Monochamus alternatus
(Japanese pine sawyer)

See also CABI/EPPO (1998, No. 105).

Several potentially effective phytosanitary measures are proposed: selective felling, removal, and debarking of healthy trees before the flight period of M. alternatus, inspection of wood in the mill, heat and chemical treatments, and so on (Evans et al., 1996).

Hosts of M. alternatus come from the family Pinaceae, particularly from the genus Pinus. The host range in Japan is summarized by Kojima and Nakamura (1986) and by Kishi (1995). P. echinata and Cryptomeria japonica are excluded from the host range list due to uncertainty over their status as hosts. Mineo and Kontani (1973) and Furuno (1982) reported attack by M. alternatus on pine species introduced to Japan. Wang (1983) and Song et al. (1991) describe the host range in China. Chen and Chao (1998) added P. taiwanensis to the host range.

Voltinism of M. alternatus varies in different areas. In Japan, M. alternatus requires one or two years to complete its life cycle. In China, the insect is univoltine in Jiangsu province (Wang, 1988) whereas it is bi- or trivoltine in Guangdong province under a subtropical climate (Song et al., 1991). M. alternatus overwinters at the aging larval stage (Togashi, 1989b,d; Song et al., 1991).

M. alternatus adults emerge from dead host trees between May and July in central Japan (Ochi and Katagiri, 1974b; Togashi and Magira, 1981). In Guangdong, China, in years when the insect is bivoltine, adults of the overwintering generation emerge between April and May and the first-generation adults between July and August. In years when a trivoltine lifecycle is observed, adults of the overwintering generation emerge between late March and early April, first-generation adults between late June and early July, and second-generations between mid-October and early November (Song et al., 1991).

The average life-span of adults is about 7 weeks in outdoor cages in central Japan (Togashi and Magira, 1981) and 12 to 13 weeks in Guangdong (Song et al., 1991). Adults have been recorded between early June and late September at a Pinus thunbergii stand in central Japan (Shibata, 1981; Togashi, 1988), where oviposition activity is sometimes recorded in October (Togashi, 1989b). Laboratory rearing allows them to survive more than 6 months (Togashi and Sekizuka, 1982).

Adults emerge from dead trees reproductively immature and feed on the bark of pine twigs. Males require at least 5 days before they are ready to inseminate females (Nobuchi, 1976) and females require an average of 3 weeks to oviposit although the variation in pre-oviposition period is large (Ido and Takeda, 1975). Acetone extractives of P. thunbergii bark from 1-year-old twigs elicit a stronger feeding response in M. alternatus adults than those from current-year twigs (Miyazaki et al., 1974). In the case of P. densiflora, methanol-soluble fraction from hot-water extractives of 1-year-old twig bark causes a stronger feeding response than those of current- and 2-year-old twig barks (Miyazaki et al., 1974). Feeding response to water extractives from P. thunbergii needles is much less than that to water extractives from the twig bark (Miyazaki et al., 1974). The foliage of P. densiflora contains ethane and saturated hydrocarbons with straight C5 to C10 chains which acts as a repellent to M. alternatus adults (Sumimoto et al., 1975). Adult females feeding on current-year twigs of P. densiflora develop ovaries fastest, followed by those feeding on 1- and then 2-year-old twigs in that order (Katsuyama et al., 1989).

