The Humongous Fungus--Ten Years Later

Has it already been ten years? On April 2, 1992, the non-mycological world first became aware of very large fungi, thanks to the efforts of Myron Smith, Johann Bruhn, and Jim Anderson. They published a landmark article in Nature (Smith , M., J. Bruhn and J. Anderson, 1992. The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356:428-431), but no one expected the media blitz and the scientific interest that would follow.

First you'll need to know a bit of background on Armillaria, also known as the Honey Mushroom. Armillaria (Fr.:Fr.) Staude is a genus of mostly pathogenic agaric fungi. Perhaps the most important aspect of the life cycle of Armillaria is the formation of rhizomorphs, conglomerations of differentiated parallel hyphae with a protective melanized black rind on the outside. The rhizomorphs are able to transport food and other materials long distances, thus allowing the fungus to grow through nutrient poor areas located between large food sources such as stumps. The rhizomorphs can also act as "scouts" for the rest of the thallus, searching for new food sources. These proliferative rhizomorphs apparently permit Armillaria colonies to spread and become quite large. Thus enters the Humongous Fungus.

The science that led to this seminal Nature publication (Smith et al. 1992) turns out to be quite interesting and very thorough. The project was actually an offshoot of a grant from the Department of Defense, which funded a project to study the possible biological effects of ELF (Extra Low Frequency) stations in the Upper Peninsula of Michigan. These ELF stations were built to communicate underground with ocean-going submarines in time of war. The humongous fungus site, which Johann Bruhn had been studying for many years, was actually one of the control sites, nowhere near the ELF stations. Historically, the site (near Crystal Falls, Michigan near the Wisconsin border) had been mostly northern red oak/white birch/ sugar maple forest, but the native trees had been harvested with more profitable red pines planted in their place. When the oaks were cut, the stumps were mostly left in the ground to rot. The oaks had been infected with Armillaria root rot, but had survived very well because they were not under any stress. However, when pines were planted, some species of Armillaria were able to kill the young pine seedlings. The particular species that garnered their attention was Armillaria bulbosa, which is now correctly known as Armillaria gallica. I'll tell you more about this taxonomic problem later.

The study of Smith et al. (1992) was performed by collecting vegetative mycelium of Armillaria by "baiting" with small pieces of poplar wood, actually popsicle stick-like tongue depressors. Since Armillaria is a wood decay fungus, the mycelium quickly colonized the tongue depressors. The labeled inoculum stick could then be easily collected. Additional subcultures, including tissues and single spore isolates, were made directly from fruiting bodies that appeared in the fall or from the black rhizomorphs and mycelial fans that are always present in the soil or on the wood, especially under the bark. The laborious process of analysis began, first with checking the mating type loci by mating on media in Petri dishes. Molecular techniques were then employed, first looking at mitochondrial DNA (mDNA) restriction patterns. These were both good markers for the study because mating type loci and mDNA restriction patterns are both highly variable within Armillaria species. Once these were determined, RAPD (Random Amplified Polymorphic DNA) and RFLP (Restriction Fragment Length Polymorphisms) markers were employed to check for additional heterozygous loci in the nuclear genome. With these several types of data, they could begin to draw maps of the area to determine the limits of each individual. One of these clones turned out to be quite large, covering 15 hectares (37 acres). Within this area, all the vegetative isolates had the same mating type , the same mDNA restriction pattern, and had the same eleven RAPD products and five RFLP-based markers, each marking a heterozygous locus. These data indicated that this 15 hectare clone is a single organism. However, some argued that this only meant that they had the same alleles at these genetic loci, bringing up the possibility that the samples were from separate, but closely related organisms (or individuals) that arose from separate matings. In their paper, Smith et al. (1992) presented some complex statistics that show that the probability of this being the case was infinitesimally small (P= 0.0013), given that all the samples share all the heterozygous markers examined. Even so, to lend even more credence to their conclusions, eventually they tested 20 RAPD and 27 nuclear restriction fragments that were found to be invariable in the large clone. By far the most likely hypothesis is that this clone reached it enormous size through vegetative growth. Thus the Armillaria clone was proven to be quite a humongous fungus. By estimating (very conservatively, I might add) the growth rate of the fungus under their natural conditions and by extrapolating the weight of the clone from smaller soil samples (again very conservatively), Smith et al. found the clone to be at least 1500 years old and weigh at least 9,700 kg (more than 21,000 pounds or 100 tons), close to the mass of an adult blue whale. They compared the mass to that of a giant redwood (Sequoiadendron giganteum) estimated to be about 1,000 tons, most of which is dead xylem tissue. The conclusion of their paper states, "This is the first report estimating the minimum size, mass, and age of an unambiguously defined fungal individual. Although the number of observations for plants and animals is much greater, members of the fungal kingdom should now be recognized as among the oldest and largest organisms on earth."

