Collectively (and in many cases individually), Armillaria species have a huge host range . Many conifers and hardwoods, and even some herbaceous plants, are susceptible.
Age of the host may influence the disease. With conifers, killing of young, vigorous trees is fairly common, especially in plantations. Older trees can tolerate infections much better and they survive much longer with infection. Older trees often get butt rot if they are infected rather than extensive killing of sapwood, cambium, and phloem.
Several species in the genus Armillaria, commonly called oak fungus or honey mushroom, cause similar diseases. These fungi, in the Agaricales, form mushrooms. The characters of the mushrooms for field identification are:
We used to call everything in this group Armillaria mellea. Now we know that there are over 30 distinct entities there. They are difficult to distinguish morphologically. In most cases, however, we now recognize them as distinct species because: (a) they are intersterile; (b) there are some differences among them in morphology and molecular-genetic characters; (c) there are differences in distribution, host range, and virulence, and; (d) it is a very important genus, both ecologically and economically. Following are some of the most studied species [2, 6]:
Armillaria borealis frequently causes butt rot in conifers. It rarely kills trees and has been moderately virulent in inoculations. Rhizomorph branching dichotomous. Distributed in the northern parts of Europe, Scandinavia, Russia.
Armillaria calvescens is most commonly found on hardwoods in northern hardwood forests, where it often causes butt rot. It may kill stressed trees. Rhizomorph branching monopodial. Probably the most common species in much of northeastern North America.
Armillaria cepistipes may function largely as a saprobe, but also can infect living hardwoods. It causes butt rot in hardwoods and may attack sapwood and cambium in stressed trees. It has also been found causing butt rot in conifers in Finland and Scotland. Rhizomorphs abundant; branching monopodial. Europe, North America, Japan.
Armillaria gallica commonly causes butt rot in hardwoods, especially oaks. When the trees are stressed, the fungus can move into more vital tissues, causing significant damage and death. The best-known case is in the northeastern U.S., where repeated defoliation by the introduced gypsy moth leads to killing by A. gallica of trees that might otherwise recover from the defoliation stress. Rhizomorphs large (up to 5 mm diameter) and abundant; branching monopodial. Circumboreal: Europe, eastern North America, Japan.
Armillaria gemina is almost always found on hardwoods. One report based on limited observations indicates it is similar to A. ostoyae in pathogenicity , but it is normally not found causing disease in the forest. Eastern North America.
Armillaria luteobubalina has a wide host range among the tree species in its habitat, dry sclerophyll eucalypt forests. Rhizomorphs absent or sparse. Australia.
Armillaria novae-zelandiae is found in wet forests. It causes particular damage to the introduced tree species Pinus radiata. New Zealand, eastern Australia, New Guinea, South America (?).
Armillaria ostoyae is probably the most common and aggressive pathogen of conifers in the genus. It can kill trees of all ages and may cause butt rot in older conifers. However, it is known to occasionally attack and kill hardwoods associated with conifers, and it has even caused significant mortality in cherry orchards in one area . Rhizomorphs usually thin, delicate and sparse; branching dichotomous. Circumboreal: Europe, North America, Japan.
On Sept. 2, 1899, a traveling mycologist, Elam Bartholomew, collected some nice mushrooms from the base of a spruce stump just outside of Gunnison, Colorado. It was new to him, and he sent the collection to Charles Horton Peck, a renowned mycologist (actually the State Botanist) at the New York State Museum. Peck described it as a new species, Armillaria solidipes. More recently, this species was rediscovered, and determined to be conspecific with A. ostoyae, which was described in 1970 .
According to the rules of priority, then, the proper name of the fungus should be Peck’s name, Armillaria solidipes. However, a group of forest pathologists in western North America took alarm at this prospect. They marshalled all the mycological arguments they could , but really the community was just tired of changing names and, by golly, they weren’t going to take it anymore. So in the end they did the proper thing to prevent that, and a propoosal to conserve the newer name against A. solidipes was accepted.
I have to admit I have a soft spot for the name A. solidipes, largely because the type specimen was collected in Gunnison, where I worked for many years. And the name may rise again! Independent molecular analyses have shown that the population from Europe is clearly distinct from the population from North America [7, 9]. In fact, the American population is more related to A. gemina than to A. ostoyae in Europe. As evidence mounts, the species may be split, and there would be no choice this time but to give the American species its rightful name, Armillaria solidipes Peck!