Immature adults disperse by flying in a random direction (Togashi, 1990a). The combination of (+)-juniperol and (+)-pimaral in a certain ratio, which are isolated from healthy tree trunks of P. densiflora and P. thunbergii, attracts M. alternatus adults (Sakai and Yamasaki, 1990). The attractiveness, however, is diminished by (-)-germacrene D, which is isolated from foliage of healthy P. densiflora trees (Yamasaki et al., 1997). Reproductively mature adults are attracted to the monoterpenes and ethanol emitted by dying or recently killed Pinus trees (Ikeda and Oda, 1980; Ikeda et al., 1980). Thus, they tend to concentrate on host trees that are recently dead or dying, as well as the surrounding healthy trees (Shibata, 1986; Togashi, 1989c). Flight activity is higher before sexual maturity than after (Ito, 1982; Togashi, 1990b). In most cases M. alternatus is not a strong flier. The immature adults move 7 to 40 m per week in P. thunbergii stands (Togashi, 1990a). In a P. densiflora stand heavily infested with pine wilt disease, the adults moved an average of 10.6 to 12.3 m during their lifetime (Shibata, 1986). However, they have been known to fly a distance of 1 to 2 km (Fujioka, 1993). Adults are nocturnal (Nishimura, 1973).

In mating, the male is initially passive, staying motionless with his antennae widespread and emitting volatile pheromone which attracts the female (Fauziah et al. 1987; Kim et al., 1992). He dashes towards an approaching female, mounts her, and licks the female's elytra to calm her. Copulation occurs when she stops walking (Fauziah et al. 1987). A contact pheromone eliciting copulatory behaviour in the male is present on the body surface of female and male (Kim et al., 1992). A long pair-bond is formed in which repeated copulations occur with the ovipositing female (Fauziah et al., 1987). Adults of both sexes copulate with several mates. Both males and females obtain mates from already established pairs. The antennae are used to ward off other males and females (Fauziah et al., 1987).

For oviposition, the female gnaws at the bark surface with her mandibles to make a wound. Then, she turns 180° to position the ovipositor over the wound, inserts the ovipositor through the centre of the wound, and deposits a single egg in the inner bark. Before withdrawing her ovipositor from the wound, she deposits a jellylike secretion (about 1×1×1 mm) at the bottom of the central hole of the wound. Just after withdrawal, she rubs the wound with her abdominal tip (Anbutsu and Togashi, 2000). As females often deposit no eggs in the wound, the oviposition ratio, which is calculated by dividing the egg number by oviposition scar number, is about 0.5 (Togashi and Magira, 1981). Several compounds have been isolated from the inner bark of P. densiflora and are identified as oviposition stimulants: D-catechin, (2R, 3S)-3,5,7,3',4'-pentahydroxyflavan, (-)-2,3-trans-dihydroquercetin-3'-O-b-D-glucopyranoside, dihydroconiferyl alcohol-9-O-b-D-glucopyranoside, cedrusin-4'-O-b-D-glucopyranoside, cedrusin-4'-O-a-L- rhamnopyranoside, 7-O-methyl cedrusin-4'-O-a-L- rhamnopyranoside, and 1-(4'-hydroxy-3'-methoxyphenyl)-2-[4"-(3-hydroxypropyl)-2"-hydroxyphenoxy]-1,3-propanediol-4'-O-b-D-xylopyranoside (Islam et al., 1997; Sato et al., 1999a,b). Any compound is inactive alone. Larval frass and the jelly-like secretion deposited by the adult female prevent further oviposition on that part of the bark (Anbutsu and Togashi, 2001; 2002).

The mean age-specific fecundity curve is unimodal under outdoor conditions (Togashi and Magira, 1981). In Japan the mean lifetime fecundity varies depending on study site. It is 86.2 in Ishikawa Prefecture (Togashi and Magira, 1981) and 32.9 in Nara Prefecture (Shibata, 1987). The mean lifetime fecundity of early emerged females (157.3) is much more than that of mid- and late emerged females (78.0 and 23.5 respectively) (Togashi and Magira, 1981). Shortened longevity and the increased proportion of sterile females are the causes of the decrease in mean lifetime fecundity associated with later emergence (Togashi and Magira, 1981). The mean lifetime fecundity is 87.6 in Jiangsu province, China (Wang, 1988).

