Exomala orientalis (oriental beetle)

E. orientalis is an exotic, invasive species in the USA. E. orientalis was probably a native of the Philippine Islands, carried to Japan and was introduced from Japan to the USA. Some time before 1908, it was introduced to the Hawaiian Island of Oahu, where it became a serious pest of sugarcane (Saccharum officinarum). On the mainland, the adults were first collected in 1920 in a New Haven (Connecticut) nursery, having presumably been imported directly from Japan in infested nursery stock. In view of the fact that this nursery imported plants, some of them with earth around the roots, from Japan in 1911, 1912 and 1916, it is probable that the insect came directly from Japan on imported nursery stock. Twelve years later, E. orientalis was limited to an area within 145 km of New York City. It is currently present in twelve north-eastern states and North Carolina (Alm et al., 1999).

Waterhouse first described E. orientalis in 1875 as Phyllopertha orientalis. It was subsequently reclassified as Anomala orientalis (Heyden, 1887) but it is now placed within the genus Exomala (Reitter, 1903). E. orientalis is in American literature and Blitopertha orientalis is in Japanese literature (see Alm et al., 1995). However, both names are in Korean literature (Choo et al., 2002b).

E. orientalis is distributed in Japan, Micronesia, Hawaii, eastern states in the USA, Korea (North and South) (Kim, 1996; Choo et al., 2002b) and China (Smith et al., 1992). E. orientalis was carried to Japan and introduced to the USA (Tashiro, 1987). In Korea, E. orientalis is found from all areas, but information of its distribution is not known.

Waterhouse first described E. orientalis in 1875 from specimens taken in Japan and the habitat was given as Kawachi, Nagasaki and Hakodadi. According to Muir, some time before 1908 it was imported into Hawaii and became established in the cane fields on the island of Oahu, Hawaii. In 1920, adults were collected in a nursery in New Haven, Connecticut and in 1922 a complaint was received. In 1926, E. orientalis was discovered in Jericho, Long Island and New York, USA. It has since been found in large numbers there and neighbouring towns. Since 1925, a few beetles have been found in several towns of Westchester county in New York and Elizabeth in New Jersey (Friend, 1929). Using pheromone trap research, Alm et al. (1999) reported that E. orientalis was distributed in Cape Cod, Central Massachusetts, Delaware, south-eastern New Hampshire, North Carolina, Ohio, Maryland, New Jersey and Virginia. Recently Tennessee, West Virginia, Maine and South Carolina were newly detected areas of E. orientalis in the USA. The natural spread of E. orientalis has been slow, presumably because it is not a strong flier (Hallock, 1933; Bianchi, 1935). The major root of spread of E. orientalis is via the shipment of nursery stock (Alm et al., 1999).

E. orientalis is exotic in the USA. This insect entered directly from Japan with infested nursery stock (Friend, 1929). As pests of nursery stock, the larvae have been shipped to new locations in containers or balled and burlaped plants (Alm et al., 1995). E. orientalis is an A1 quarantine pest in the EPPO region (Smith et al., 1992) and is also of quarantine significance for OIRSA (Organismo Internacional Regional de Sanidad Agropecuaria). If it is introduced into new regions, E. orientalis can cause considerable losses to horticulture, especially to grass.

Little is known about the host range of E. orientalis adults. The adults chew the flowers of some plants and the larvae kill grasses by eating the roots close to the soil surface, especially of lawns and turf grasses in golf courses (Arnett, 1985; Choo et al., 2002b). E. orientalis is a polyphagous pest, whose larvae feed on the roots of most grasses, ornamental plants and many vegetable crops, and have been recorded in particular damaging maize (Zea mays), pineapples (Ananas comosus) and sugarcane (Saccharum officinarum) (Bianchi, 1935; Westcott, 1964; Alm et al., 1995). It also infests strawberry beds and nursery stock, as well as the roots of potted plants that are grown outdoors (Potter, 1998). The adults feed on flowers of Alcea rosea, Dahlia spp., Iris spp., Phlox spp., roses (Friend, 1929), Castanea crenata, Euonymus japonicus and Nandina domestica (Choo et al., 2002b).

