Donald,P.A., W.T. Stamps, and M.J. Linit. Pine wilt disease. The Plant Health Instructor. DOI:10.1094/PHI-I-2003-0130-01
DISEASE: Pine wilt disease
PATHOGEN: Bursaphelenchus xylophilus
HOSTS: Scots, Austrian, jack, mugo, and red pines and, less commonly, white pines.
AuthorsP.A. Donald, USDA ARS, Jackson, TNW.T. Stamps and M.J. Linit, University of Missouri
Pine wilt disease. (Courtesy P. Donald, copyright-free)
Pine wilt is a dramatic disease because it usually kills affected trees within a few weeks to a few months (Figure 1). The pine wood nematode (Bursaphelenchus xylophilus) that causes death of the trees is microscopic. Most plant-parasitic nematodes are associated with plant roots, but the pine wood nematode is found in aboveground parts of the tree. Nematodes kill the tree by feeding on the cells surrounding the resin ducts. This causes resin to leak into the tracheids, resulting in "tracheid cavitation" or air pockets in the water transport system. Just as a person cannot drink through a straw with holes in it, the tree cannot move water upward and consequently wilts and dies. Pine sawyer beetles (Monochamus spp.) vector the nematodes. The nematodes hitch a ride with the beetles and thus move from tree to tree as the beetles feed on the young shoots of pine trees.
Scots pine is the most susceptible tree species, although other conifers can be affected, such as Austrian, jack, mugo, and red pines and, less commonly, white pines. Tree death usually progresses from the top of the tree downward, distinguishing this disease from needle diseases. Needle discoloration is usually the first symptom. Needles change from their normal color to a grayish green color and finally a tan to brown color. Needles do not fall from the branch, which is another diagnostic feature. Sometimes, a branch will die, and no disease progression will be seen until the next growing season.
The pine wood nematode was found widely distributed in the United States after its rediscovery in a dying tree in 1979. In the United States, the highest incidence of the disease is currently in the Midwest. Worldwide, the problem is epidemic in Japan and other parts of Asia. In all areas, the disease is most serious on stressed coniferous trees not native to North America. Age of the tree also influences susceptibility. There is an increased risk of developing pine wilt when trees are greater than 10 years of age.
Diagnosis requires observation and identification of the nematode, which can be obtained from cross-sections of symptomatic limbs greater than 2.5 cm (1 in.) in diameter soaked in water. The greatest success in finding the nematode involves soaking a trunk section in water for 24 to 48 hours. One can also sample wood by drilling into branches or the trunk with a large diameter (1-2.5 cm/ 0.5-1 in.) auger drill bit and soaking the resulting wood chips in water. Nematodes may not be well distributed throughout the tree, so it may be necessary to test several samples from different areas of the tree to find the nematodes. Microscopic examination of the liquid is needed to identify the nematode.
Several different bacterial-and fungal-feeding nematodes can be found in the dead or dying wood. Removal of bark before the samples are soaked can reduce the number of other nematodes. There can be several species of Bursaphelenchus present, but not all species are causal agents of pine wilt.
Pine wilt results from interactions among the pine wood nematode (Bursaphelenchus xylophilus) (Figures 2 and 3), the pine sawyer beetle (Monochamus spp.) (Figure 4), a host coniferous tree, and sometimes blue-stain fungi (Ceratocystis spp., Ophiostoma piceae) (Figures 5 and 6).
The pinewood nematode is a microscopic unsegmented worm about 1 mm in length. It is one of at least 49 described species of Bursaphelenchus, most of which have a symbiotic relationship with insects. Bursaphelenchus xylophilus is believed to be native to the United States. It was documented causing damage to trees in 1934 and was rediscovered in 1979. The nematode feeds on fungi within the wood and on living plant cells surrounding the resin canals of pines.
Spread of the nematode from tree to tree occurs via the pine sawyer beetle (Monochamus spp.). The nematodes are carried in the tracheae of the beetle's respiratory system (Figure 7). When the beetles feed on branches of healthy trees, the nematodes emerge and enter the trees through feeding wounds created by the beetles. The adult sawyers are attracted to recently dead or dying trees for oviposition (egg laying). Trees with bark are necessary for oviposition and larval development. The beetle larvae feed several weeks in the cambial wood and then bore into the sapwood.