Myron Smith wrote to me recently in an email "I have often been asked something like,'what made you look for a large fungus?' Like most discoveries (and this is a point that needs to be stressed to granting agencies), we did not set out to make this discovery. Initially, (at least when Jim and I came on the scene) we wanted to find out how mitochondrial DNA was inherited in fungi in nature (Smith, Duchesne, Bruhn and Anderson, 1990). The first year we went out and sampled from a 120 x 60 m area. Nearly every sample was identical for mDNA and mating type.  The second year we extended our sampling over a 1 km transect through the area and, again, detected this one wide-spread genotype.  By extending the areas sampled in subsequent years, we were finally able to delimit the large area occupied by this genotype and then go on to show that this genotype likely represents an 'individual'."

Although they knew they were publishing a very good paper, Smith, Bruhn, and Anderson never expected what happened next. On that historic publication day, the furor began. Johann Bruhn, at that time at Michigan Technological University in Houghton, Michigan, now at the University of Missouri- Columbia, received the first of many phone calls from the media. Since it was April 2, he thought that this was a late April Fool's joke, but soon more calls began pouring in. All of the major television networks called; all of the major newspapers called from around the world. CNN called and reported that they had a plane in the air and would Johann please drive over to the site and wave so that they could take photos of the fungus. One Japanese businessman called and wanted to set up a partnership to build a boardwalk around the humongous fungus and charge people to view "the pulsating mass of fungus" that was there. Johann reports shutting himself into his office and having the secretary screen the calls one at a time as they came in. The two authors at the University of Toronto, Myron Smith (now at Carleton University in Ottawa) and Jim Anderson (still at the University of Toronto) experienced a similar media deluge. I first became aware of the media hype as I heard Jim Anderson being interviewed on US National Public Radio. You'll have to talk to the three authors to hear further interesting stories.

The media blitz lasted a month or so, then seemed to dissipate as things got back to normal. However, on May 18, 1992, it all began again. Terry Shaw, then in Colorado with the US Forest Service, and Ken Russell, of the Washington DNR, reported that they had been working on an even larger fungus, Armillaria ostoyae, that covered over 600 hectares (1500 acres, 2.5 square miles) south of Mt. Adams in southwestern Washington. The newspaper headlines read "Humongous Fungus has BIG brother out west." The fungus wars had begun. Who had the larger fungus? Questions arose as to who had better proof that theirs was a single organism. Russell and Shaw had only shown that the mating type loci were the same, but they had beautiful aerial photos showing growth of the large colony in a radial pattern, showing where it had killed the conifer trees. Smith et al. had a much more convincing argument, with several meticulous lines of genetic evidence showing without a doubt that theirs was a single clone.

Ten years later, we are still experiencing the fungus wars. In August of 2000, Catherine Parks of the US Forest Service in Oregon (along with collaborators Brennan Ferguson, Oregon State University; Tina Dreisbach, PNW Research Station, Forest Service; Greg Filip, Oregon State University; and Craig Schmitt, Wallowa-Whitman National Forest, Forest Service) reported that they had found an even larger fungus (again Armillaria ostoyae) in the Blue Mountains/ Malheur National Forest in Eastern Oregon. Their fungus is nearly 900 hectares (2,200 acres or 3.4 square miles or "as large as 1,665 football fields") and is estimated to be more than 2,400 years old. They used methods similar to those of Smith et al., including mating type analysis, but with the addition of DNA fingerprinting, not widely available in 1992. It seems likely that there are larger Armillaria clones out there somewhere. Myron Smith wrote to me, "As far as I (and I think this is true for Johann and Jim as well) was concerned, the 'Fungus wars' were a non issue; another example of sensationalistic journalism. The chance of finding "the largest fungus" is incredibly small.  Our main point was how to unambiguously identify a genetic individual.  That we did find a large individual by chance, however, suggested to us that massive, old fungi are probably not uncommon."

One interesting offshoot of these findings of humongous fungi has been a scientific discussion of "what exactly is an organism?" Most people understand the concept of an organism in an animal, which has very carefully defined limits--and most of it is usually visible as it moves around. However, much of a typical plant and most of a typical fungus is not visible to the naked eye. In particular with fungi, the limits of the individual are not clearly defined. The large question was "are these humongous fungi acting as single organisms?" It was well proven that the genetics of various parts of the humongous fungus organism are identical, but can, for example, one part of the organism communicate with other parts of the organism? Do they share physiology? If different parts are growing through different substrates, are they supplying other parts of the fungus with missing nutrients? Several articles began to appear in the scientific literature including Gould (1992) in which he spent a great deal of time discussing populations of asexually reproducing aphids. One letter to the editor by James Bullock of Oxford University (1992) pointed out some larger clones of plants, including an aspen clone (Populus tremuloides) covering 81 hectares and over 10,000 years old. At that time Bullock did not know about the larger A. ostoyae clones.