The symptoms of E. orientalis larval infestation in turf grass are expressed as dead patches (Choo et al., 2002b), but normally these are not easily seen during the 4 or 5 years of infestation. The larvae feed on grass roots within 2.5 cm of the soil surface. Densities of 40-60 grubs per 0.1 m² are fairly common and cause severe damage. Early turf symptoms include gradual thinning, yellowing, wilting in spite of adequate soil moisture, and the appearance of scattered and irregular dead patches. As the damage continues, the dead patches join together and increase in size. Infested turf feels spongy underfoot because the grubs pull up the underlying soil (Potter, 1998). In dry and hot summers, and in autumn, the damaged turf becomes whitish and wilted. These plants die relatively quickly and in the cases of high grub density, dead and black or white patches appear. In the following spring, E. orientalis-damaged grass has reduced growth and greening because of a lack of vitality and destroyed roots.Feeding by E. orientalis adults is usually restricted to the flowers of some plants (Friend, 1929; Potter, 1998; Choo et al., 2002b). The adults occasionally cause a little damage by feeding on the flowers but they are not considered to be a serious pest.

All white grubs have similar signs of infection. In general, early damaged turf gradually thins, yellows and wilts in spite of adequate soil moisture, and scattered, irregular dead patches appear. Infested turf feels spongy underfoot because the grubs churn up the underlying soil (Potter, 1998). These are signs of damage by E. orientalis larvae. Nevertheless, many other white grubs show similar signs. Therefore, if some of these signs appear in the patches, it is recommended to collect white grubs from the damaged areas and examine the rasters of the grubs.

E. orientalis has a 1-year life cycle in Korea and New York, USA. The adults begin to emerge from late June, with peak emergence in mid-July in New York and a few may still be around into August (Facundo et al., 1999b), whereas they emerge from late May and peak in mid-June in Korea (Choo et al., 2002b). The adults are weak fliers, but they may fly short distances during the day. The adults are active in the evening from sunset, especially around 20.00 h (Choo et al., 2002b) and more males are captured than females in the turf grasses of golf courses (Facundo et al., 1999b; Choo et al., 2002b). The interval between mating and oviposition can be as short as 1 day, but is normally about 5 days. Oviposition occurs both during the day and night for up to 20 days after mating (Alm et al., 1995). The females deposit their eggs singly, 2.5-23 cm deep in damp soil. The females lay an average of 25 eggs, but some may deposit as many as 63 in June in Korea, but in July and early October in New York, USA. The egg stage lasts for approximately 17 to 25 days, depending upon temperature and moisture. First-instars may feed up to 30 days before moulting. The grub population consists mainly of first-instars in August, second-instars by early September and third-instars by early October in New York, USA whereas in Korea first-instars were observed in July. The grubs feed by severing plant roots close to the soil surface. Their depth in the soil depends on the soil texture and moisture. The larvae burrow deeper into the soil as the surface layer dries out during the summer. The damage usually appears by early September and third-instars by early October. E. orientalis responded rapidly to shifting temperature (Villani and Wright, 1988). As soil temperatures drop to about 9.9°C in October, the larvae move downward for hibernation. They hibernate in an earthen cell, 20-40 cm underground. In spring, as soil temperatures warm to 6.1°C during late March or early April, the grubs start to move upward. Feeding continues until early June, when the grubs again burrow down 8-23 cm to pupate. The prepupal and pupal periods last approximately 1 and 2 weeks, respectively. Most of the grubs pupate by mid- to late June (Friend, 1929; Alm et al., 1995; Potter, 1998). E. orientalis pupal development is initiated at 10°C (Keizi, 1997). The pupae usually vibrate the tips of their abdomens at the pupal period. The beetles begin emerging in late June, completing the annual cycle (Friend, 1929; Alm et al., 1995; Potter, 1998). The adults emerge 1 month earlier in Korea than in New York. According to observations on the developmental stage of E. orientalis on the fairway of golf courses in Korea, it has a 1-year life cycle (Choo et al., 2002b) and the first E. orientalis adults were observed in late May. Adult emergence increased during the first week of June and peaked on 12 June. The emergence slowed by 19 June and was nearly complete by 27 June. By early July, only the eggs were found. By late July a few eggs remained, but most of the population were first- or second-instars. Only the third-instars were found after early October. The density of larvae was 12.0/0.09 m² in late July but decreased to 0-3/0.09 m² by the mid-April of the following year (Choo et al., 2002b).