Armillaria sinapina is often found in mixed hardwood-conifer forests, but usually more often on the hardwood component. It is usually not found causing substantial disease and has been only weakly pathogenic in inoculations. However, it is sometimes found on conifers without a significant hardwood component. In British Columbia, it is often found in disease centers in conifers with A. ostoyae . Although there is some evidence that it killed conifers independently in British Columbia, most evidence suggest that it is only weakly pathogenic and tends to follow pathogens such as A. ostoyae as secondary invaders. Rhizomorphs abundant. North America.
Stress may play a role in some cases. The fungus may behave like a saprobe or cause a nonlethal butt rot until the trees are stressed (e.g., gypsy moth defoliation of oaks). Then, host physiology is altered and fungus can successfully attack and kill vital tissues. This tends to be the case more often in hardwoods. In conifers, killing of vigorous trees is more often observed. However, killing of hardwoods can be seen without apparent stress too.
This disease is so difficult to deal with partly because it uses as a food base not only the trees it kills, but also stumps of trees killed by felling or other means. Thus, any management we do, if it involves felling, stands a chance of backfiring and making the situation worse.
While an infected tree is still alive or long after it has died, the pathogen has three means of dispersal to to other trees:
- Mycelium can grow through direct root contacts and grafts with uninfected trees
- Rhizomorphs can grow through soil to contact uninfected trees
- Mushrooms produce basidiospores, which are wind-dispersed to wreak death and destruction in new places
The first two means of dispersal, via mycelium at root contacts and rhizomorphs, are short-range. This local spread is very important and is generally the dominant source of infection. The fungus can move by these means from an old root system, perhaps from a previous forest, to plants currently growing on the site. This leads to the appearance of disease in a previously uninfected population. This has been so common in California on sites formerly occupied by oak and cleared for orchard production that the pathogen there is commonly called the “oak root fungus.” Because the pathogen may survive for 50 years or more in stumps , it can wait until the new generation provides a large target for infection. The fungus can also move this way from a diseased tree to a neighboring healthy tree, leading to expanding areas of disease and mortality, usually called root disease centers.
Root disease centers, as well as saprobic growth of the fungus, involve indeterminate growth through the forest. Resulting clones can cover many hectares, perhaps even miles, and be thousands of years old. Armillaria is the famous humongous fungus that was in all the news some years ago (more on this below).
Rhizomorphs are macroscopic, 1-5 mm diam., reddish brown to black, bundles of organized hyphae with an organized apically growing tip. Rhizomorphs grow through soil, produce branches, and look very much like roots (rhizo-morph) or shoestrings (thus a common name for the disease, “shoestring root rot”). They use energy from a stump or killed tree to grow and infect a nearby tree. They can grow many meters through the soil.
When I was a fresh assistant professor, I was so excited about Armillaria species that I spent the better part of a day digging up a rhizomorph system, more or less intact. The featured image above shows the result. The ruler in center is 32 cm long; the total length shown might be 20 m.
The third means of dispersal, basidiospores, seems to be the least common. Although mushrooms and basidiospores are common enough, the spores don’t seem to get established very easily. There is indirect evidence that they do occasionally colonize stumps or wounds, especially in moist climates.
Persistence in dead roots and stumps, the saprobic phase, may be dominant for some species that subsist by colonizing dead trees but rarely seem to kill them. Armillaria species may be abundant in the forest without a lot of obvious, damaging disease in some situations. Other species decay dead trees and stumps and build up energy to attack neighboring trees.
External, above-ground symptoms on individual trees are variable and not specific to this disease or even to root diseases in general. It is not uncommon for the disease to be very advanced but showing no obvious symptoms. Symptoms include:
- reduced terminal growth (most detectable in conifers)
- dieback of twigs and branches (most apparent in hardwoods)
- chlorosis of needles
- stunted leaves
- crown thinning
- premature fall coloration (hardwoods)
- basal resinosis (conifers)
- heavy production (‘stress crop’) of cones or fruits
Internally, the disease may develop as butt rot in some situations and as cambial killing in others. The difference may be related to stress and host differences. If the host is resistant, a major wound may be required for infection, and the fungus would be restricted to inner, inactive wood (butt rot). If the host becomes stressed, the fungus is then able to attack cambial regions, even of unwounded trees.
Clear mortality centers, from a few trees to several hectares, may be seen in some cases and not in others.
The decay is a spongy, often wet, white rot. Zone lines can usually be found in the decayed wood. In hardwoods the decay often has a gelatin in it.