There is a large difference in lifetime fecundity among female adults, ranging from 0 to 343. Female lifetime fecundity and body size are positively correlated (Togashi, 1997). As the number of eggs deposited during a day by individual females does not largely change with age (Ochi, 1969; Togashi, 1997; Xu Z and Linit MJ, 1998), lifetime fecundity can be expressed as a product of oviposition rate and oviposition period. Increased body size contributes to lifetime fecundity through oviposition rate 24 times as much as through oviposition period (Togashi, 1997). Females have a mean of 22.5 ovarioles with no correlation between female body size and the number of ovarioles; this suggests that the increase in oviposition rate is explained by the increase in egg production rate per ovariole (Togashi, 1997).

Large females deposit larger eggs than small ones although small females deposit larger eggs relative to their body size (Togashi et al., 1997). Consequently, large females produce larger newly hatched larvae with larger head capsules than those produced by small females (Ochi, 1975).

The time period during which individual trees are subject to oviposition depends on when they are dying. Oviposition lasts for 1 to 2 months on trees dying from pine wilt disease in June and July and 1 to 4 weeks on trees dying in August and September (Togashi, 1989c). The number of oviposition scars per tree is greatest on trees dying in June and July and decreases as the time of tree death is delayed seasonally (Togashi, 1989c). After the oviposition season, oviposition scars show a clumped distribution among trees and among 50-cm-long bolts obtained from tree trunks (Shibata, 1984), but a uniform distribution on the bark surface of each bolt (Kobayashi, 1975; Shibata, 1984). Eggs also show a uniform distribution on surface of the bark (Shibata, 1984). Such uniform distribution may be induced by deterred oviposition of female adults due to the jellylike secretion deposited and larval frass (Anbutsu and Togashi, 2001; 2002). Oviposition scar density reaches 0.12 scars per cm² of trunk bark surface (Togashi, 1989c).

Thermal constant and developmental zero for egg development are 85.5 day-degrees and 12.9°C, respectively (Okuda, 1973). Larvae feed on inner bark to grow. The fourth larval instar is final (Ochi, 1975; Ochi and Katagiri, 1974a; Morimoto and Iwasaki, 1974a). The third- and fourth-instar larvae excavate a tunnel in the wood and enter it when they encounter danger (Togashi, 1989b,d). The tunnel extends first horizontally to the wood surface up to about 2 cm and then turns upward in standing tree trunks along the direction of the wood fibres (Togashi, 1980a). Before winter comes, they plug the entrance of the tunnel with wooden fibrous shreds. In central Japan M. alternatus overwinters at the first to fourth larval instars (Togashi, 1989b). Some larvae excavate a depression on the wood surface and pupate under the thick bark such as found in nodes of trunks (Togashi, 1980a). The proportion of larvae that pupate under the bark is larger in warm areas than in cool areas (Kishi et al., 1982). Well developed larvae enter diapause prior to winter (Togashi, 1989b). Diapause larvae are yellowish white to yellow and have no food in their intestines. Cold temperatures in winter terminate the diapause, so in the field, diapause is terminated by mid-February (Togashi, 1991b). Thermal constant and developmental zero are 333.3 day-degrees and 12.6°C respectively for post-diapause larvae to pupate and 526.3 day-degrees and 11.9°C for post-diapause larvae to eclose to adults (Enda, 1975). The pupal stage lasts for 12 or 13 days at 25°C (Yamane, 1974). Development analysis of field population shows that cold winter temperatures allows the third- and fourth-instar, pre-diapause larvae to skip the diapause and pupate in early summer (Togashi, 1989d). This was shown experimentally for pre-diapause, fourth-instar larvae by Togashi (1995). Larvae that overwinter at the first and second instars resume feeding after winter and then enter diapause. Cold winter temperatures terminate diapause, resulting in a two-year life cycle (Togashi, 1989b,c,d). Obligate diapause is observed in Japan (Okuda, 1969) whereas in Taiwan diapause is facultative (Enda and Kitajima, 1990).

