beetle was first discovered in New Jersey, USA in 1916. It probably entered the USA as grubs with iris bulbs before 1912 when plant materials were first examined. Although not a pest in Japan, extensive, well-watered, turf, and a lack of parasites, allowed populations to rapidly build up and spread steadily west to the Mississippi River. The loss of the chlorinated hydrocarbon insecticides, and the end of the Federal quarantine on nursery stock, has allowed beetles to move into western states at a rapid rate. Beetles are pests of quarantine concern in the western USA and Europe. P. japonica was found on Terceira Island, Azores, Portugal in the 1980s. Again, extensive turf allowed establishment of beetles, population explosions, the infestation of that island, and subsequently of three more of the Azorean Islands. Beetles have moved considerably outside of the climatic conditions in their native Japan.

P. japonica originates from north-eastern Asia where it is native in northern Japan and in the far east of Russia (Fleming, 1972a). Fleming’s (1972a) report of P. japonica in China and Korea, probably referred to closely-related species, but not the Japanese beetle (Ping, 1988; Reed et al., 1990).

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.

In the USA, P. japonica, is established in all states boarding, or east of the Mississippi River, with the possible exception of Florida. Several western states have isolated established populations of the beetle. Pest survey data are submitted to NAPIS by participating USA states in the Cooperative Agricultural Pest Survey (CAPS) with USDA, APHIS, PPQ and the resulting distribution of P. japonica in the USA is mapped from 2001 to the present (2010), and can be found here: http://www.ceris.purdue.edu/napis/pests/jb/mgif/jbnation.gif. See also Smith et al. (1997).

In Russia, the last report of P. japonica restricted it to the South Kirile region of Sakhalin, on the island of Kunashir (Chebanov, 1977). It is absent in the EPPO region except for Terceira Island, Azores (Portugal), where the pest probably spread from the USA air base (Simoes, 1984). An infestation on the island of Faial was found in 1996. More recently Pico and San Miguel both become infested in 2006. Both Terceira and Faial are generally infested, but eradication programmes are being considered for the isolated infestations on Pico and San Miguel.

P. japonica is an A1 quarantine organism for EPPO (OEPP/EPPO, 1980), and is also of quarantine significance for CPPC, JUNAC, NAPPO, and OIRSA. Within the USA, P. japonica is the object of an USDA/APHIS quarantine, restricting interstate movement of aircraft from regulated airports (USDA-APHIS, 2004). The interstate shipment of plant material is covered by the US Domestic Japanese Beetle Harmonization Plan (National Plant Board, 2004). Very few of the P. japonica infestations in states west of the Mississippi River have been associated with movement of beetles by aircraft.

Temperature and particularly soil moisture are the main factors limiting potential spread of the beetle into new areas. According to Fleming (1972a), the Japanese beetle is adapted to regions were the mean soil temperature is between 17.5 and 27.5^oC during the summer, and above -9.4^oC in the winter. It should be noted that the winter temperature is 0.5-1.0 m below ground surface where the larvae overwinter. 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. The Japanese beetle distribution in the USA is far south of the beetle distribution in its native Japan. The distribution in Japan may be influenced by other species of Popillia, or other scarabs, competing for limited resources.

Allsopp (1996) used a computer-generated modified Match Index to analyze climatic suitability and predict the potential worldwide distribution of P. japonica. According to the model, in North America the beetle has the potential to spread west to the middle of Nebraska, Kansas, Oklahoma, and Texas, south to the middle of South Carolina and Georgia, and most of Alabama and Mississippi. The Japanese beetle has already met or exceeded all of these parameters in the past 12 years. The southern parts of the Canadian Maritimes and eastern British Columbia, and parts of Washington and Oregon are also suitable. Indeed, Oregon has had several P. japonica infestations, as has California, and now Colorado and Utah. In addition Ontario, Quebec and Nova Scotia all have infestations in eastern Canada. Most of continental Europe, except most of Scandinavia and the Mediterranean areas, are suitable, as are the UK and Ireland. Suitable areas in Asia include the Caucasus and areas to the north, eastern central China, and the Korean Peninsula. In Africa, the mountains of Morocco and coastal south-eastern South Africa seem suitable. In the Southern Hemisphere, the south-eastern highlands of Australia, Tasmania, New Zealand, and the Rio de la Plata area between Argentina and Uruguay, and parts of costal Chile are suitable. Once established in these areas, P. japonica could cause enormous damage and significant economic loss. 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 the USA, adult P. japonica have been observed feeding on at least 295 species of plants in 79 plant families (Fleming, 1972a). 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, Anacardiaceae, Betulaceae, Clethraceae, Ericaceae, Fagaceae, Gramineae, Hippocastanaceae, Juglandaceae, Lauraceae, Leguminosae, Liliaceae, Lythraceae, Malvaceae, Onagraceae, Platanaceae, Polygonaceae, Rosaceae, Salicaceae, Tiliaceae, 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). Fleming (1972a) provided a detailed account of the biology of P. japonica. Larvae (mainly third-instar) overwinter in an earthen cell about 15-20 cm deep in the soil. In early spring, when the soil temperatures increase to about 10^oC, the grubs move closer to the surface and resume feeding on plant roots at 2.5 to 5.0 cm depth. Pupation usually occurs after 4-6 weeks of feeding, and the adults emerge from mid-May to mid-July, depending on latitude.