Genetics

Peng and Leal (2001) identified and cloned a pheromone-binding protein (EoriPBP) from the Japanese and American populations of E. orientalis. EoriPBP has 116 amino acids, with a calculated molecular mass of 12,981 Da, pI of 4.3, and six highly conserved cysteine residues. 5'-RACE amplifications led to the characterization of a signal peptide with 19 amino acids.

Reproductive Biology

The mating season of E. orientalis in New York, USA began in the middle of June, with a peak in the first week of July and ended in mid-August (Facundo et al., 1999b). However, this occurs 1 month earlier in Korea (Choo et al., 2002b). Both sexes were most active around sunset (Facundo et al., 1999b; Choo et al., 2002b). Mate acquisition and copulation occurred on the soil surface near the female emergence site, with both sexes engaging in pheromone-mediated behaviours after having emerged from the soil. A highly stereotyped female pheromone release or calling behaviour was observed, consisting of the insertion of the female's head into the soil and the elevation of the tip of her abdomen into the air. Mating and copulation occurred without an obvious complex courtship, but observations of postmating behaviours suggested that mate guarding occurs (Facundo et al., 1999a).

Associations

In Korea, the emergence time of E. orientalis is the same as blooming of Japanese chestnut (Castanea crenata). Early-, intermediate- and late-maturing varieties of Japanese chestnut are being grown in Korea. The adults were found on the flowers of the late-maturing chestnut variety because the flowers of the early and intermediate varieties were in senescence at the time of E. orientalis female emergence. Thus an outbreak of E. orientalis can be predicted by the blooming of late-maturing Japanese chestnut. The concentration of females on late-blooming Japanese chestnut trees led to higher densities of E. orientalis larvae. The late-blooming variety of Japanese chestnut tree is an important factor that affects the distribution of E. orientalis in turf grasses in Korea (Choo et al., 2002b).

Naturally occurring predators, parasites and diseases are important. Cophinopoda chinensis, Philonicus albiceps (Choo et al., 2000) and Promachus yesonicus (Choo et al., 2000) are predators and Scolia manilae [Campsomeris marginella modesta], Tiphia vernalis and Tiphia popilliavora are parasites of E. orientalis (Tashiro, 1987; Alm et al., 1995; Choo et al., 2000). Paenibacillus popilliae was the most effective bacterial disease in the larva of E. orientalis (Dutky, 1941; Tashiro, 1987; Choo et al., 2000; 2002b). The Bacillus thuringiensis serovar japonensis strain Buibui was effective against E. orientalis larvae (Suzuki et al., 1992; Alm et al., 1997; Koppenhöfer et al., 1999). Protozoan (Gregarinidae) were found in infested E. orientalis larvae (Hanula and Andreadis, 1988). The entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae, and the entomopathogenic nematodes, Steinernematidae and Heterorhabditidae were found in E. orientalis larvae (Choo et al., 2000).

