A relatively small, but taxonomically diverse array of organisms cause root diseases of forest trees. All kill trees and cause dramatic loss under certain circumstances, but they have distinctive pathogenic lifestyles and, consequently, represent very different threats as potentially invasive organisms in foreign environments.

ROOT DECAY FUNGI
Most familiar, but perhaps least threatening as exotic invasive species, are the Basidiomycete wood decay fungi that decompose the cellulose of large roots, killing trees outright or, more commonly, making them vulnerable to windthrow or bark beetle attack. Armillaria and Heterobasidion are the best known of this group. These genera attack many tree species and are found on all continents with forests. They possess a complicated population genetic structure, with regional, reproductively isolated groups that differ in pathogenicity. H. annosum, for example, often thought of as a single but variable species, is in fact a complex of geographically and reproductively isolated populations with distinct host preferences. For example, the P type of H. annosum in Europe, is an aggressive pathogen on several North American conifers planted abroad, including cedars and firs, but the P type recognized in western North America is largely confined to pines and juniper.

Figure 1. Armillaria ostoyae on pine.

Root decay fungi are characterized by slow increase and great persistence in forests. They require a mass of colonized, decayed wood as a food base for spread, either through spores or more commonly by vegetative growth across root contacts. Insect vectors do not play an important role, and the fungi are in or on the woody roots, not soilborne. Root decay fungi colonize trees slowly, often taking 20 or more years to kill large trees. Evidence for accidental long-distance transport is limited. Normally, a sizeable mass of colonized wood must be moved and then reburied in contact with susceptible roots to establish a new infection beyond the range of airborne spores. One example makes the point: A. mellea was introduced to Cape Town, South Africa, presumably in trees or woody shrubs transplanted there 200 years ago by European colonizers. The fungus has since spread only by root contact and is still not found beyond a few hundred meters of the presumed point of introduction.

PHYTOPHTHORA ROOT DISEASES
Phytophthora is a genus of Oomycetes, more closely related to some algae than to true fungi. These water molds produce swimming zoospores to seek out and infect the fine roots of their hosts in water-saturated soils. In some host-Phytophthora combinations, the pathogen grows up the roots through the phloem tissue and girdles the tree, resulting in rapid death. In other cases, infection is confined to the fine roots, resulting in chronic disease. Phytophthora often forms resting spores (chlamydospores or oospores) with thick cell walls that are released into the soil as roots decompose. These allow the pathogen to survive dry periods or long-distance transport in soil.

P. cinnamomi has been introduced to many ecosystems around the world, with destructive consequences. P. lateralis was introduced into the mixed coniferous forests of the western United States, where it causes a lethal root disease of Port Orford cedar (Chamaecyparis Lawsoniana) and the quite unrelated Pacific yew (Taxus brevifolia). It illustrates the threats Phytophthora species pose to trees around the world, through the transport of nursery stock and soil.

Port Orford cedar (POC) root disease was first reported in 1923 in nurseries growing ornamental cultivars of POC. It largely eliminated POC as a commercial ornamental tree in western North America. In 1952 it was first reported on POC in its native range and has now spread through most of the forest areas where the tree grows. Transport to the forest was apparently in infested soil around nonhost plants raised in an infested nursery.

Phytophthora lateralis is a cool temperature species, active through the mild wet winters of the area and inactive, or even dying in the warm, dry, summer months. In the native forests where POC grows, uphill transport is primarily along roads on vehicles and road maintenance and logging equipment, while downslope movement occurs in streams and through overland flow during periods of heavy winter rains.

Phytophthora species are serious threats as invasive organisms because of the ease of transport in soil and young plants and the difficulty of control once established. They may attack unexpected hosts in new environments.

LEPTOGRAPHIUM ROOT DISEASES
Leptographium species are conidial fungi with morphological features and sporulation behavior that facilitate dispersal by insects. Conidia are formed in insect galleries beneath the bark of dead or dying roots. The spores are commonly carried by bark beetles. Sexual stages, where known, are in the genus Ophiostoma, and are ‘relatives’ of O. ulmi, and O. novo-ulmi, the Dutch elm disease fungi.

Figure 4. Hylastes nigrinus, a root-feeding bark beetle and vector of blackstain root disease.	Figure 5. Steremnius carinatus, a root-feeding weevil and vector of blackstain root disease.

Some species, including L. wageneri on conifers, cause "wilt" diseases by colonizing the vascular system and disrupting water transport. Blackstain root disease (BSRD) is caused by three varieties of Leptographium wageneri: var. wageneri on pinyon pines; var. ponderosa on ponderosa and lodgepole pines and mountain hemlock; and var. pseudotsugae on Douglas-fir. On Douglas fir especially, disease severity is closely related to forest silvicultural activities, and the observed increase in damage in recent decades is apparently the result of intensified forestry operations. BSRD is only found in western North America, but both exotic and native conifers grown in Europe are susceptible, and insects that might function as vectors are present.

Figure 6. Symptoms of blackstain root disease on Douglas fir.	Figure 7. Hyphae of Leptographium wageneri in xylem tracheids.

L. wageneri can grow for a few centimeters through the soil and through root grafts. Insects, however, provide its primary means of dispersal. In Douglas fir, a root-feeding bark beetle and two root and crown weevils are known vectors of the pathogen. Vectoring by similar insects is strongly suspected in the pines as well.

These insects breed in the dying roots of trees severely stressed by a variety of agents, including BSRD. They do not have an obligate relationship with the fungus, but they are very efficient at finding blackstain-infected roots on trees, even before crown symptoms are visible to the human eye. They overwinter as pupae in galleries excavated at the interface between xylem and phloem and emerge as adults in the spring. Adults fly, or crawl in the case of Steremnius, apparently following olfactory cues released from stressed trees. They land, burrow down to the roots, and feed on root phloem. If feeding wounds etch the xylem, and if the insect is carrying the fungus, then a new infection may result.

Blackstain may be a threat to forestry wherever conifers are grown. European species are susceptible, and the variety of insects known to act as vectors suggests that others could serve the role as well.

REFERENCES

Erwin, D.C., and O. K. Ribeiro. 1996. Phytophthora Diseases Worldwide. APS Press.

Hansen, E. M., and K. J. Lewis, eds. 1997. Compendium of Conifer Diseases. APS Press.

Hansen, E. M., D. J. Goheen, E. S. Jules, and B. Ullian. 2000. Managing Port-Orford-cedar and the introduced pathogen Phytophthora lateralis. Plant Disease 84:4-14.

Harrington, T. C., and F. W. Cobb, Jr., eds. 1988. Leptographium Root Diseases on Conifers. APS Press.

Shaw, C.G., III, and G.A.Kile, eds. 1991. Armillaria Root Disease. USDA Forest Service. Agric. Handbook No. 691.

Woodward, S., J. Stenlid, R. Karjalainen, and A. Huttermann, eds. 1998. Heterobasidion annosum: Biology, Ecology, Impact, and Control. CAB Intern.