Armillaria root disease
Armillaria altimontanaArmillaria gallica
Location: throughout California
Hosts (in California): a wide variety of both hardwood and conifer trees
Management: Armillaria species are so fundamental to the ecology of many forests—functioning not only as tree-killers but also as ubiquitous forest decomposers—that management of the diseases they cause is difficult. In California, the Armillaria species that have been observed do not, for the most part, produce widespread mortality. Primarily, the fungus causes problems in situations where native forest cover has been replaced with agricultural crops, ornamental landscaping, or the built environment near and around remnant forest patches. However, how these Armillaria species may emerge to cause problems in the future under a changing climate is unknown. Where Armillaria does cause mortality in the forest, management approaches should center on (1) improving the vigor or remaining trees, (2) removing stumps that could be harboring the fungus, and (3) increasing the proportion of Armillaria-resistant tree species in the stand. All three of these prescriptions are difficult and require considerable time and trial, particularly considering the long generation and activity cycles of Armillaria species, which have been shown to be some of the oldest and most pervasive organisms in many northern hemisphere forests.
Highlights: Armillaria species have a variety of mechanisms for spreading and reproducing in forest stands. Armillaria species can be seen in the forest in several forms. When conditions are good for growth and nutrient acquisition (such as in a newly killed tree), Armillaria can be observed as a flat, white mycelium growing between the bark and wood of the host. This mycelial form is usually fan-shaped, evenly flat, and able to be peeled away from the wood like dried paint. When foraging through the soil or attempting to colonize a living host, the fungus can be observed as rhizomorphs, which are brown-to-black, shoestring-like outgrowths of the fungus that form a network of varying sizes, lengths, and growth patterns depending on the Armillaria species. These structures’ hard rinds protect them from competition and predation by other soil microorganisms. In California, Armillaria gallica produces especially copious growths of rhizomorphs, suggesting a great capability for vegetative, as opposed to sexually reproductive, growth and spread. Finally, when the host is thoroughly colonized, Armillaria species produce mushrooms that grow on the outside of the host and disperse airborne spores that enable the fungus to colonize more distant trees. These mushrooms, also called honey mushrooms, usually grow in groups, have medium-to-large caps, and feature rings around their stalks.
Of the species that have been found in California, Armillaria mellea is typically the most aggressive. It is often seen on oaks and causes especially noticeable damage in areas where humans have heavily modified the environment (e.g., on trees growing in heavily irrigated lawns or on grapevines where native oak forest was cleared to plant vineyards). The other species are usually found in native forests. Armillaria gallica is a prominent decomposer of dead trees, producer of butt rot in a variety of living hardwoods, and both a decomposer and apparent killer of some conifers. Armillaria nabsnona is a decomposer of dead trees, particularly alder and grand fir, along the north coast. Armillaria altimontana is found in the true fir forests of the southern Cascades; its ecological roles are not completely understood, but some early research suggests it may play a beneficial symbiotic role for some trees, protecting them from infection by more virulent pathogens. It is interesting to note that the most aggressive conifer-killing Armillaria species in the western U.S., Armillaria ostoyae (also known as Armillaria solidipes), has not been found in California to date although it is widespread in neighboring states.
Mushrooms, most likely of Armillaria mellea, at the base of a coast live oak snag.
Armillaria sp. infection at the base of a recently killed Douglas-fir, showing “peelable” mycelium.
Initial penetration of Douglas-fir bark by Armillaria sp., showing white mycelium and fungal degradation of bark tissues as a precursor to cambium and wood infection.
Baumgartner, K. and Rizzo, D.M. 2001. Distribution of Armillaria species in California. Mycologia 93(5), pp. 821-830.
Baumgartner, K. and Rizzo, D.M. 2001. Ecology of Armillaria spp. in mixed-hardwood forests of California. Plant Disease 85, pp. 947-951.
Baumgartner, K. and Rizzo, D.M. 2002. Spread of Armillaria root disease in a California vineyard. American Journal of Enology and Viticulture 53(3), pp. 197-203.