Losses mainly arise from the larvae of E. orientalis feeding on the roots, which may be severely damaged, with crops turning brown and dying. In lawns, feeding by the overwintering larvae may kill the grass in June, but more often in August and September, with areas from a few square centimetres to 1-2 ha turning brown. In 1928, about 6 ha of lawn were injured in New State alone (Smith et al., 1992). It is considered the most serious grub pest of turf and woody ornamental plantings in Long Island, northern New Jersey and Connecticut, USA (Facundo et al., 1999b). Turf grasses now cover an estimated 10.1 to 12.1 million ha in the USA, and turf grass culture is at least a US$25 billion per year industry (Potter and Braman, 1991). Economic losses by E. orientalis larvae are serious in turf grasses. When scarab larvae were sampled at 15 golf courses in 11 provinces of Korea, the most abundant species was the E. orientalis (Choo et al., 1998b, 1999). Primary injury from larvae consuming turf roots is followed by secondary damage from wild birds searching for and feeding on grubs in the infested area (Choo et al., 2002b). Damage by E. orientalis in turf grasses is increasing in Korea.

The standard golf course hole cutter (11 cm diameter), or an oversized 15 cm diameter hole cutter are useful for the detection of the eggs, larvae and pupae of E. orientalis in turf grass (Schumann et al., 1998; Potter, 1998). The larvae are collected by handpicking though each soil core. They are identified using raster characteristics observed under a hand lens. Another method of sampling for grubs is to cut off sod using a flat-blade spade. Up to a 0.1 m² sample is cut on three sides to a depth of 7-10 cm and then the sod is turned back as if it were a flap. The soil is then broken up and the grubs detected (Schumann et al., 1998; Potter, 1998).A pheromone trap was a useful detection instrument for E. orientalis adults. Identification of the E. orientalis pheromone, (Z)-7-tetradecen-2-one (Leal, 1993; Leal et al., 1994; Facundo et al., 1994; Zhang et al., 1994; Alm et al., 1999) has made detection possible.

Cultural Control and Sanitary Methods

Cultural control consisted of adequate lime, fertilizer and irrigation to maintain healthy turf (Alm et al., 1995).

Host-Plant Resistance

All species of cool-season turf grasses and many warm-season grasses, are susceptible to attack by white grubs. Among cool-season grasses, tall fescue (Festuca arundiancea) is generally more tolerant of grub damage than Kentucky bluegrass (Poa pratensis), creeping bentgrass (Agrostis stolonifera) or perennial ryegrass (Lolium perenne) (Alm et al., 1995; Potter, 1998).

Biological Control

Biological control agents consisted of natural enemies and microbial agents. E. orientalis grubs were susceptible to milky disease, Paenibacillus popilliae (Dutky, 1941; Tashiro, 1987; Choo et al., 2000; 2002b). Populations of milky disease-infected E. orientalis grubs differed between sites and with time (Dunbar and Beard, 1975; Hanula and Andreadis, 1988; Choo et al., 2000, 2002b). The Bacillus thuringiensis serovar japonensis strain Buibui was effective against E. orientalis larva (Suzuki et al., 1992; Alm et al., 1997; Koppenhöfer et al., 1999). Protozoan (Gregarinidae) was found in infested E. orientalis larva (Hanula and Andreadis, 1988). Entomopathogenic nematodes (e.g. Steinernema spp. and Heterorhabditis bacteriophora) can provide good control of E. orientalis larvae (Alm et al., 1992; Yeh and Alm, 1995; Lee et al., 1997a; Koppenhöfer et al., 1999; Choo et al., 2002a; Lee et al., 2002a; Polavarapu et al., 2007). Several entomopathogenic fungi are active against E. orientalis. Metarizium anisopliae (Lee et al., 1997b; Yokoyama et al., 1998; Choo et al., 2000), Beauveria bassiana (Lee et al., 1997c) and Beauveria brongniartii (Choo et al., 2002a) are useful for the biological control of E. orientalis. The dipteran predators, Cophinopoda chinensis, Philonicus albiceps (Choo et al., 2000) and Promachus yesonicus (Choo et al., 2000) and hymenopteran parasitoids, Scolia manilae [Campsomeris marginella modesta], Tiphia vernalis and Tiphia popilliavora are natural enemies of E. orientalis (Tashiro, 1987; Alm et al., 1995; Choo et al., 2000). Biological control of this pest and the related Adoretus sinicus was attempted in Hawaii intermittently between 1916 and 1953. As a result, two scolioid parasitoids from related hosts in the Philippines became established: C. marginella modesta and Tiphia segregata, which achieved substantial control of E. orientalis (Pemberton, 1964). Later C. marginella modesta was successfully introduced into Guam from Hawaii where a fair degree of control was obtained (Clausen, 1978). On the USA mainland, a major programme for the control of Popillia japonica was carried out, which led to the establishment of T. popilliavora and T. vernalis that also parasitize other white grub pests including E. orientalis.

