The State of Taxonomy of the Genus Armillaria

Home , Armillaria, Armillaria calvescens, Armillaria gallica, Armillaria ostoyae, Armillaria tabescens, Lepiota

THE STATE OF TAXONOMY OF THE GENUS ARMILLARIA

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

The genus Armillaria has been the bane of mycologists ever since its estab- lishment 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” respon- sible 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 surpris- ing 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 Ticholoma 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).

4 Back in the early sixties the literature on A. mellea was extremely confus- ing. It was considered by different researchers to be either a virulent pathogen (in the west) or an 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 diflicult 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 diftlcult 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. lutes 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 sim- ple 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.

5 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 distinguishing 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 for this endeavor, since they overlap or are very similar between taxa. Nevertheless, with practice and experience, there are morphological characteristics that can be used 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 con- vinced” 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 distribution of many of the species is incomplete because the sometimes complicated determination of the correct species is being practiced by only 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 by 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 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 Xl are still to be described and named. These species are rarely found fruit-

6 7 ing and are thus delimited km 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 subspecies. 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. lutes, 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. Using a broad spectrum of characteristics it is often possible to “provision- ally” identify the more common Armillaria species of North America. The following key may be of use in such a venture. We are currently developing a key using both macroscopic and microscopic characters, once we figure out what those are.

8 5. Annulus cortinaceous, very thin and collapsing quickly on the stipe as a fibrous zone, usually with bright yellow tints, but sometimes pale cream; cap brown to reddish brown, covered with rather dense brown fibrils, sometimes with small scales; stipe 5-8 cm long, 0.5-1 cm broad at apex, slightly wider at base, shades of brown toward base but covered with a thin layer of appressed yellow fibrils or more distinct annulations of bright yellow fibrillar material (remains of the yellow fibrous universal veil); occurring mainly on deciduous trees in the northern tier of the eastern United States and throughout forested areas of southern Canada, but frequent on conifers in the Pacific Northwest ...... A.. sinapina 5. Annulus not yellow ...... 6. 6. Cap light to medium brown, covered with reddish brown to dark brown fibrils sometimes clustered into hair-like tufts, occasionally scaly, annulus membranous to thick and cottony, with brown pigmented margin, stipe nearly concolorous with cap, tapered to base, occurring in small to large clusters, most frequently found at base of dead or dying conifers, distributed throughout the northern United States and southern Canada ...... A. ostoyae 6. Nearly identical to A. ostoyae but associated only with deciduous trees, especially maple; distributed from southern Quebec and Ontario through northeastern USA ...... A. gemina

Morphological descriptions of species. Armillaria mellea (Vahl:Fr.) Kummer. Although this name was widely used for nearly all members of the genus until the 1970’s, true Armillaria mellea has a smaller distribution, occurring mainly in the southeastern United States up into the northeast into Quebec and in the midwest in the hardwood forests, although it is occasionally found on conifers in mixed forests. It has been reported from northern California but is not common in the west. Although A. mellea is the type species of the genus, it is rather different than the other species, and is relatively easy to identify with practice. It is char- acterized by its clustered caespitose habit, usually 8-10 but sometimes in groups of 30 or more, which results in a tapered to pointed base on each individual stipe. The pileus is honey colored and the surface is smooth, with no squamules. However, the most consistent character of this species is microscopic; this is the only species of Armillaria that lacks clamp connections at the base of the basidia. Spores 7.2-8.9 X 5.6-6.7 µm. Armillaria ostoyae (Romag.) Herink. This species is mostly restricted to conifers and is a serious pathogen of many species in the northern conifer zone. It is also found in caespitose clusters, sometimes pointed at the bases of the individual stipes, with a brownish annulus. The pileus is brown, covered by dark scales, and can be very large, up to 1 foot in diameter, especially in the Pacific Northwest. This is the species that has been reported to cause some people some gastrointestinal upset if collected from hemlock, but we believe that most of the reported upset is due to undercooking (and overeat- ing) of some of these larger collections. Spore size 8-11 X 5.5-7 µm. Armillaria sinapina Bérubé & Dessureault. This species is similar in color