Brazee, N.J., Ortiz-Santana, B., Banik, M.T., and Lindner, D.L. 2012. Armillaria altimontana, a new species from the western interior of North America. Mycologia 104 (5), pp. 1200-1205.
Chen, L., Bóka, B., Kedves, O., Nagy, V.D., Szűcs, A., Champramary, S., Roszik, R., Patocskai, Z., Münsterkötter, M., Huynh, T., Indic, B., Vágvölgyi, C., Sipos, G., and Kredics, L. 2019. Towards the biological control of devastating forest pathogens from the genus Armillaria. Forests 10(11), 1013.
Ferguson, B.A., Dreisbach, T.A., Parks, C.G., Filip, G.M., and Schmitt, C.L. 2003. Coarse-scale population structure of pathogenic Armillaria species in a mixed-conifer forest in the Blue Mountains of northeast Oregon. Canadian Journal of Forest Research 33, pp. 612-623.
Heinzelmann, R., Dutech, C., Tsykun, T., Labbé, F., Soularue, J.-P., and Prospero, S. 2019. Latest advances and future perspectives in Armillaria research. Canadian Journal of Plant Pathology 41(1), pp. 1-23.
Kubiak, K., Żółciak, A., Damszel, M., Lech, P., and Sierota, Z. 2017. Armillaria pathogenesis under climate changes. Forests 8(4), 100.
Raabe, R.D. 1962. Host list of the root rot fungus, Armillaria mellea. Hilgardia 33(2), pp. 25-88. Available online at http://hilgardia.ucanr.edu/fileaccess.cfm?article=152569&p=SZZFQV.
Smith, M.L., Bruhn, J.N., and Anderson, J.B. 1992. The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356, pp. 428-431.
Volk, T.J., Burdsall, Jr., H.H., and Banik, M.T. 1999. Armillaria nabsnona, a new species from western North America. Mycologia 88(3), pp. 484-491.
Warwell, M.V., McDonald, G.I., Hanna, J.W., Kim, M.-S., Lalande, B.M., Stewart, J.E., Hudak, A.T., and Klopfenstein, N.B. 2019. Armillaria altimontana is associated with healthy western white pine (Pinus monticola): potential in situ biological control of the Armillaria root disease pathogen, Armillaria solidipes. Forests 10(4), 294.
Black Stain Root Disease
Leptographium wageneri var. wageneri
Leptographium wageneri var. ponderosae
Leptographium wageneri var. pseudotsugae
Location: throughout California
Hosts (in California): var. wageneri: piñon pine; var. ponderosae: ponderosa pine; var. pseudotsugae: Douglas-fir
Management: The fungi that cause black stain root disease spread long-distances on beetle vectors seeking compromised trees for feeding and breeding. In many cases, these are root- and stump-feeding beetles, so preventative management often depends on (1) avoiding management activities that will stress root systems, such as road construction or other activities that will compact soil over root systems and (2) avoiding tree harvest, particularly precommercial thinning, during months of heavy beetle flight activity (typically spring) in areas where root disease is known to be a problem. The fungi can also move from tree to tree through underground root-to-root connections and also for very short distances through soils. Management activities designed to reduce the risk of root disease development can sometimes be in conflict with each other—for example, thinning stands to reduce competition-induced tree stress, host susceptibility, and root connectivity can also create stumps and slash that are attractive to root-feeding beetles—so the optimal management regime often depends on trial and error and the development of long-term site-specific knowledge of the stand. Direct control of the native beetles that spread the fungi is infeasible, as is direct control of the fungus. Since the causal fungi kill trees by blocking water-conducting vessels and not by decaying woody tissues, presence of the fungus does not directly indicate structural hazard, although subsequent development of other decay fungi eventually will compromise tree integrity.