Once introduced into a tree seedling, the nematodes migrate mainly via the cortical resin canals in branches. Cortical tissue is not present in stem tissues of trees over four years of age, and therefore it is not likely that the nematodes spread within mature trees via cortical tissue. It has been suggested that spread within mature trees occurs through xylem resin canals. The nematodes migrate downward to the tree bole without interruption by the periderm (cork or bark). The nematodes can destroy surrounding tissue and invade cortical tissue until they invade the xylem resin canals and the trunk. When not feeding on the plant cells, the nematodes feed on fungi present within the wood. Bark beetles carry blue-stain fungi to trees, and these fungi, along with other wood-inhabiting fungi, colonize the tree after it is weakened or killed. Research indicates that there is an increase in nematode reproduction when a blue-stain fungus is the food source for the nematode.
The plant-feeding phase of the nematode, B. xylophilus, is usually characterized by rapid reproduction of the nematode and tree death. Laboratory studies show that reproduction can progress from egg to adult in four to five days in the laboratory, feeding on fungi at 25°C (77°F); however, generation time is temperature-dependent. Measurements on pine resin canal tissue are much harder and thus direct comparisons cannot be made here. The nematode goes through four juvenile stages punctuated by molts before becoming an adult. This pathway for the nematode life cycle can continue as long as conditions are favorable for growth and reproduction.
Tree death or scarce food supply results in the nematode switching to a dispersal mode. There is much closer physiological relationship in this mode between the nematode and the insect. The nematode will only molt into fourth-stage dispersal juveniles in the presence of pine sawyer beetles, and the pine sawyer beetle only vectors fourth stage larvae. The dispersal juveniles aggregate around the pupal chambers of the beetles, and migrate toward the insect tracheae located in the spiracles. The fourth stage dispersal juveniles can survive for a year. Laboratory research has shown that removal of the insect pupa from its chamber will trigger increased nematode reproduction. The adult beetles chew their way through the sapwood and exit the tree. Carrying the nematodes, adult beetles fly to healthy trees to feed or to dead or dying trees to lay eggs.
Several months of hot, dry weather are necessary for pine wilt development and spread. Nematode dispersion and multiplication are key factors in disease symptoms and tree death. The pine wood nematode can be a primary or secondary invader of plant tissue (Figure 8); therefore, its presence in dead or dying wood is not proof that the nematode killed the tree.
Adult beetles feed on bark of young branches (Figure 9) and the nematodes present in the insect spiracles (Figure 7) enter the tree through feeding wounds caused by the beetle. Inside a susceptible tree, the nematodes develop into adults and migrate throughout the tree, feeding on parenchyma cells of the ray canals, and reproduce. When conditions favor the nematode (susceptible host, optimal temperature, virulent nematode isolate), internal host responses can be seen within one to three days after infection. Cell death, increased host respiration, decreased water conductivity, increased ethylene production, and increased phytotoxic compounds are found. Trees infected in this manner usually wilt and die rapidly. The nematode is the primary pathogen in this case, and the result is pine wilt. It has been theorized that in susceptible trees the rapid spread of the nematode throughout the tree triggers hypersensitive reactions from the tree in cells behind the nematode. The combination of the nematode movement, feeding, and exudation stimulate the tree to essentially kill itself.
The nematodes can also be a secondary invader of dead or dying trees when they enter the wood when the sawyer beetle is ovipositing (Figure 10). In these cases, the cause of the tree death may not be the pine wood nematode or pine wilt. There is evidence that the nematode exists naturally independent of the disease. These populations of the nematode serve as reservoirs of the nematode for later dispersal by sawyer beetles.