Despite the large size of the mycelia of these humongous fungi, the fruiting bodies (mushrooms) are really quite average in size. However, during a good fruiting season, the honey mushrooms may be quite abundant, producing a widespread biomass. However, the largest single fruiting bodies are produced by perennial polypores (shelf fungi), such as Bridgeoporus nobilissimus, Rigidoporus ulmarius, and even Ganoderma applanatum.. Some of these large fruiting bodies may weigh over 160 kg or 300 pounds! Certainly these are much larger than Armillaria fruiting bodies, which are typically 50-100 g each.

I promised to tell you something about why Armillaria gallica is the name we should use for this species rather than A. bulbosa. Armillaria species typically produce a white spore print and have attached to decurrent gills. Most species have an annulus. Delimiting species in fungi is often difficult, but in Armillaria the biological species concept, based on mating compatibility, has gained wide acceptance. Until the late 1970's Armillaria mellea (Vahl:Fr.) Kummer was considered by most researchers to be a pleiomorphic (highly variable) species with a wide host range and distribution. The pathology literature on A. mellea was extremely confusing. The fungus was considered by different researchers to be either a virulent pathogen, an opportunistic pathogen, or an innocuous saprobe. Its host range was one of the broadest known for fungi. It was clear that more than one species must be involved. Because of the difficulty with studying the basidiomata using traditional characters, other methods of study were devised. Hintikka (1973) developed a technique that allowed determination of mating (incompatibility) types in Armillaria based on culture morphology of single-spored (haploid) pairings. He and his colleagues found six biological species in Europe. The work was extended into North America, where Anderson and Ullrich (1979) demonstrated that what had been considered as Armillaria mellea in North America was actually 10 genetically isolated biological species (North American Biological Species or NABS). Anderson, Korhonen, and Ullrich (1983) found that most of the biological species of Europe (including A. gallica, NABS VII or EBS E) were also represented in North America, although the reverse was not true.

There is a bit of controversy about what to call this species. Very briefly, the name A. bulbosa Velenovský (1927) [a.k.a. A. bulbosa (Barla) Velenovský, but Barla's (1887) name A. mellea var. bulbosa was illegitimate] has a very poorly preserved type specimen. Vladimir Antonín (1986, 1990) of the Czech Republic has examined Velenovský's type specimens (preserved in a liquid fixative) and has concluded that the specimen could be any of three species. According to Marxmüller (1992) Velenovský's species is identical with A. cepistipes Velen. (1920), which has priority, being an older name (see also Termorshuizen and Arnolds, 1987). Another name proposed for this species has been Armillaria lutea Gillet, but this species lacks a type specimen, and Gillet's (1874) description could represent any one of three species. Armillaria gallica Marxmüller & Romagnesi (1987), which has an excellent type specimens and abundant cultures, is the only name that can unequivocally be assigned to European Biological Species E and NABS VII. See Volk & Burdsall (1995) for a clear explanation of this taxonomic problem.

The humongous fungus has been great publicity for the science of Mycology; we couldn't buy publicity like this. The humongous fungus even made David Letterman's Top 10 list. (see www.crystalfalls.org).

U-Haul, known for their truck rental services, got into the act in about 1997, when they contacted me for more information about the humongous fungus. Famous for publicizing some of the more bizarre "roadside attractions" on their trucks, U-Haul planned on putting the humongous fungus on some of their trucks to honor the state of Michigan. Through my web page, they contacted me and asked to use one of my pictures. I consented, hoping to help promote mycology to the masses. A month later they sent me a sample drawing for my approval-and the mushrooms were PINK! I diplomatically pointed out that in fact the mushrooms were not pink and that they should put them on the truck in their natural tan/brown/yellow color, since there were thousands of professional and amateur mycologists throughout North America who would know that their fungi were discolored. The U-Haul people replied back that they had taken some "artistic license" with the color, since they thought the natural color was not exciting enough. Sheesh. So now there are several hundred U-Haul trucks around the continent with pink Armillaria fruiting bodies on them. U-Haul now even has a website about the humongous fungus (Anonymous 2002A). It's exciting for me to see one of my pictures (well, sort of one of my pictures...) on one of the 500 or so Humongous Fungus trucks as I drive down the highway-- I've seen the humongous fungus trucks from Maine to California, from Minneapolis to Houston. I like to think it's helping to make the public more aware of fungi and mycology. Myron Smith again wrote: "I like to think that what grabbed the imagination of the public in this case was the idea that there are common, unseen things all around us that are magnificent.  Of course, the mental image of a large, old fungus lumbering over the countryside is also bizarre and wonderful."