Highlights: These diseases are called “black stain” diseases because the hyphae of the fungi inhabit the water-conducting vessels (tracheids) in the outer layers of the functional sapwood, clogging up the tree’s sap stream and shutting off water supply to the crown. They can be recognized as a black stain confined to those outer layers, resembling a black arc in the sapwood. This is in contrast to so-called “blue stain” fungi, which are usually less virulent and can inhabit all layers of the sapwood, including the ray parenchyma that are oriented horizontally in the woody tissue, so that blue stain fungi are recognized by a wedge- or pie-shaped stain in the bole. The three fungi mentioned above are potentially not the only ones to cause a “black stain” disease in conifers. Also present in California are aggressive pathogens of other pines such as Leptographium wingfieldii on Monterey pine, shore pine, and bishop pine and an as-yet-unnamed species that has been observed causing a black stain in the sapwood of dying Monterey pines. Many researchers now refer to these fungi as Grosmannia sp., denoting the sexually reproducing form of the fungus, rather than by the asexual form-name Leptographium; however, the sexual form of Leptographium wageneri has only been observed once, so the asexual name is still widely used.
Heterobasidion root disease
Typical black stain root disease center in Douglas-fir, with trees in various stages of decline.
Symptoms of black stain root disease in Douglas-fir: thin crown, abundant crop of smaller-than-normal cones, and foliage that eventually turns red.
Hessburg, P.F., Goheen, D.J., and Koester, H., 2001. Association of black stain root disease with roads, skid trails, and precommercial thinning in Southwest Oregon. Western Journal of Applied Forestry 16(3), pp. 127–135.
Hessburg, P.F. and Hansen, E.M., 1986. Mechanisms of intertree transmission of Ceratocystis wageneri in young Douglas-fir. Canadian Journal of Forest Research 16(6), pp. 1250–1254.
Kearns, H.S.J. and Jacobi, W.R., 2005. Impacts of black stain root disease in recently formed mortality centers in the piñon–juniper woodlands of southwestern Colorado. Canadian Journal of Forest Research 35(2), pp. 461–471.
Marincowitz, S., Duong, T.A., Taerum, S.J., de Beer, Z.W., and Wingfield, M.J., 2020. Fungal associates of an invasive pine-infesting bark beetle, Dendroctonus valens, including seven new Ophiostomatalean fungi. Persoonia 45, pp. 177-195.
Schweigkofler, W., Otrosina, W.J., Smith, S.L., Cluck, D.R., Maeda, K., Peay, K.G., and Garbelotto, M., 2005. Detection and quantification of Leptographium wageneri, the cause of black-stain root disease, from bark beetles (Coleoptera: Scolytidae) in Northern California using regular and real-time PCR. Canadian Journal of Forest Research 35(8), pp. 1798–1808.
Witcosky, J.J., Schowalter T.D., and Hansen, E.M., 1986. Hylastes nigrinus (Coleoptera: Scolytidae), Pissodes fasciatus, and Steremnius carinatus (Coleoptera: Curculionidae) as vectors of black-stain root disease of Douglas-fir. Environmental Entomology 15(5), pp. 1090–1095.
Witcosky, J.J., Schowalter, T.D., and Hansen, E.M., 1986. The influence of time of precommercial thinning on the colonization of Douglas-fir by three species of root-colonizing insects. Canadian Journal of Forest Research 16(4), pp. 745–749.
Brown Cubical Root Rot
Location: Throughout California
Hosts in California: most conifers
Management: In areas where it is prevalent, some conifers (e.g., Douglas-fir in the Coast Ranges) are heavily colonized and decayed by this pathogen by the time they reach a century old; consequently, commercial management can involve limiting rotation ages. Where susceptible conifer species are dominant around developed areas, larger trees should be surveyed periodically for signs of decay, since the butt rot caused by this pathogen can make trees fail with little warning. Coring of trees to determine sound rind percentage can help in determining hazard potential.
Highlights: Phaeolus schweinitzii is found throughout much of the northern hemisphere and is capable of infecting a large number of conifer species. Its spores percolate down through the soil column and infect root tips, and the pathogen grows upward through progressively larger roots until it colonizes large portions of the tree butt. P. schweinitzii is ecologically important for several reasons. First, although it can be pervasive throughout large areas, it colonizes and decays trees slowly so that trees fall out of the overstory one by one over many years. Second, it is one of the few “brown rot” fungi that return decay residues rich in lignin to the soil, contributing to soil texture, structure, and stability. Third, infection with P. schweinitzii is often associated with attack by other native insects and pathogens: notably, in the case of Douglas-fir, it is associated with Douglas-fir beetle and other root diseases such as Armillaria spp.