This pathogen is very generous in providing oodles of signs to allow diagnosis. They all require some experience to identify to the genus Armillaria with certainty. They are:
- Mycelial fans (like soft, white, peelable paint) can be seen under the bark of tree portions that are colonized while the tree is alive or shortly thereafter.
- Rhizomorphs (see above under Disease Cycle)
- Mushrooms (see above under Pathogen and under Disease Cycle)
Armillaria species cause root disease throughout most temperate regions of the world. See the list of species under Pathogen, above, for details.
Here’s what doesn’t work:
- Stump-top chemical treatment
- Wide spacing
Here’s what often does work:
- Inoculum Reduction – There are two approaches to inoculum reduction, both pioneered in the Pacific Northwest (PNW). One is mechanical stump removal, either during harvest by simply pushing trees over, or after harvest by removing stumps with a big excavator. Small roots stay in the soil, but the fungus won’t last long in them. This is of course expensive, and is done with sites that are otherwise good. The other is fumigation. This is more in the experimental stage. Volatile, toxic chemicals are placed in a hole drilled into an infested stump. The chemical kills the fungus or weakens it to the point other fungi can kill it.
- Resistant Species – We are learning more all the time about host ranges of the major Armillaria species. Planting or favoring the more resistant species will avoid the disease. For PNW, larch, birch and to lesser degree ponderosa pine are resistant. Following a rotation with resistant species, the pathogen should have died out in the old root systems, permitting the reestablishment of susceptible species. This is crop rotation.
- Increasing Host Vigor – This is applicable in cases where the disease is linked to prior stress. Examples might be control of defoliating insects; using good planting practices to avoid deformed roots or using seeds.
Here are management guidelines for PNW conifers:
- In establishing new stands (such as after a clearcut), where discrete disease centers can be identified and marked, stumping or planting resistant species can be tailored for the centers. Elsewhere, a preferred, susceptible species may be planted. If inoculum is scattered, stumping or resistant species can be used throughout.
- During thinning, resistant species can be favored. However, thinning may do more harm than good, and not doing it should be considered.
- In a partial harvest, consideration should be given to focussing on disease centers, removing stumps or planting resistant species afterward.
- Note that most of these approaches require field personnel who are skilled in recognizing symptoms and disease centers. You will find this for all the root and butt rots.
Here’s something that might work: biological control. We found a fungus that is similar to Armillaria and apparently competes with it. We investigated the degree to which they compete and how they are affected by silvicultural treatments in stands threatened by gypsy moth and subsequent Armillaria root rot . Others have investigated biological control as well. This may be the future for management for this disease, as silvicultural approaches are often quite limited.
A Fungus Gets Its 15 Minutes of Fame
Small fields like mycology and forest pathology can be turned upside down when something strikes the media’s fancy on a slow news day. Such was the case in 1992 when M. Smith, J. Bruhn and J. Anderson published an article in Nature  highlighting the ability of Armillaria gallica to form very large clones. All it took was for the media to link that concept with the phrase, ‘humongous fungus’, and the hounds were released! An article in The New York Times, a feature on ABC News, and David Letterman’s Top Ten followed in quick succession. Find more on this amusing story. Uhaul has a great web page on it, as it is one of the featured supergraphics on their rental vans.
A Glow-in-the-Dark Fungus!
Beowulf and Armillaria
. . . it is not that far hence
in milemarks, that the mere [swamp] stands;
over it hangs frost-covered groves,
tree held fast by its roots overshadows the water;
there one may every night a horrible marvel see:
fire on the water; not even the wise of them lives,
of men’s sons, that knows the bottom.
Though the heath-stepper harrassed by hounds,
the hart with strong horns, seeks the forest,
put to flight from far, first he will give up his life,
existence on the shore, before he will leap in
to hide his head; it is not a pleasant place!
translation by Benjamin Slade
. . . Not far is it hencetranslation from The Harvard Classics, Volume 49 by Frances B. Grummere, presented on the web by Erik Max Francis
in measure of miles that the mere expands,
and o’er it the frost-bound forest hanging,
sturdily rooted, shadows the wave.
By night is a wonder weird to see,
fire on the waters. So wise lived none
of the sons of men, to search those depths!
Nay, though the heath-rover, harried by dogs,
the horn-proud hart, this holt should seek,
long distance driven, his dear life first
on the brink he yields ere he brave the plunge
to hide his head: ’tis no happy place!
