The state of taxonomy of the genus Armillaria

Thomas J. Volk* and Harold H. Burdsall, Jr. Center for Forest Mycology Research, Forest Service,
U. S. D. A., One Gifford Pinchot Drive, Madison, WI 53705-2398

*Current address Tom Volk
Dept. of Biology and Microbiology
3012 Cowley Hall
University of Wisconsin-La Crosse
La Crosse, WI 54601

Modified from a paper originally published by Burdsall and Volk, in McIlvainea 11:4-11. 1993.
In particular, the key to the species of Armillaria has been redone.
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The genus Armillaria has been the bane of mycologists ever since its establishment by Fries as a tribe of Agaricus (1821), a genus to which he ascribed nearly every gilled fungus, regardless of spore color, nutritional situation, or other characteristics we use in taxonomy today. Even Fries was uncertain as to how he wanted to recognize the tribe Armillaria; four years later he placed the species in the genus Agaricus, tribe Lepiota (1825), then again recognized the tribe Armillaria in 1838 with twice as many species as it had originally. Finally, in 1857 Staude raised Armillaria to generic rank, and although there has been great discussion regarding the person "legally" responsible for this move, we agree with the arguments that support the authority being Staude (Watling and Kile, 1982), with the genus formally designated Armillaria (Fr.:Fr.) Staude.

Then there is the question of which generic name to apply to this group. Controversy over which author was the first to raise Fries' tribe Armillaria to generic rank have led to the widespread use of Armillariella in the last 15 years or so. Fortunately this dilemma has been resolved, and the generic name Armillariella has been gently laid to rest (stomped to death, actually.) Roy Watling, Glen Kile, and Norma Gregory provided a beautiful eulogy in 1982. We can now ignore the name Armillariella as an obligate synonym of Armillaria and get comfortable with Armillaria for these fungi.

When one considers the broad distribution of its species, it is very surprising that the genus Armillaria has gone so long with so little attention to its taxonomy. For example, at least until the early 1980's here in North America no one had even heard of the widely distributed and very common A.ostoyae. On the other hand, there have been over 250 species referred to the genus Armillaria, although most of these are only distantly related to the group now called by that name. Included among them are species of many descriptions and functions that can now be placed in over 25 modern genera. The genus Armillaria in the modern and biologically functional sense is reserved for facultatively parasitic root and butt rot fungi that produce rhizomorphs. Common species such as Armillaria ponderosa (= Tricholoma magnivelare, the American matsutake) are now found in the genus Tricholoma with other mycorrhizal species. Conversely, the fungus formerly called Clitocybe tabescens belongs in Armillaria with its root-rot relatives.

This paper will concentrate on the taxonomy of Armillaria in the Northern Hemisphere. Most of our comments will also apply to the Southern Hemisphere, but we are not as familiar with those species, and there will be enough names and species concepts without introducing others that may only confuse the issue. Photos of many of the species from both hemispheres can be found in Watling et al. (1991).

Back in the early sixties the literature on A. mellea was extremely confusing. It was considered by different researchers to be either a virulent pathogen (in the west) or a opportunistic pathogen (and then not very virulent) in the eastern United States. Its host range was phenomenal, one of the broadest known for fungi, and its morphology was extremely variable.

In the early seventies Hintikka (1973) developed a technique that allowed the recognition of several European species in this group. Hintikka's technique demonstrated the existence of five Armillaria species in the European species complex. The technique depended on growing single spore isolates together in a petri dish and observing the change or lack of change in colony morphology. Single spore isolates of Armillaria species are generally white and quite fluffy. They need to fuse with a single spore isolate of opposite mating type (not male with female, but similar in effect) in order to complete the life cycle. When fusion of compatible mating types occurs, the coalesced colonies become dark brown, appressed (flattened), crustose, and sometimes (depending on the species) produce rhizomorphs. If the single spore isolates are from different species, the colonies will not grow together and will remain white and fluffy. Using this method, Korhonen (1978) was able to distinguish five Biological Species (BS). These are called biological species rather than morphological species because isolates within a species are able to interact in a biologically meaningful (i.e. sexual) way. In addition, the species were difficult to distinguish using morphological characteristics, which is still the case today. Appropriate names have been applied to each of these European BS as follows: BS A = A. borealis, BS B = A. cepistipes, BS C = A. ostoyae, BS D = A. mellea, BS E = A. gallica (a.k.a. A. bulbosa and A. lutea). Unfortunately, in spite of the ability to distinguish the five European biological species by using mating compatibility, the problem of distinguishing the morphological species that we are more used to dealing with, has not been entirely resolved. Morphological distinctions were (are) still difficult to recognize. Added confusion resulted from the application of different names to these various BS. For example, BS C was called A. ostoyae or A. obscura, depending on who was to be followed and BS E was known as A. bulbosa or A. lutea at this particular time. Later the name A.gallica was to be applied to this BS.