In the midwestern United States, the disease has the greatest impact on homeowners and planted natural areas, wherever susceptible, non-native, poorly adapted pines are planted. Large plantings of Scots pine as windbreaks and landscape planting occurred especially in the Midwest, where this tree species was considered well adapted to the environmental conditions. Stands of single tree species (monocultures) provide an excellent breeding site for the insects and associated nematodes. Because the trees become more susceptible after they reach 10 years of age, the affected and dying trees are well-established trees and their removal has a big impact on the landscape.
Scots pine is the tree of choice for Christmas tree plantations in the Midwest. Most Christmas trees are harvested before they reach 10 years of age unless they are kept for display in large commercial buildings. The biggest threats to existing Scots pines are abandoned Christmas tree plantations, homeowners who do not remove the dead trees, and public areas where dead trees are left standing.
Homeowners should be discouraged from planting susceptible tree species, including Scots pine, Japanese red, or black pine as ornamentals. Within these susceptible tree species, there is no genetic resistance to pine wilt disease although when trees die, not all die at the same time. At this time it is not known whether the longevity of certain trees in a grouping, such as a windbreak, is due to a form of resistance, avoidance, or other factors. It is not uncommon, however, to see an entire windbreak die from pine wilt disease over the course of ten years. This would suggest that resistance was not present, but that for whatever reasons the beetles feed differentially on the trees in the windbreak.
Justin Evertson from the Nebraska Statewide Arboretum has suggested the following as better Midwestern-adapted evergreen tree species [the "(N)" indicates trees native to the Midwest or Great Plains]: balsam fir, concolor fir, nikko fir, Korean fir, Chinese juniper, Rocky Mountain juniper, eastern red cedar (N), Norway spruce, white spruce, Serbian spruce, Colorado spruce, Chinese white pine, jack pine, lacebark pine, Swiss stone pine, pinyon pine, lodgepole pine, limber pine (N), Bosnian pine, Korean pine, mugo pine, Japanese white pine, ponderosa pine (N), Balkan pine, Virginia pine, Douglas fir, Japanese yew, anglojap yew, eastern arborvitae, western arborvitae, and eastern hemlock. There are thus many tree species homeowners can plant that will not succumb to pine wilt.
Pine wilt management at the current time in the United States is best achieved by removal of symptomatic trees. Adult beetles are attracted to recently dead, dying, or freshly cut wood (Figure 11). The beetles fly from dying trees to healthy trees in the spring until the fall and therefore spread of the disease from tree to tree does not occur during the winter months. Depending on the temperature from spring through fall, the beetle can have several generations during a growing season, so trees can be infected anytime until the onset of winter. Dead trees should be burned or buried as soon as possible. It is important that the stumps also be removed or buried, as the stumps are attractive to the sawyer beetles.
In areas of the world where susceptible trees are common and the disease is not present (Europe and Scandinavia), avoidance is the primary means of control. There are strict quarantines on import of wood into these countries. Wood can be heat-treated or debarked before export, in some cases (Figure 12).
In the United States, nematicide and insecticide treatment of trees is impractical, very expensive, and ineffective. In Japan, where the disease is much more devastating, insecticide and nematicide treatments, biological control, and induced resistance through use of less virulent strains of Bursaphelenchus have been investigated.
The disease has a different impact on U.S. exporters of wood products than on homeowners. Bursaphelenchus xylophilus is a quarantine organism in the European Union. Because of the number of susceptible pine hosts and suitable insect vectors in Europe, and the devastating impact the disease has had on native forests in Japan, China, Korea, and Taiwan, unseasoned wood from areas where the pine wood nematode was known to occur was banned in the European Union and China. In Japan, survival of pine trees in a stand can be less than 50% due to pine wilt. An exact measure of the economic impact of the ban on lumber exports from the U.S. and Canada cannot be directly made because of other variables, such as the changes in the Japanese economy and other market factors.
Canadian and U.S. exporters are working with researchers to develop wood treatments that kill the nematodes present in wood chips or other unseasoned lumber (Figure 12). Currently, heat-treating unseasoned lumber to a core temperature of 56°C (133°F) for 30 minutes is sufficient to satisfy the European Union that wood products are free of living nematodes or their beetle vectors. Researchers are studying the risk of pest introduction based on visual inspection of lumber.
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