Phaeolus schweinitzii produces fruiting bodies that grow from infected roots and, when tree colonization is extensive, directly from the tree base. Fresh fruiting bodies, produced in the fall, can be any shade of yellow, orange, or brown with a fuzzy top, leading to the common name “velvet top fungus.” The pathogen is also called the “cow pie” fungus because the dried annual fruiting bodies resemble cow pies, and it is called the “dyer’s polypore” because compounds extracted from the fungus provide very good dyes in a range of colors including yellow, olive green, and brown.
Fruiting body of Phaeolus schweinitzii that appears to be growing from the ground but is actually connected to roots
Close up of fruiting body in
Barrett, D.K. 1985. Basidiospores of Phaeolus schweinitzii: a persistent source of soil infestation. European Journal of Forest Pathology 15(7), pp. 417-425.
Barrett, D.K. and Greig, B.J.W. 1985. The occurrence of Phaeolus schweinitzii in the soils of Sitka spruce plantations with broadleaved on non-woodland histories. European Journal of Forest Pathology 15(7), pp. 412-417.
Dubreuil, S.H. 1981. Occurrence, symptoms, and interactions of Phaeolus schweinitzii and associated fungi causing decay and mortality of conifers. Ph.D. Dissertations, University of Idaho. 157 pp.
Heterobasidion Root Disease
Heterobasision irregulare and H. occidentale (formerly known as H. annosum or Fomes annosus)
Hosts (in California): Nearly all conifers and some hardwoods. H. irregulare infects pines, incense cedar, juniper and, rarely, hardwoods including oaks and madrone. H. occidentale infects true firs, Douglas-fir, giant sequoia, hemlock, spruce and western redcedar.
Management: Heterobasidion root diseases (formerly called Annosus root disease) constitute a long-term problem in forest stands. Infection occurs on freshly cut stumps or wounds and can spread for years or even decades through root contacts to neighboring susceptible trees. Prevention is the best form of control which means the treatment of freshly cut stumps with a borax based registered pesticide formulation to preclude infection by fungal spores. This is especially important on Sierra east side pines. Avoiding wounds in true firs is also critical. In known disease centers planting of non-host species for the existing type of Heterobasidion is an option.
Highlights: The disease is common throughout California infecting nearly all conifer species. Infection occurs on freshly cut stumps or wounds and spreads through root contact from susceptible tree to susceptible tree. Disease centers can spread for years, sometimes decades, killing trees in the center of the site with declining trees and individuals with thinning or discolored crowns further out. The fungi cause white, stringy rots in the roots and boles of the infected trees. Host trees are very susceptible to attacks by bark and engraver beetles, particularly during periods of drought. Often the first indications of infection are when trees fall over in storms due to the lack of structural root support or are attacked by bark beetles. Fungal fruiting structures can occur as small buttons on or just under the bark (“popcorn conks”) or as shelf-like conks within the rotted stumps. These conks tend to be brown to cinnamon colored on the top and creamy to white colored on the pored surface of the undersides (most common on true firs).
Heterobasidion root disease
Fruiting bodies (conks) within a rotted stump.
Thinning, discolored crown of pine
Bradley, T. and Tueller, P., 2001. Effects of fire on bark beetle presence on Jeffrey pine in the Lake Tahoe Basin. Forest Ecology and Management, 142(1-3), pp.205-214.
Egan, J.M., Sloughter, J.M., Cardoso, T., Trainor, P., Wu, K., Safford, H. and Fournier, D., 2016. Multi-temporal ecological analysis of Jeffrey pine beetle outbreak dynamics within the Lake Tahoe Basin. Population ecology, 58(3), pp.441-462.