In the mid-seventies Anderson and Ullrich (1979) applied the techniques developed by Hintikka and expanded by Korhonen to isolates collected from widely distributed locations in North America. This work 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). This led to substantial confusion in both mycology and forest pathology circles; the more conservative element, who liked the simple concept of Armillaria mellea referring to all the taxa, felt that "those damn splitters" were playing some more nomenclatural games (as taxonomists have been known to do). In 1988, Anderson determined that two of the NABS delimited in 1980 were superfluous. However, by this time another biological species, NABS XI, had been recognized by Morrison et al. (as species F, 1985), and with A. tabescens now considered a member of the genus, the species count was once again ten. Anderson et al. (1980) demonstrated the genetic compatibility of the NABS with all but one of the European BS; only A. borealis was found to be genetically isolated (incompatible) from all the NABS. As a result the NABS have been designated by the names of their European counterparts with the exception of NABS V and X which are incompletely and inconsistently compatible with A. cepistipes of Europe.

With this new technology available for the distinguishing of species of Armillaria, mycologists both in North America and in Europe began trying to distinguish the biological species using morphological characters. This desire led to the accumulation of as many characters as can be brought to bear to make these distinctions. As always we like the easy characters, but easily used characters are in short supply in this group. Some of the more familiar characters, including spore size and shape, are not useful characters for this endeavor, since they overlap or are very similar between taxa.

However, there are morphological characteristics that can be used with practice and experience on fresh specimens. Color of the basidiome, presence and type of squamules, shape and color of the stipe, habit, host associations, and geographical distribution can all be used in the effort to distinguish the species. However, applying the characters to dried specimens is very difficult at best and providing a written description from which a dried specimen can be identified, at least with some of these species, is practically impossible. Distribution is an important character for some species, but more as a negative character, and the possibility that an exception is in hand is always a problem. For example, after three years of heavy collecting of Armillaria in Wisconsin and northern Michigan we were "absolutely" convinced that A. mellea sensu stricto was restricted to the southern half of Wisconsin, but in the fourth year we found A. mellea s.s. in the Upper Peninsula of Michigan! The point is, since the concept of having many Armillaria species is relatively new, the exact distributions of many of the species is incomplete because the sometimes complicated determination of the correct species is being practiced by only a relatively few laboratories.

One of the primary questions that is asked is why does anyone care about distinguishing the species of Armillaria? From the mycophagist's view they are all similarly edible and delicious, although there are unconfirmed reports from the Pacific Northwest about slight toxicity of Armillaria ostoyae collected on hemlock. But from the view of the forester, it becomes very important to distinguish between species that vary greatly in their pathogenicity. For example A. mellea is known to kill trees, especially oaks, that have been weakened by drought or other pathogens. A. ostoyae is known as a virulent pathogen of conifers. On the other hand A. gallica is usually an innocuous saprophyte, living on organic matter in the soil and not harming trees to any great extent. A forester finding an Armillaria fruiting in the woods would like to be able to tell whether or not there is a potential problem with Armillaria root disease so that mitigative procedures can be taken if necessary. Very little is known about the pathogenicity of the other species of Armillaria at present.

In spite of the difficulty in describing the species characteristics sufficiently to allow easy identification of Armillaria species, three of the NABS not found in Europe have been described, as A. gemina (NABS II), A. calvescens (NABS III) and A. sinapina (NABS V). The last mentioned is partially compatible with A. cepistipes from Europe as is the unnamed NABS X. NABS IX, X, and XI are still to be described and named. These species are rarely found fruiting and are thus delimited from the other species based on their incompatibility reactions. It is possible that additional biological species will be found with further collecting and testing against cultures of known species. It is also possible that additional species will be "demoted" to sub-species.

Since the delimitation of the segregates of the Armillaria mellea complex began, numerous nomenclatural problems and inconsistencies have been encountered. An example is that of deciding whether the name A. obscura or A. ostoyae should be used. It was finally determined that the concept of A. obscura was not firm enough to be used and that because there was an available type specimen for the name A. ostoyae, that name was the best to be used (Marxmüller, 1992). The situation with the name A. bulbosa created more confusion because among the several different groups working on this most widely distributed species, the names A. bulbosa, A. lutea, and A. gallica were all being used. Finally with the publication of Marxmüller's article (1992) the nomenclature of the species was settled. Armillaria gallica is the name to be used. Even though the other two names have priority (i.e. they were published earlier), they were rejected as ambiguous names that could refer to a number of species.

