Armillaria root disease is a chronic problem in California vineyards. Commonly called “oak root fungus,” the disease is caused by Armillaria mellea. This fungus is native to forest trees in California. Its range includes the Central Valley, the San Gabriel Valley, the Coastal Mountains, and elevations up to 6,000 ft. of the Sierra Nevada (Baumgartner & Rizzo, 1998).

Though several Armillaria species are native to California, only Armillaria mellea kills grapevines. Armillaria root disease has been reported on grapevines in the southeastern U.S., Brazil, Central and Eastern Europe, and Australia (Hood et al., 1991).

Armillaria infects vine roots and can eventually kill the vine. It may spread to neighboring vines forming distinctive clusters of dead vines. Attempts to replant within these clusters are usually ineffective. Currently, there are no adequate controls for Armillaria root disease.

Disease symptoms

Armillaria causes above-ground symptoms typical of most root diseases: dwarfed shoots, yellow or red leaves, and premature defoliation. Symptoms are most obvious in late summer when vines may completely collapse and die. Symptomatic vines can be positively diagnosed by examining their root collars for below-ground disease characteristics. Unique to Armillaria are: mycelial fans (white sheets of fungal tissue found beneath bark [see photo]) and rhizomorphs (black, shoestring-like structures found on bark and growing through soil). Armillaria may form mushrooms at or near the base of infected vines in winter, but this may not occur on an annual basis. Therefore, absence of mushrooms does not mean absence of infection.

Course of the disease

How long it takes symptoms to develop and for the vine to die after infection is not predictable. This depends on a number of factors, such as rootstock tolerance, amount of inoculum present, extent of infection, and soil conditions. In vineyard and greenhouse studies, we are currently examining how reliable disease symptoms are for predicting vine death. Our results to date show that both symptom development and time until death after infection can take from one to several years.

How infections spread

Armillaria may be present on a site before a vineyard is established. The disease affects more than 500 species of woody plants, including most native trees, such as oak, madrone, laurel, Douglas fir, and Ponderosa pine (Raabe, 1962). After land is cleared of an oak woodland, any infected roots that remain underground become inoculum sources.

Armillaria is a wood-decay fungus. It lives in soil but needs woody tissue on which to survive. It can live in decaying roots for up to 50 years, depending on their mass.

Rhizomorphs, the agents of infection, grow through the soil from an infected root, but they die if they are separated from the roots they feed on.

Armillaria can attack any woody part of a grapevine’s root system. Vines become infected when roots grow into contact with old Armillaria-infected root pieces, or when rhizomorphs grow from these inoculum sources and contact vine roots. In either case, mode of infection is the same: once the fungus contacts a root, it bores through the bark with the aid of lytic enzymes. Below the bark, Armillaria kills the cambium and a mycelial fan forms. The mycelial fan expands beneath the root bark, and the fungus decays the wood.

Armillaria does not live freely in the soil. It is present only on infected root pieces. Vines planted in infected sites may not show signs of root disease for several years, because it takes time for roots to grow into contact with inoculum in the soil or vice versa.

Once a vine is infected, Armillaria can move to neighboring vines in two ways: by direct vine root-to-root contact or via rhizomorphs. Hyphae (strands of fungal tissue) grow from infected roots to healthy roots that are touching them. Rhizomorphs grow from an infected root, through the soil, to the roots of a nearby vine.

Vine-to-vine spread of Armillaria is usually quite slow. The rate of spread depends on many factors, including soil moisture and temperature, rootstock growth rate and tolerance, amount of inoculum, and vine-spacing. Three things definitely hasten Armillaria infection and spread: excessive soil moisture, large quantities of inoculum, and close vine-spacing.

Chemical infection controls

Pre-plant soil fumigation is more effective for control of Armillaria root disease than post-infection spot fumigation. If soil moisture and texture are optimal, methyl-bromide will kill inoculum to a depth of approximately one meter. For spot fumigation, however, methyl-bromide is often only effective for a few years, which is about how long it takes for roots of replants to meet inoculum. Spot-fumigation only works if the fumigant penetrates deep enough to kill Armillaria on the roots of the dead vine and the inoculum that originally infected it.

Unfortunately, based on our observations of infected vineyards that were fumigated before planting, we know that methyl-bromide doesn’t always provide permanent control. Without thorough land-clearing, infected roots below a depth of one meter are not affected by methyl-bromide.

The use of Enzone (sodium tetrathiocarbonate or STTC) for control of Armillaria root disease in grapevines was found to be ineffective in limited experimental trials (Doug Gubler, Dept. of Plant Pathology, University of California, Davis, personal communication), although some control was achieved in almonds (Adaskaveg et al., 1999). We are currently testing its efficacy in pears.