Sound production by larvae begins soon after hatching and lasts till the end of feeding (Izumi and Okamoto, 1990). The larval mandibles are in contact with the wood wall of the gallery at the time of sound production (Izumi et al., 1990). However, the mechanism and function of sound production are unknown.

Newly eclosed adults are white except for their compound eyes, mandibles, and elytra (Yamane, 1974). They emerge from pupal chambers after the integument is sclerotized. The emergence hole on bark averages 9 mm in diameter. The emergence holes are distributed contagiously among trees but uniformly among 50-cm-long bolts obtained from tree trunks and bark surface (Shibata, 1984).

The survival rate of M. alternatus in trees is high. A field study conducted over 5 years showed that the mean survival rate from egg to adult stage at emergence is 0.249 in a P. thunbergii stand (Togashi, 1990c). It is estimated to be 0.289 in Kochi Prefecture, Japan (Ochi K and Katagiri, 1979). The highest survival rate is observed in trees dying in July (0.348) and the lowest in those dying in June (0.147). Key factor analysis shows that the third and fourth larval instars in pupal chamber are responsible for the fluctuation in survival rate up to adult emergence (Togashi, 1990c).

In the absence of natural enemies (excluding micro-organisms) the number of M. alternatus adults emerging per unit area of bark surface increases with increasing egg density, reaches a maximum, and then decreases slightly (Morimoto and Iwasaki, 1974b; Togashi, 1986). The density-dependent mortality factor responsible for this is intraspecific competition, which is ascribed to larvae killing each other with their mandibles and the competition for food resources (Togashi, 1986). The mortality of the early larval stage increases as the distance between newly hatched larvae decreases (Anbutsu and Togashi, 1997). Early-hatched larvae always kill late-hatched ones when they encounter each other (Anbutsu and Togashi, 1997). Thus, oviposition by adult females under bark that is not infested with oviposition scars and larval frass may increase the survival of her offspring (Anbutsu and Togashi, 1996). In contrast, the mortality from natural enemies such as insects and birds is reported to be density-independent (Togashi, 1986). One of the reasons for a density-independent manner by natural enemies is that they utilize sympatric weevils and bark beetles.

M. alternatus adults transmit the pinewood nematode, Bursaphelenchus xylophilus, which causes pine wilt disease and reproduces in dead trees (Mamiya and Enda, 1972; Morimoto and Iwasaki, 1972). The final instar larvae of M. alternatus excrete palmitoleic, oleic and linoleic acids which concentrate the nematode in the pupal chamber (Miyazaki et al., 1977a,b). Toluene and o-xylene isolated from beetle adults also attract the nematode (Shuto and Watanabe, 1987). The nematodes, attracted by the emitted carbon dioxide (Miyazaki et al., 1978) enter the tracheal system through the spiracles of newly-eclosed beetles (Mamiya, 1972).

There is a great variation in the number of nematodes harboured in a M. alternatus adult, ranging from 0 to over 100,000 (Mamiya and Enda, 1972; Morimoto and Iwasaki, 1972). The maximum recorded in Japan is 289,000 (Kishi, 1995). The nematode load of adults at emergence is influenced by the fresh larval weight, the wood's nematode density, the fungal flora in the pupal chamber and the water content of the wood (Togashi, 1989a; Fukushige, 1990; Maehara and Futai, 1996; 1997; Aikawa and Togashi, 1997; Aikawa et al., 1997).

After M. alternatus adults emerge from dead trees, the nematodes turn around in the tracheae and exit from the spiracles (Aikawa and Togashi, 2000). Beta-myrcene, linoleic acid, and 1-monoolein tend to promote the nematodes to depart from the body of M. carolinensis beetles (Stamps and Linit, 1998a). Nematodes harboured in the tracheal system contain a greater content of neutral storage lipid than do those that have exited (Stamps and Linit, 1998b). The volatiles from excised normal P. densiflora twigs repress nematode departure from M. alternatus (Aikawa and Togashi, 1998).