The humongous fungus continues to be a great boon for educating non-mycologists on the importance of fungi in their lives. The important publicity generated by the work of Myron Smith, Johann Bruhn, Jim Anderson, and the others that followed continues to speak well for the science of Mycology. Even more humongous fungi will no doubt continue to be found. As mycologists we have a multitude of Armillaria researchers to thank for putting mycology in the news in favorable light for a very long period of time. Mycology is not likely to get such great publicity again in our lifetimes. But you never know...

Acknowledgments: Thanks to Myron Smith, Jim Anderson, Dan Czederpiltz, and Sean Westmoreland for reading the manuscript and making helpful suggestions.

• Anderson, J.B. and R.C. Ullrich. 1979. Biological species of Armillaria in North America. Mycologia 71: 402‑414
• Anderson, J.B., K. Korhonen, and R.C. Ullrich. 1980. Relationships between European and North American biological species of Armillaria mellea. Exper. Mycol. 4: 87‑95.
• Anonymous. 2002A.U-Haul Humongous fungus web page http://www.uhaul.com/supergraphics/fungus/
• Anonymous. 2002B. Crystal Falls Fungus Fest webpages. http://www.crystalfalls.org/FUNGUS%20FEST.htm http://www.crystalfalls.org/humongou.htm
• Antonín, V., 1986. Studies in annulate species of Armillaria - I Study of type-specimens of Armillaria cepaestipes Velenovský. Ceská Mykol. (Praha) 40: 38-40.
• Antonín, V., 1990. Studies in annulate species of Armillaria - III. Species described by Josef Velenovský. Acta Mus. Moraviae Sci. Nat. 75: 129-132.
• Barla, G.1887. Bull. Soc. Mycol. France 3:143
• Dodge, Sherri Richardson.2001. An Even More Humongous Fungus, http://www.fs.fed.us/pnw/news/fungus.htm
• Bollock, James, 1992.Huge organisms. New Scientist 30 May, p. 54
• Gillet, C.-C., 1874. Les Hymmenomycčtes ou description de tous les champignons (Fungi) qui croissent en France.
• Gould, Stephen Jay, 1992.A humongous Fungus Among Us.Natural History, July p. 10-14.
• Herink, J. 1973. Taxonomie Václavky Obecné‑ Armillaria mellea (Vahl. ex Fr.) Kumm. Pp. 21‑48. In: Vysoká Skola Zem_d_lska V Brné. Vyznamenaná Rádem Prace BRNO; J. Hasek, ed. Brno: Lesnicka fakulta VSZ.
• Hintikka, V. 1973. A note on the polarity of Armillariella mellea. Karstenia 13:32‑39.
• Marxmüller, H. 1992.Some notes on the Taxonomy and Nomenclature of five European Armillaria species. Mycotaxon 44 (2): 267-274.
• Marxmüller, H. and H. Romagnesi 1987. Bull. Soc. Mycol. France 103:152
• Shaw, Charles T. and G.A. Kile.1991. Armillaria root disease. Agriculture handbook 691, 233 pp.
• Smith , M., J. Bruhn and J. Anderson, 1992. The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356:428-431
• Smith, M.L., L.C Duchesne, J.N Bruhn,. and J.B Anderson,. 1990.  Mitochondrial genetics in a natural population of the plant pathogen Armillaria.  Genetics 126: 575-582
• Termorshuizen A. and E. Arnolds, 1987. On the nomenclature of the European species of the Armillaria mellea group. Mycotaxon 30: 101-116.
• Velenovský, J., 1920.Ceské Houby 1: 1-950
• Velenovský, J., 1927. Václavka hlíznatá (Armillaria bulbosa Barla) Mykologia (Praha) 4: 116-117; translation to English by Vladimír Antonín. (Pers. Comm.)
• Volk, Thomas J. and Harold H. Burdsall, Jr. 1995.Nomenclatural study of Armillaria and Armillariella species (Basidiomycotina, Tricholomataceae) Fungiflora, Oslo, Norway: Synopsis Fungorum 8, 121 pp. ISBN 82-90724-14-4
• Volk, Thomas J. 1995-2002. Tom Volk's fungi. TomVolkFungi.net

If you have anything to add, or if you have corrections or comments, please write to me at volk.thom@uwlax.edu

You can read about other species of Armillaria here and about the discovery of Armillaria nabsnona here

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