Enzone is either applied as a soil drench or injected into the soil near the root collar of infected trees on a yearly basis as a preventative measure. Enzone (and other chemical eradicants) must kill all inoculum to provide permanent control. If inoculum remains, root collar applications of Enzone may be required throughout the vine’s life.

Cultural controls

Cultural controls are more promising for long-term control of Armillaria than chemical controls, especially those that decrease soil moisture at the base of the vine. If Armillaria is restricted to the ends of vine roots, a healthy plant can make new roots to compensate for those destroyed by infection. However, once infection surrounds the root collar, the plant is girdled and will likely die.

Moving drip-line emitters to areas between vines as soon as possible after planting may keep Armillaria away from the root collar. We have seen severe cases of root disease in vineyards where emitters were left directly at the base of vines over two years after planting.

In the absence of excessive moisture, many plants can restrict Armillaria infections to tolerable levels. Living native trees bordering an orchard or vineyard, even though they may be infected, contribute little in the way of inoculum. Once they are cut, however, root wood is quickly converted to inoculum.

One of the worst cases of Armillaria we studied was in a vineyard with a freshly-cut laurel stump two meters from its edge. Vines directly adjacent to this stump began showing symptoms only five years after planting. Now a cluster of dead vines extends 20 meters into the vineyard radiating from the edge nearest the stump. After the tree was cut, its root system became one huge piece of inoculum.

Mycorrhizal fungi do not protect grapevine roots from Armillaria root disease. These fungi infect root hairs, while Armillaria infects woody roots. Mycorrhizae do contribute to the overall health of a grapevine though, and healthy vines are less likely to die from root disease than stressed vines.
Root-collar excavation is a common practice used to control Armillaria root disease on infected ornamental and landscape trees. It often extends the tree’s life and causes Armillaria to die back. Biological reasons behind this method’s success are unclear and results are primarily anecdotal,however, it may be due to several effects. Root-collar excavation helps keep bark dry and can offset the influence of excessive moisture. It may restrict infections to peripheral roots, prevent initial root-collar infection by rhizomorphs, and allow infected tissues to recover

Success of root-collar excavation depends on the extent of infection when the treatment is applied. However, it is unlikely to harm an infected vine and is costly only in terms of time spent digging.

Avoiding infection

The best way to avoid root disease is to plant on land with no Armillaria on it. When clearing an orchard or vineyard, look for foliar symptoms (most obvious in late summer) and clusters of dead plants. Look for mycelial fans (present year-round) on symptomatic plants by removing approximately five inches of soil from around the root collar and peeling back the bark with a knife.

Unfortunately, Armillaria is harder to detect in oak woodlands because above-ground symptoms are rare. Mycelial fans and mushrooms do form on infected oaks, but all native Armillaria species make these fans and mushrooms, and they look identical.

Whether you positively identify Armillaria on a site or not, we recommend thorough land-clearing. Absence of symptoms and mycelial fans does not ensure absence of root disease. Infections can exist below the root collar. Ripping the soil in several directions after clearing will bring most large roots to the surface and intensive root-picking will likely remove most inoculum. This should be done even if you plan to fumigate.

We are currently screening 20 different grapevine rootstocks, selected by Andrew Walker (Department of Viticulture & Enology, University of California, Davis), for resistance to Armillaria root disease. Based on the biology and frequency of Armillaria in native habitats commonly cleared for vineyard establishment in California, a management program — including careful land-clearing, use of resistant rootstocks, and cultural controls such as those described here — will likely provide longer-lasting control of root disease than a single chemical eradicant. n

Acknowledgments

Research is funded by the USDA Viticulture Consortium and the American Vineyard Foundation. We thank Rex Geitner, Greg Bjornstad, and Don Gehring for access to vineyard and oak woodland study sites. We also thank Rob Gross for helpful comments on root collar excavation.

References

Adaskaveg, J. E., H. Forster, L. Wade, D. F. Thompson, and J. H. Connell. 1999. “Efficacy of sodium tetrathiocarbonate and propiconazole in managing Armillaria root rot of almond on peach rootstock.” Plant Disease 83: 240-246. Baumgartner, K., and D. M. Rizzo. 1998. “Armillaria root disease in California.” Proceedings of the 46th Annual Western International Forest Disease Work Conference, Reno, Nevada, Sept. 28-Oct. 2, 1998.

Hood, I. A., D. B. Redfern, and G. A. Kile. 1991. “Armillaria in planted hosts.” In: Armillaria Root Disease. Washington, D.C., United States Department of Agriculture Forest Service Agriculture Handbook No. 691. 122-149. Raabe, R. D. 1962. “Host list of the root rot fungus, Armillaria mellea.” Hilgardia 33: 25-88.