Mating begins at emergence, and egg-laying soon follows. Virgin females produce a volatile sex pheromone (Ladd, 1970), identified and called Japonilure (Tumlinson et al., 1977). Early in the seasonal flight period, aggregations containing up to many dozens of males form on the ground around a single, emerging female. Females also remate 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, 1972a; Rowe and Potter, 1996). The adults are attracted to feeding-induced plant volatiles, resulting in aggregation on damaged plants (Fleming, 1972a; Loughrin et al., 1996). Females may leave host plants during the day and fly to suitable sites for oviposition. Areas with moist, loamy soil covered with turf or pasture grasses are preferred (Fleming, 1972a; Allsopp et al., 1992). 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. At the latitude of Virginia and Maryland, the populations consist of mainly adults and eggs in July, first- and second-instars by mid-August, second- and third-instars by early September, and third-instars from late September to late April, and prepupae and pupae in May and early June. Normally, there is one generation per year, even in the most southern areas, but at the northern edge of its range, a few individuals may need 2 years to complete the life cycle (Fleming, 1972a; Vittum, 1986; Vittum et al., 1999).

Several indigenous, generalist, predators, especially ants and ground beetles, help to suppress Japanese beetle populations 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, crows, grackles, and gulls. Moles, skunks, raccoons and armadillos, feed on the grubs, but cause considerable damage to the turf or 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 Metarrhizium anisopliae and Beauveria bassiana, entomopathogenic nematodes including Steinernema and Heterorhabditis species, bacterial pathogens such as Paneibacillus popilliae, the protozoan, 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 OEPP/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), or for skeletonized leaves during the beetles flight period in early- to mid-summer. Adults are most active on warm days between 10 am and 3 pm. Traps containing the three part food-type lure (phenethyl propionate + eugenol + geraniol) and the sex attractant (Japonilure) (Ladd et al., 1981) are widely used in the USA and Azores for monitoring and survey purposes, and to delineate infestations. Grubs can be detected by cutting sections of sod with 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 (1972a) 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 when planning a landscape, or replacing damaged plant material, is a key to managing adults. Highly susceptible trees such as Sassafras, Prunus cerasifera, Ancer ploatanoides, and Tillia 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 arundinacae or perennial ryegrass, Lolium perenne, with fungal endophytes (Neotyphodium spp.) does not provide resistance to this pest.

Physical removal and exclusion

Hand removal may provide some control for small plantings. Beetles on plants are sluggish in the morning, before 9 am, or when the temperature is <21^oC, and can be killed by picking them, or shaking them, into a bucket of soapy water (Ladd and Klein, 1982). This is most effective when done before damage to the plants. High-value plants such as roses 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, Japanese beetle traps are an important tool in the identification and delimitation of new P. japonica infestations. California (Potter and Held, 2002) and Oregon monitor 10,000 and 5,000 traps per year, respectively, and have both eradicated isolated infestations in their states. Other western states utilize traps to a lesser extent. 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).

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 Japanese beetle-infested areas in the USA (Fleming, 1968). Only a few of these became established, the most widely distributed are Tiphia vernalis, a wasp that parasitizes overwintered grubs in the spring, and Istocheta aldrichi, a tachinid fly that parasitizes adults (http://www.oardc.ohio-state.edu/biologicalcontrol). The spring Tiphia seems to be well-established throughout the beetle-inhabiting areas. Istocheta 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). A third established parasitoid, Tiphia popilliavora, the fall tiphia, has not been recovered since 1969, although isolated populations may still be present. These parasitoids provide some suppression, particularly I. aldrichi, in areas with restricted turf, but 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 Japanese beetle populations, 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 larvacidal activity against P. japonica and other grubs (Ohba et al., 1992; Alm et al., 1997), but lacks a commercial product in the USA.

Entomopathogenic nematodes in the genera Steinernema and Heterorhabditis are the most commonly used pathogens against P. japonica. Nematodes such as Steinernema glaseri and Heterorhabditis bacteriophora are better-adapted to locate and parasitize the grubs in the soil (Gaugler et al., 1997). Wright et al. (1988) showed that nematodes could be used to control P. japonica grubs in container-grown nursery plants. Techniques for using these nematodes can be found at http://www.oardc.ohio-state.edu/nematodes, or in the training video “Entomopathogenic Nematodes: Tools for pest management” (Gaugler and Klein, 1998). Autodissemination of the fungus Metarrhizium anisopliae has been used to suppress Japanese beetle populations 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).

Phytosanitary Measures

Control of larvae in nursery stock is a far greater problem with quarantine concerns. Approved procedures are limited to chlorpyrifos dips of balled and burlapped nursery stock, and application of Marathon (imidacloprid) and Discus (imidacloprid + cyfouthrin) to field stock (Mannion et al., 2000; 2001; National Plant Board, 2004; Oliver et al., 2007). None of these materials provide 100% mortality of grubs, resulting in the three west-coast states (CA, OR, WA) prohibiting plants with any soil. Adult beetles are usually eliminated from fresh produce by commercial grading. However, grading has failed to remove P. japonica from blueberries, where adult beetles eat inside the berry and can not be seen. Movement of beetles by aircraft from infested to protected States is regulated by USDA/APHIS (2004). 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 retreated if live beetles are found.

27/03/2008 Updated by:

Michael Klein, Ohio Agricultural Research and Development Center, Adjunct Associate Professor, 1680 Madison Avenue, Wooster, OH 44691, USA