Key to species of Armillaria. Using a broad spectrum of characteristics it is often possible to "provisionally" identify the more common Armillaria species of North American. In the Macilvainea article we published a key to the North American species of Armillaria. We have replaced this with another key that uses macroscopic, microscopic and distributional characters. WARNING: there are many inline images of Armillaria species on this page, so it may take a while to load at slower modem speeds.

North American Biological Species (NABS) of Armillaria, some synonyms, and known distributions
NABSSpecies & SynonymsDistribution
I Armillaria ostoyae (Romagn.) Herink
= Armillaria obscura (Schaeff.) Herink [nomen ambiguum]
northern conifer zone, occasionally on hardwoods
II Armillaria gemina Bérubé & Dessureault. northeast USA, Québec, Ontario
III Armillaria calvescens Bérubé. & Dessureault. Québec to Michigan and Wisconsin, Canadian prairie
V (IV)Armillaria sinapina Bérubé & Dessureault. northern conifer zone, but usually on hardwoods in the East and usually on conifer in the West
VI (VIII) Armillaria mellea (Vahl:Fr.) Kummer hardwood zone, mostly southestern USA north to Iowa and Wisconsin and west to Oklahoma and Texas.. Eastern distribution from Florida to the Appalachians to Québec. Also known from California, but not other areas of the West.
VII Armillaria gallica Marxmüller & Romagn.
= Armillaria lutea Gillet [nomen ambiguum]
= Armillaria bulbosa (Barla) Kile & Watling [misapplied name]
hardwoods, deep South to Northeast to Midwest, rare in Pacific northwest
IX Armillaria nabsnonaVolk & Burdsall known from Idaho, Washington, Oregon, Alaska, and British Columbia (Volk, Burdsall, & Banik, 1996)
X unnamed known only from British Columbia and Idaho
XI probably = Armillaria cepistipes Velenovsky
= Species F, Morrison et al. 1985
known from British Columbia and Washington (Banik, Volk, & Burdsall, 1996)
Armillaria tabescens (Scop.) Emel Southeastern USA into the Northeast, west to Ohio, also further west and north on shores of Great Lakes
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Literature Cited

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.

Anderson, J.B. 1986. Biological species of Armillaria in North America: redesignation of groups IV and VIII and enumeration of voucher strains for other groups. Mycologia 78: 837-839.

Banik, Mark T., Thomas J. Volk, and Harold H. Burdsall, Jr. 1996. Armillaria species on the Olympic Peninsula of Washington State, including confirmation of North American biological Species XI. Mycologia 88: 492-496.

Bérubé, J.M. & Dessureault., 1988. Morphological characterization of Armillaria ostoyae and Armillaria sinapina sp.nov. Canad. J. Bot. 66:2027-2034.

Bérubé, J.M. & Dessureault., 1989. Morphological studies of the Armillaria mellea complex: Two new species, A. gemina and A. calvescens. Mycologia 81: 216-225.

Darmono, T.W., M.T. Banik, and H.H. Burdsall, 1992. Time and space partitioning of Armillaria mellea and Armillaria gallica. Inoculum 43:30.

Fries, E.M. 1821. Systema Mycologicum. Gryphiswaldae.

Fries, E.M. 1825. Systems Orbis Vegetabilis. Lundae.

Fries, E.M. 1838. Epicrisis systematis mycologici. Upsaliae.

Hintikka, V. 1973. A note on the polarity of Armillariella mellea. Karstenia 13:32-39.

Korhonen, K. 1978. Interfertility and clonal size the in Armillaria mellea complex. Karstenia 18: 31-42.

Mallett, K.I. 1990. Host range and geographic distribution of Armillaria root rot pathogens in the Canadian prairie provinces. Canad, J. Forestry Res. 20: 1859-1863.

Marxmüller, H. 1992. Some notes on the taxonomy and nomenclature of five European Armillaria species. Mycotaxon 44: 267-274.

Morrison, D.J., D. Chu, and A.L.S. Johnson. 1985. Species of Armillaria in British Columbia. Can. J. Plant Pathol. 7:242-246.

Staude, F. 1857. Die schwämme Mitteldeutschlands insbesondere des Herzogthums. Coburg.

Volk, Thomas J., Harold H. Burdsall, Jr. and Mark T. Banik. 1996. Armillaria nabsnona, a new species from western North America. Mycologia, 88: 484-491.

Watling, R., G.A. Kile and N.M. Gregory. 1982. The genus Armillaria - Nomenclature, Typification, the identity of Armillaria mellea and species differentiation. Trans. British Mycol. Soc. 78:271-285.

Watling, R., G. Kile, and H.H. Burdsall, Jr. 1991. Nomenclature, Taxonomy and Identification in Armillaria Root Disease, C.G. Shaw and G. Kile, eds. Agriculture Handbook No. 691. USDA Forest Service. pp. 1-9.

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