B. xylophilus enters healthy and dying pine trees via feeding and oviposition wounds made by M. alternatus adults (Mamiya and Enda, 1972; Morimoto and Iwasaki, 1972; Arakawa and Togashi, 2002).

There are two types of nematode transmission curves, unimodal and L-shaped, which are represented by the temporal change in the number of nematodes transmitted per unit time by individual M. alternatus adults to excised, healthy P. densiflora twigs through feeding wounds (Kishi, 1978; Togashi, 1985; Shibata and Okuda, 1989). The number of nematodes transmitted by individual beetles increases as the initial nematode load increases (Togashi, 1985; Shibata and Okuda, 1989) but the beetle's life-span is negatively correlated with the initial nematode load (Togashi and Sekizuka, 1982). This suggests that a M. alternatus adult population is divided into three functionally different subpopulations. The first subpopulation with a great nematode load produces resources for oviposition (dead and dying trees), a second, with little nematode load only reproduces, and a third with a considerable nematode load produces oviposition resources and reproduces (Togashi, 1985).

A positive correlation is observed between M. alternatus density and the incidence of pine wilt disease in P. densiflora and P. thunbergii stands (Shibata, 1981; Togashi, 1988). Diseased pine trees show a clumped distribution in P. thunbergii stands, which is explained by a difference in the chemotaxis of beetles before and after maturity, different life-spans and the nematode-transmission ability of beetles with different initial nematode loads (Togashi, 1991a). Shibata (1985) used Togashi's (1980b) model to estimate that the peak of nematode invasion of pine trees in a stand occurs about 2 weeks after the number of adult beetles reaches a maximum.

The ant, Monomorium nipponense, was found to feed on 51% of M. alternatus eggs on a P. thunbergii tree in Kochi Prefecture, Japan (Ochi and Katagiri, 1979). Mortality due to parasitic wasps such as Atanycolus initiator and Spathius spp. and predatory insects such as Trogossita japonica was small (Togashi, 1990c). However, parasitism by the beetle, Dastarcus longulus, reached at least 58% of larvae in pupal chambers in a P. densiflora stand (Okamoto, 1999). Woodpeckers sometimes prey on more than 50% of larvae in pupal chambers in wood (Yui et al., 1993). Natural enemies are reported by Arihara (1984), Inoue (1985), Taketsune (1983), and Togashi (1989c, 1990c) and summarized by Nobuchi (1980), Katagiri and Shimazu (1980), and Kishi (1995) in Japan. In China, Dastarcus longulus, Sclerodermus guani, and a fungus are recorded (Li et al., 1986).

Look for oviposition scars on the bark of trunks and branches of dying and felled trees and logs. Look under the bark and search for the eggs, galleries and frass. If there are no oviposition scars, you should still remove the bark where frass is evident or where the bark is easily depressed by thumb. Search for larvae in the galleries. If you find no larvae, look for whirled, fibrous shreds of wood and remove them to expose the entrance hole of the tunnel into the wood. Inspect the tunnel and in most cases you will find the larva, pupa, or adult.

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.

Early warning systems

Mathematical models of pine wilt disease have been employed to evaluate effective optimal control strategies (Lee, 2014; Lee and Lashari, 2014).

Physical/mechanical control

M. alternatus in dead trees can be destroyed by burning or chipping (Kobayashi, 1988; Kishi, 1995). However, burning in pine forests in Japan can induce the occurrence of a fungal disease caused by Rhizina undulata (Sato et al., 1970).

When logs infested with M. alternatus were buried in soil over 15 cm deep, no adults emerged from the soil (Matsubara and Yonebayashi, 1980).

Silvicultural control through preventative clear-cutting and the manual removal of logs significantly suppressed spread of pine wilt disease compared with districts using conventional controls (physical or chemical treatment of wilt pine trees) (Kwon et al., 2011).

