Vector Relationships in the Pine Wilt System

Marc J. Linit

The pinewood nematode, Bursaphelenchus xylophilus, is a mycophagous and phytophagous species of nematode (a microscopic worm) and the causal agent of pine wilt. This disease is common in parts of North America and eastern Asia causing a rapid wilt of susceptible pine species. The nematode is carried from an infested tree to a new host tree by longhorned beetles in the genus Monochamus (Coleoptera: Cerambycidae). M. carolinensis is an important vector in North America, while M. alternatus is important in Asia. The nematode was first described from logs of long-leaf pine in the United States in 1931; however, it was not recognized as a primary pathogen. In the 1970s the nematode was identified as the causal agent of a widespread epidemic causing pine mortality in Japan. The nematode is believed to be indigenous to North America but introduced and established in Japan and other parts of eastern Asia. Some pine species not indigenous to North America appear to be highly susceptible, while those that have coevolved with the nematode in its native range appear to be resistant or tolerant to nematode infestation. For example, the disease is commonly expressed on Scots pine planted as an ornamental or in Christmas tree plantations in North America. In Asia, Japanese black and Japanese red pines are affected in plantations and forest environments.

Figure 1. A Scots pine killed by pine wilt. The yellow-brown foliage is characteristic of pine wilt-killed trees.

The foliage of a diseased tree fades progressively from light gray-green to yellow-green to yellow-brown in three to six weeks (Fig. 1). Fading may occur uniformly throughout the crown of the tree or may progress from one branch or section of the crown to another. Coincident with foliage changes, there is a cessation of resin flow and a decrease in moisture content of the xylem.

Pathogen-vector relationships
The disease is expressed through the complex interaction of the nematode, its insect vector, and the host tree. Indeed, within the host tree the development of the nematode is mediated by that of the beetle. This synchrony insures that the dispersal stage of the nematode is present when the newly formed adult beetle is ready to exit the tree in which it developed. All but one life stage of the nematode and the beetle occur solely within a host tree.

Figure 2. Life cycle of the pinewood nematode illustrating the reproductive and dispersal pathways.

The nematode develops through four juvenile stages then molts to a sexually reproducing adult stage (Fig. 2). In a favorable environment, with ample wood moisture content and fungal growth, the generation time is about four days. As the environment within a dying tree deteriorates, the nematode population switches from this rapid reproductive pathway to a dispersal pathway. The second juvenile stage molts to a third-stage dispersal juvenile. This molt appears to be environmentally mediated. The molt to the fourth-stage dispersal juvenile only occurs in the presence of a pupal or early adult Monochamus beetle.

Figure 3. Adult male and female Monochamus alternatus. The sexual dimorphism in antennal length and the general pattern of coloration is typical of many species in the genus Monochamus.

Figure 4. Graphic representation of a Monochamus gallery system, showing the oval hole made by larval entry into the xylem, larval gallery, widened pupal chamber, and emergence of a newly formed adult beetle.

Adult Monochamus beetles (Fig. 3) are attracted to volatile chemicals emitted from a stressed or dying pine, where they land on the trunk and mate. Females chew an oviposition pit in the bark and deposit eggs in the cambium layer below. After the larvae hatch from the eggs, they feed in the cambium, while the later stages (instars) enter the xylem through oval shaped holes and construct a c-shaped gallery in the wood (Fig. 4). The beetle pupates in the end of the gallery, molts to the adult stage, then chews its way out of the tree. Newly emerged adults fly to the crown of a healthy tree to feed on the bark of young twigs.

Figure 5. Cross section of a Monochamus carolinensis trachea arising from the first abdominal spiracle. The wall of the trachea is identified by the red arrow. Phoretic fourth-stage dispersal juveniles are indicated by the blue arrow.

Figure 6. Fourth-stage dispersal juveniles of the pinewood nematode can be introduced into new trees through feeding wounds made by beetles on healthy trees (left) or through oviposition pits made by adult females on stressed and dying trees (right).

Within the pupal chamber, newly formed fourth-stage dispersal juvenile nematodes move into the respiratory system (tracheae) of newly formed adult Monochamus beetles (Fig. 5). The dispersal stage nematodes reside in the thoracic spiracles and trachea arising from them. Individual beetles carry up to 50,000 dispersal-stage nematodes, rarely as many as 100,000. Beetles commonly carry between 0 and 10,000 nematodes as they emerge from the tree in which they developed. Nematodes can exit as the beetle feeds on pine branches of healthy trees and enter the tree through the feeding wound (Fig. 6). If nematodes enter a susceptible host species through a feeding wound the presence of the nematode population can result in pine wilt. Alternately, nematodes can exit during beetle oviposition on stressed or dying trees and enter the tree through the oviposition wound. In the latter case, the nematode is a secondary saprophyte, feeding on fungi introduced by other insects that colonize dying pines.

Risk of movement through international trade
It is generally believed that the pinewood nematode was introduced into Japan from North America about 100 years ago. More recently it has been introduced into other parts of eastern Asia. Thus, the ability of the nematode to be transported and established in new geographical areas through the international movement of infested wood has been established. Indeed, regulatory sanctions have been in place for several years to minimize the chance for nematode establishment in the European Union. Movement of the nematode in infested wood likely occurs as third-stage dispersal juveniles. If Monochamus larvae are also present in the wood, newly formed adult beetles could carry fourth-stage dispersal juveniles to host trees in the new location as they emerge from the transported wood.

Transport of pathogens by forest insects is a common feature of disease cycles found in forest ecosystems. The phoretic relationship between Monochamus beetles and the pinewood nematode is just one example. Others include Dutch elm disease and Leptograhium root disease, both vectored by bark beetles. See Hansen’s paper on root disease pathogens for more detail on the role of insects as vectors of root diseases.

References:

Bergdahl, D.R. 1988. Impact of the pinewood nematode in North America: Present and future. J. Nematol. 20:260-265.

Linit, M.J. 1988. Nematode/vector relationships in the pine wilt disease system. J. Nematol. 20:227-235.

Mamiya, Y. 1988. History of pine wilt disease in Japan. J. Nematol. 20:219-226.

Necibi, S., and M.J. Linit. 1998. Effect of Monochamus carolinensis on Bursaphelenchus xylophilus dispersal stage formation. J. of Nematol. 30:246-254.