Chemical Control

Chemical control of adult E. orientalis has not been adequately tested and may not be practical in most situations (Alm et al., 1995). There are two methods concerning grub control: the curative or corrective approach and preventive control. Curative control is applied in the late summer, after the eggs have hatched and the grubs are present. Preventive control is applied as insurance, before a possible grub problem develops. Preventive control requires the use of an insecticide with a relatively long residual activity (e.g. imidacloprid, halofenozide) (Potter, 1998). Imidacloprid and halofenozide were recently registered for use on turf in the USA (Kunkel et al., 1999) and have good control efficacy for E. orientalis larvae (Cowles and Villani, 1996; Cowles et al., 1999) but stage-specific differences in susceptibility (Villani et al., 1988; Cowles and Villani, 1996). Isofenphos was also registered in the USA (Potter, 1998). The insecticides chlorpyrifos-methyl, ethofenprox, and imidaclopride, were registered for the control of the white grub on turf in the Republic of Korea (Anonymous, 2003).

Early Warning Systems

The use of sex pheromone traps (Leal, 1993; Facundo et al., 1994; Leal et al., 1994; Zhang et al., 1994; Alm et al., 1999; Polavarapu et al., 2002) to monitor the adults provides a warning of potential outbreaks.

Field Monitoring/Economic Threshold Levels

Wire-mesh emergence cones, pheromone traps or direct observation have been used for monitoring E. orientalis adult emergence or activity (Facundo et al., 1999b) and soil sampling is recommended for monitoring the larvae (Hellman, 1989; Potter, 1998). Indirect methods using the entrance and exit holes made by E. orientalis adults, which are active from sunset into the night, are practical for monitoring populations on the grass at Korean golf courses (Choo et al., 2002b). These entrance and exit holes are discrete and characteristic for E. orientalis adults (Choo et al., 1999). Another indirect monitoring method of E. orientalis distribution, is to check the presence of the Japanese chestnut and magpie damaged areas. The presence of the late-blooming variety of Japanese chestnut around the green and magpie damage are correlated with E. orientalis infestations (Choo et al., 2002b). Over 95% accuracy was obtained between real numbers and estimated numbers of E. orientalis larvae at a density of over 303 larvae/m² when areas of 20 by 20 cm were sampled in golf courses (Lee et al., 2002b). From 43 to 65 grubs per 0.1m² are often present, causing complete destruction of the turf (Tashiro, 1987) and 30 grubs per 0.1m² cause complete destruction of turf in Korean golf courses (Lee et al., 2002b). The presence of as many as 590 grubs per 0.1m² has been reported (Tashiro, 1987).

IPM Programmes

Checking for the occurrence of E. orientalis by observing the entrance and exit holes in the green of golf courses can aid in spraying decisions. The use of insecticide is expected to further decrease because of the concerns for the environment and human health (Choo et al., 2002a). Choo et al. (1998a) used a combination of biological control agents or insecticides and entomopathogenic nematodes against E. orientalis. In most cases, such combinations resulted in additive or synergistic effects.