Hood, S.M., Cluck, D.R., Jones, B.E. and Pinnell, S., 2018. Radial and stand‐level thinning treatments: 15‐year growth response of legacy ponderosa and Jeffrey pine trees. Restoration Ecology, 26(5), pp.813-819.
Paine, T.D., Millar, J.G., Hanlon, C.C. and Hwang, J.S., 1999. Identification of semiochemicals associated with Jeffrey pine beetle, Dendroctonus jeffreyi. Journal of chemical ecology, 25(3), pp.433-453.
Seybold, S.J., Bentz, B.J., Fettig, C.J., Lundquist, J.E., Progar, R.A. and Gillette, N.E., 2018. Management of western North American bark beetles with semiochemicals. Annual review of entomology, 63, pp.407-432.
Smirnova, E., Khormali, O. and Egan, J.M., 2019. Functional analysis of spatial aggregation regions of Jeffrey pine beetle-attack within the Lake Tahoe Basin. Statistics & Probability Letters, 144, pp.57-62.
Status: Both native and non-native
Location: throughout California
Hosts killed by this pathogen in California: a wide variety of trees, shrubs, and herbaceous plants
The plant disorders caused by soilborne Phytophthora species are often called “diseases of the site” because once these pathogens are established in the soil, the only way to remove them is to thoroughly fumigate the soil with chemicals that also destroy beneficial soil biota. Some success has been found with applying phosphonate fungicides as a soil drench to provide resistance to native tree and shrub species susceptible to Phytophthora cinnamomi in Australia. Since many soilborne Phytophthora species are major pests of agricultural crops, specific fungicide applications and intensive cultural practices have been developed to manage these pests in those crops. Otherwise, management of these soilborne pathogens depends largely on preventing their spread to new, uninfested areas by delineating infested areas; implementing cleanliness measures to limit the human-assisted spread of the pathogens on footwear, tools, and vehicles; and designing clean plant production systems to limit the inadvertent spread of Phytophthora species on plants grown for landscaping and ecological restoration.
The exception to the paragraph above is Phytophthora lateralis, which causes Port Orford-cedar root disease in northwestern California and southwestern Oregon. This pathogen has received intensive study leading to the development of management recommendations with a higher likelihood of success than in the case of more generalist pathogens in this genus. Depending on the management goals, geographic area of activity, and managing agency, these recommendations include implementing specific cleanliness measures; clearing Port Orford-cedar from infested sites for a period of time; removing small Port Orford-cedar regeneration from roadsides and other areas where the pathogen can easily reach the small trees to initiate new infections; and deploying known disease-resistant stock for reforestation within the natural range of Port Orford-cedar.
Highlights: Phytophthora species resemble fungi in their growth habit and production of infective spores. However, they belong a group of organisms called oomycetes, which belong in a diverse kingdom of life called Stramenopila. Other stramenopile organisms include diatoms, brown algae such as kelp, and the organisms that produce downy mildews of crops such as soybeans, hops, grapes, and squash. One way in which Phytophthora species differ from fungi is in their production of spores that can swim in water by means of flagella (all fungal spores are non-motile and get from place to place passively). Phytophthora species are commonly called “water molds” because their survival and reproduction is dependent on the presence of free water. Although many of them can produce resistant, thick-walled spores that can survive in roots or soil for long periods of time under unfavorable environmental conditions, they require at least a thin film of water to grow and reproduce. When these conditions appear—for example, during flooded conditions in the soil—Phytophthora species can produce hundreds of thousands of infective spores in a very short period of time. They are well-adapted to boom-and-bust environmental conditions.
There are around 200 known Phytophthora species, not all of which have described and named, and it is likely that many more are undiscovered. Many of these are plant pathogens, and many infect roots in roughly the same ways and produce similar symptoms. The four listed above are some of the most prominent in California.
P. lateralis was introduced from its native habitat (Taiwan) into North America in the 1920s, infecting planted Port Orford-cedars; from the point of introduction in the Pacific Northwest, the pathogen slowly spread into the native range of the tree in southwest Oregon and northwest California. By the end of the first decade of the 2000s it had become established in the southernmost and easternmost major drainages that support populations of Port Orford-cedar (southernmost: the Trinity and Mad River drainages in Humboldt County; easternmost: the upper Sacramento River drainage in Siskiyou County).