Maybe the coolest thing about Armillaria species has nothing to do with pathology. Its mycelium glows in the dark! The mushrooms do not glow much, if at all, but if you open a piece of wood with advanced decay caused by Armillaria, and view it in the dark, you stand a good chance of seeing the luminescence. It helps to let your eyes adjust to the dark. The amount of light varies greatly from different pieces of decaying wood. It’s not likely to blind you, but some pieces are quite bright. Other fungi glow, including in some cases the fruitbodies, but Armillaria is certainly the most common and widespread luminescent fungus.
It certainly is a wondrous thing to see in the night, bringing a strange mix of delight and spookiness. So it is easy to imagine strange and magical things behind it. Glowing wood has indeed found its way into folklore and mythology. It has been termed “fairy fire” but is more commonly called “foxfire” in modern times (is that derived from “faux,” or false, fire?). Aristotle called it a “cold fire”. It made a brief appearance to lend an eerie air of dread to a scene in the oldest surviving piece of English literature, Beowulf (see quotes).
It is fun to speculate what selective advantage luminescence may confer. Some have suggested it may attract animals that serve the fungus in some way. Others have suggested some physiological role in metabolizing damaging waste products. Also, keep in mind that not every character has a ‘purpose’. If it is selectively neutral, or a byproduct of some advantageous trait, it may persist in a population of fungi indefinitely.
- 1.Bérubé JA, Dessureault M. 1989. Morphological studies of the Armillaria mellea complex: two new species, A. gemina and A. calvescens. Mycologia 81:216-225. Mycologia 81(2):216–225 <10.2307/3759703>.
- 2.Blodgett JT, Worrall JJ. 1992. Distributions and hosts of Armillaria species in New York. Plant Disease 76(2):166–169 <10.1094/PD-76-0166>.
- 3.Burdsall HH, Volk TJ. 2008. Armillaria solidipes, an older name for the fungus called Armillaria ostoyae. North American Fungi 3(7):261–267 <10.2509/naf2008.003.00717>.
- 4.Burrill EA, Worrall JJ, Wargo PM, Stehman SV. 1999. Effects of defoliation and cutting in eastern oak forests on Armillaria spp. and a competitor, Megacollybia platyphylla. Canadian Journal of Forest Research 29(3):347–355 <https://forestpathology.org/pdfs/burrill1999megacollybia.pdf>.
- 5.Dettman JR, van der Kamp BJ. 2001. The population structure of Armillaria ostoyae and Armillaria sinapina in the central interior of British Columbia. Canadian Journal of Botany 79(5):600–611 <10.1139/b01-033>.
- 6.Gregory SC, Rishbeth J, Shaw III CG. 1991. Pathogenicity and virulence. In: Armillaria Root Disease: Agricultural Handbook vol. 691, eds Shaw III CG, Kile GA, pp. 76–87. Washington, DC: USDA Forest Service.
- 7.Guo T, Wang HC, Xue WQ, Zhao J, Yang ZL. 2016. Phylogenetic analyses of Armillaria reveal at least 15 phylogenetic lineages in China, seven of which are associated with cultivated Gastrodia elata. PloS one 11(5):e0154794 <http://www.ncbi.nlm.nih.gov/pubmed/27138686>.
- 8.Hunt RS, Morrison DJ, Bérubé J. 2011. Armillaria solidipes is not a replacement name for A. ostoyae. Forest Pathology 41(4):253–254 <10.1111/j.1439-0329.2011.00730.x>.
- 9.Klopfenstein NB, Stewart JE, Ota Y, Hanna JW, Richardson BA, Ross-Davis AL, Elías-Román RD, Korhonen K, Keča N, et al. 2017. Insights into the phylogeny of Northern Hemisphere Armillaria : Neighbor-net and Bayesian analyses of translation elongation factor 1-α gene sequences. Mycologia 109(1):75–91 <https://www.fs.usda.gov/treesearch/pubs/54041>.
- 10.Proffer TJ. 1987. Biological species of Armillaria isolated from sour cherry orchards in Michigan. Phytopathology 77(6):941 <10.1094/Phyto-77-941>.
- 11.Raabe RD. 1962. Host list of the root rot fungus, Armillaria mellea. Hilgardia 33:23–88.
- 12.Redfern DB, Filip GM. 1991. Inoculum and infection. In: Armillaria Root Disease: Agricultural Handbook vol. 691, eds Shaw III CG, Kile GA, pp. 48–61. Washington, D.C.: USDA Forest Service.
- 13.Smith ML, Bruhn JN, Anderson JB. 1992. The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356:428–431.