Biological control

Application of the entomophagous fungus, Beauveria bassinana, with nonwoven fabric strips induces an 80% mean mortality of M. alternatus larvae in the field (Shimazu et al., 1995). Sone et al. (2007) applied non-woven fabric strips inoculated with B. bassiana conidia to infested logs, and then covered the logs with a woven polyethylene sheet without openings, which increased the mortality of adults. However, branches and the edges of logs sometimes break the plastic sheet used for wrapping for fumigation, resulting in incomplete eradication. B. brongniartii is less effective than B. bassiana in laboratory tests (Shimazu, 1994).

Application of Steinernema carpocapsae in mid-April caused ca. 70 % mortality of larvae within the logs (Yamanaka, 1994), whereas the application of S. kushidai to pine logs is ineffective (Mamyia, 1989).

The parasitoid Dastarcus helophoroides, which can control medium-aged to mature larvae and pupae, was confirmed as the most important natural enemy of M. alternatus in Chinese pine forests (Lei et al., 2003; Wang et al., 2004; Zhang and Yang, 2006; Li et al., 2007).

Another parasitoid group, Sclerodermus spp. (Hymenoptera: Bethylidae) (Sclerodermus guani and S. sichuanensis), showed promise for controlling young larvae (2nd instar) of M. alternatus (Yang et al., 2014). Combinations of biological applications are more effective; for example, in field experiments the mortality of M. alternatus larvae treated with both S guani and B . bassiana was 61.11 %, compared with 40.18% for S. guani alone and 0.0% for B. bassiana alone (Liu et al., 2007).

Chemical control

Thiacloprid is widely used against M. alternatus in forests (Zhang et al., 2010). The traditional pesticides against M. alternatus, such as fenitrothion and carbaryl, have some negative consequences, including mortality of natural enemies, environmental pollution and rainfall intolerance (Ze et al., 2010). 

Insecticide application against M. alternatus adults shows a high efficacy (Kobayashi, 1988; Kishi, 1995). Insecticide can be sprayed on the crown of trees by hand, sprinkler or helicopter twice during the M. alternatus adult emergence period. The efficacy of insecticide spraying fluctuates depending on season of application and insecticide formulation (Kishi, 1995).

Injection of nematicides, such as mesulfenhos, morantel tartalic acid or levamysol hydrochloride, into healthy tree trunks during winter prevents the development of pine wilt disease, resulting in a reduced reproduction rate of M. alternatus (Kobayashi, 1988). The inhibitory effect lasts 1-2 years. Chemical application by trunk injection is a new option for wilt disease management programs in Europe; trunk-injection trials with emamectin benzoate were efficient in preventing wilt disease (Sousa et al., 2013).

Pheromones and traps

When Pinus densiflora and P. thunbergii were treated with paraquat dichloride or ethephon, they received ten times as many oviposition scars as untreated, nematode-infected trees (Yamasaki et al., 1980). After healthy pines were injected with and attractant at the base of trunk, they attracted a large number of M. alternatus females to oviposit within a week, with an average fecundity of 147.09 (Zhang et al., 1990; Song et al., 1995; Guo et al., 2002). M. alternatus can then be controlled with harvesting or chemical treating (Zhou et al., 2006).

A trap using alpha-Pinene and ethanol as attractants has been developed (Ikeda et al., 1980). Pajares et al. (2010) identified the male-produced aggregation pheromone of M. galloprovincialis as 2-undecyloxy-1-ethanol, which was also the sex pheromone component produced by M. alternatus males (Teale et al., 2011). The combination of the sex pheromone of M. alternatus and host volatiles together caught 4-5 times more M. alternatus adults than the pheromone or host volatiles alone. Removal trapping can play an important role in monitoring and controlling M. alternatus (Fan et al.,  2013).

Host resistance (incl. vaccination)

Resistant clones of Pinus densiflora and P. thunbergii have been bred selectively and are being planted in Japan, with the aim of depriving M. alternatus of oviposition substrates.

06/09/14 text updated by:

Fan JianTing, consultant, China