9 to A. ostoyue, with similar, although somewhat smaller dark scales on the pileus. It normally occurs singly or sometimes in clusters of two or three. In the Northeast it can be found mainly on hardwoods and occasionally conifers, but in the Pacific Northwest (Idaho, Washington, Alaska) it appears to occur only on conifers. The major morphological character that distinguishes this species from the others is the “presence of a golden yellow universal veil that covers young fruiting bodies and later leaves remnants consisting of yellow warts or lumps of tissue on the cap, a yellow fibrous annulus, and many patches of fibers on the stipe” (Bérubé & Dessureault, 1988). Spore size 8.2- 10 X 5.9-8 µm. Armillaria gallica Marxmüller & Romagnesi. This is by far the most widely distributed species east of the Rocky Mountains, including the northeast, midwest, and Gulf coast, but is very rare in the west. It is almost always found on hardwoods, but occasionally on conifers. It can be distinguished by its solitary to gregarious habit, usually on soil, but occasionally “climbing” onto logs or stumps to fruit. The fruit bodies, which tend to be smaller than the other species, are directly attached to rhizomorphs (Darmono et al., 1992). The partial veil is cortinaceous, i.e. very similar to the cobwebby cortina of a Cortinarius species, leaving white “arachnoid” remnants on the stipe. The pileus is “tan to pinkish brown” and “distinctly hairy” (Bérubé & Dessureault, 1988). The base is commonly swollen and sometimes stains yellow where bruised. Spore size 7.2-9.5 X 4.8-6 µm. Armillaria calvescens Bérubé & Dessureault. This species is very similar to A. gallica. It is also found solitary on the soil, but is usually found in large clusters, sometimes up to several hundred fruiting bodies, although the stipes do not radiate from a common point as in A. mellea. Pileus tan to brown, with no scales, but a finely fibrillous surface that can be easily rubbed off, leaving a “mealy” texture between your fingers. Veil golden yellow, sometimes not easily observed, sometimes leaving fibrils on the stipe, which is often swollen at the base. Usually found on maple in southeastern Canada and New England, but also found on a variety of other hardwoods west to Michigan and Wisconsin. The mycelium of this species has also been found in the Canadian prairie provinces, although it has not been observed fruiting there (Mallett, 1990). Spore size 8.5-10 X 5-7 µm. Armillaria gemina Bérubé & Dessureault. This is a rare species, reported only from southern Quebec, southern Ontario, upper New York state and Vermont, down to West Virginia. It is identical to A. ostoyae in terms of habi tats, pathogenicity, and morphology (Bérubé & Dessureault, 1989), but known only from hardwoods. It can usually be distinguished by geography, but in areas where the ranges of the two species overlap, they can be distinguished only by cultural studies. Spore size 8.2-10 X 5.2-7 µm. Armillaria tabescens (Scop.:Fr.) Dennis, Orton, & Hora. This is the only species of Armillaria in North America without an annulus of any type. It is very common in the southeastern United States, but can be found into Ohio, Michigan, and Illinois, especially in moderated climates near the Great Lakes. It is always found in caespitose clusters, usually 8-10 mushrooms, but sometimes of 50 or more. Spore size 8-10 X 5-7 µm.

10 Literature Cited

11 North American Biological Species (NABS) of Armillaria some synonyms, and known distributions

NABS Species & Synonyms Distribution

I Armillaria ostoyae (Romagn.) Herink northern = Armillaria obscura (Schaeff.) Herink conifer zone [nomen ambiguum] II Armillaria gemina Bérubé & Dessureault northeast USA, Quebec, Ontario III Armillaria calvescens Bérubé & Dessureault Quebec to Michigan and Wisconsin, Canadian prairie V (IV) Armillaria sinapina Bérubé & Dessureault, northern but partially interfertile with A. cepistipes conifer zone VI (VIII) Armillaria mellea (Vahl:Fr.) Kummer hardwood zone, N. California to Wisconsin to the Appalachians to Quebec VII Armillaria gallica Marxmüller & Romagn. hardwoods, deep =Armillaria lutes Gillet [nomen ambiguum] South to Northeast =Armillaria bulbosa (Barla) to Midwest, Kile and Watling [misapplied name] rare in Pacific northwest IX unnamed known from Idaho, Connecticut, Alaska, and British Columbia X unnamed, but partially interfertile with known only from A. cepistipes British Columbia and Idaho XI Interfertile with A.cepistipes Velenovsky known only from = Species F, Morrison et al. 1985 British Columbia Armillaria tabescens (Scop.:Fr.) Southeastern USA Dennis, Orton, & Hora into the Northeast, west to Ohio, S coasts of Great Lakes

Journal of American Amateur Mycology

Vol. 11 No. 1 1993 Publisbed by the North American Mycological Association

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