P. cinnamomi was first noted in California in the early 2000s causing dramatic mortality of a rare manzanita species, Arctostaphylos myrtifolia (Ione manzanita), in the Sierra Nevada foothills. Subsequently, it was noted in southern California on native oak species and then along the north coast associated with mortality in a diverse set of tree and shrub species including bishop pine, tanoak, madrone, bay laurel, rhododendron, chinquapin, bigleaf maple, and Douglas-fir.
P. cambivora has been associated with chinquapin mortality in roughly the same area where P. lateralis is active (northwest California/southwest Oregon). However, it has a wider host range, having also been associated with 30 other tree genera from 19 families. It has been detected throughout California and has probably been present and spreading for well over a century. P. cactorum is similar; it is very well-known as a pathogen of various agricultural crops including many fruit and nut trees. Genetic information indicates that, unlike the other Phytophthora species in this list, P. cactorum may be native to California soils.
Other soilborne Phytophthora species of particular concern in California include P. tentaculata and P. quercina. P. tentaculata has been detected on native plant species, including sticky monkeyflower (Mimulus aurantiacus), toyon (Heteromeles arbutifolia), coffeeberry (Frangula californica), and sage (Salvia spp.), that were grown and subsequently outplanted as part of native habitat restoration projects. P. quercina, which has been associated with oak decline in continental Europe, was detected in California on recently planted valley oak (Quercus lobata). The more researchers and land managers look for these soilborne pathogens in California landscapes, the more they find, making clean plant-growing practices and the development of rapid detection methods high priorities for forestry, agricultural, and restoration sectors.
Canker (area of dead stem tissue) on a madrone tree associated with Phytophthora cinnamomi and Phytophthora cactorum at a site in Santa Cruz County. Dead tissue is darker brown and on left, while still-living tissue is lighter in color and on right
Bleeding canker of red alder caused by Phytophthora siskiyouensis in Humboldt County
Phytophthora tentaculata Kr?ber & Marwitz was described in 1993 in Germany on greenhouse-grown nursery ornamentals. It has since been found in Italy, Spain, China and the U.S. (California) causing a root and stem rot of many different plant species including nursery-grown native species used for habitat restoration.
Location: California, Europe
In California, the pathogen appears to have been spread within and between nurseries by the use of infested pots and potentially by infected plants.
Susceptible hosts include members of the Asteraceae, Ranunculaceae, Lamiaceae, Rhamnaceae, Phrymaceae, Rosaceae, and Verbenaceae plant families.
P. tentaculata is classified in group I based on its primarily paragynous antheridia and papillate sporangia (Stamps et al., 1990) and is a member of phylogenetic Clade 1 (Cooke et al., 2000) along with P. cactorum, P. nicotianae, P. clandestina and P. pseudotsugae, among others.
P. tentaculata causes a moderate to severe root and crown rot, depending on the host species. It has not been shown to be a foliar pathogen. The pathogen is known to cause high mortality in heavily infected plants.
Port-Orford-Cedar Root Disease
Port-Orford-cedar root disease, caused by the pathogen Phytophthora lateralis, is a fatal disease of Port-Orford-cedar (POC), Cupressus (Chamaecyparis) lawsoniana.
Location: Washington, Oregon, California
Because of the ecological significance, limited distribution, and economic value of POC, the disease has had considerable impact. Despite the widespread, but localized, occurrence of the
root disease, the existence of POC is not endangered.
Hosts: Port-Orford-cedar (POC), Pacific yew
Biology: Phytophthora lateralis is a soil borne pathogen that infects young, non-suberized roots.
Infected trees usually undergo a rapid decline as the pathogen girdles the trunk at the soil line. The foliage throughout the crown turns yellow, then bronze, then light brown (Fig. 4). Attack of weakened trees by cedar bark beetles (Phloeosinus spp.) commonly occurs.
Port-Orford-Cedar root disease