ISSN 1188-603X

No. 538 May 24, 2019 Victoria, B.C.
Dr. A. Ceska, 1809 Penshurst, Victoria, BC, Canada V8N 2N6

This BEN issue (# 538), as well as the following one (#539), are dealing with mycological topics. Traditionally, mycology used to be a part of botany before mycologists gained their partial independence.


From: Emma Harrower - Abstract of the University Tennessee Ph.D. Dissertation

Phylogenetics is a powerful tool used for illuminating the diversity of life on Earth, their evolution and their ecology. I created a multi-gene phylogenetic tree of Cortinarius section Cortinarius and uncovered five previously overlooked species, increasing the number of species in the section from seven to twelve. All members of the clade possess both cheilocystidia and pleurocystidia and have a pigment known as (R)-39,49-dihydroxyphenylalanine. Ancestral state reconstruction estimated that the ancestral host was most likely an angiosperm, switching hosts when encountering novel host species in new lands, and only Cortinarius violaceus associating with the Pinaceae in North America. The biogeographic analysis found that it was most likely that the group originated in Australia, dispersed through the long-distance dispersal to South America, where it switched hosts to several members of the Fabaceae, diversified with Quercus in Central America, and then migrated into North America.

To test the 'secotioid' hypothesis, I performed a phylogenetic logistic regression correlating environmental variables with the state of being sequestrate. 'Mean diurnal temperature' and 'mean maximum temperature in the hottest month' were significant in estimating the probability of being sequestrate. None of the precipitation variables were significant. A world map of the distribution of sequestrate specimens included in this study shows the sequestrate taxa being present in temperate areas and absent from the tropics, which is in concordance with the finding that sequestrate taxa occur in habitats with diurnal temperature fluctuation. This study also brings in doubt that moisture is the sole driving force for the evolution of sequestrate taxa.

Recommended Citation:

Harrower, Emma. 2017.
Systematics and Biogeography of the Cortinarius violaceus group and Sequestrate Evolution in Cortinarius (Agaricales). Ph.D. Diss., University of Tennessee, 2017.


From: Brandon Landry - Abstract of the UBC MSc Thesis

Mushrooms of some Galerina species equal the most poisonous Amanita species in their concentrations of deadly amanitin toxins. Although individual Galerina mushrooms are small, eating about ten would risk delivering a lethal dose of amanitins to a child. Understanding which species of Galerina pose an acute poisoning risk requires a better understanding of species boundaries within the genus, as well as broad sampling for the presence of amatoxins.

I analyzed 61 Galerina collections and eight outgroup specimens for the presence of amatoxins using HPLC/LC-MS. I then used multi-locus DNA data (ITS, LSU and RPB2) from a broad sampling of Galerina and outgroup taxa to generate a constraint tree, to which I added 322 Galerina ITS sequences from herbarium specimens at UBC, from A.H. Smith's type material (University of Michigan), and the ITS sequences from Genbank. Then I mapped toxin analysis data onto the resulting phylogeny, which indicated that amatoxin-production in BC Galerina is restricted to two species, Galerina venenata and G. castaneipes. These two species, along with two other reportedly toxic species (Galerina aff. marginata and G. sulciceps) and seven other species whose toxin production status remains unknown, form a broad clade referred to as the Galerina marginata complex. Phylogenetic and toxin data suggest that the sister clade to the Galerina marginata complex (G. badipes) does not produce toxins, implying that the origin of amatoxin production in Galerina is somewhere within the G. marginata complex. Additionally, phylogenetic data also supports past evidence that members of the genus Gymnopilus are nested within the '_Mycenopsis_' lineage of Galerina. The results provide the first comprehensive look at toxin production in Galerina, as well as the first report of additional toxin-producing species in North America. Using the molecular data from this study to update specimen names in herbarium collections and online databases will reduce confusion resulting from inaccurate identifications or misapplied names. Doing so will contribute to ongoing efforts to update of field guides and other resources that list poisonous and edible mushrooms, allowing amateur mycologists, foragers and healthcare professionals to gain a better understanding of which Galerina pose a poisoning risk.

Recommended Citation

Landry, Brandon. 2019.
Phylogenetic relationships of alpha-Amanitin Producing Galerina from British Columbia. M.Sc. Thesis, University of British Columbia, Vancouver, BC [HTML] [pdf]


From: Cathy L. Cripps, Plant Sciences and Plant Pathology Dept., Montana State University

The open, windswept, treeless alpine tundra seems an unlikely place to look for ectomycorrhizal fungi. Typically, we think of these mutualists as forest dwellers whose mycelium needs to attach to tree roots. However, high above treeline, miniature alpine forests of dwarf willow, low bog birch, and Mountain Avens (Dryas) host their own cold-loving fungal partners. When the fungi reproduce, some tower over their plant partners in a reversal of stature, others appear as nanoforms so tiny that several fits on a penny. Locating the right vegetation patches at the right time is key to finding them, and crawling on your belly helps.

Our survey of the alpine fungi of the Rocky Mountains, initially funded by a National Science Foundation grant, has netted over 200 species of alpine macrofungi, half of which are ectomycorrhizal (Cripps & Horak 2008). We have discovered about ten new species, but most have turned out to be known Arctic-alpine species with circumpolar distributions, to which we now add disjunct alpine populations. Really disjunct! Consider that our collecting sites are primarily on the Beartooth Plateau (along the Montana/Wyoming state line) and in the Southern Rocky Mountains of Colorado, thousands of miles from the Arctic, the Alps, Finland, Greenland, Iceland, Scandinavia and Svalbard where Arctic-alpine fungi are better known. Plus we are at latitudes as low as 380 N and altitudes up to 4000 m, while arctic habitats are around 700 N and at sea level. While latitude and elevation vary greatly, hosts, mainly dwarf Salix and Dryas appear to provide unity.

So are they really the same species across continents? New methods (ITS sequencing) now allow us to compare the DNA of collections across continents to confirm that they are the same species. So far, we have molecularly matched Arctic-alpine mycorrhizal species of Inocybe (Cripps et al. 2010, Larsson et al. 2014), Laccaria (Osmundson et al. 2005), Lactarius (Barge et al. 2016), and morphologically matched species of Amanita (Cripps & Horak 2010). Continuing studies on other genera are underway, so when Henry Beker (Mr. Hebeloma!) put out a call for Hebeloma (BEN No. 511) in North America, I jumped at the chance to contribute our Rocky Mountain alpine collections. He had just finished the large 1200 page tome on European Hebeloma (Beker et al. 2016). I met Henry when I hosted the International Arctic and Alpine Symposium on the Beartooth Plateau in 2008 (Cripps & Ammirati 2010). For this project, we were joined by Ursula Eberhardt, Egon Horak, and Vera Evenson and the result was a 54 page paper on 'The genus Hebeloma in the Rocky Mountain alpine zone' published in MycoKeys (Cripps et al. 2018) which I will attempt to summarize here.

Ecology of Hebeloma

As an ectomycorrhizal fungus, Hebeloma contributes to the ability of its plant host to survive in harsh alpine and Arctic habitats. Mycelium attaches to roots, spreads out, and scours the thin, rocky soil for nitrogen and other nutrients that it passes along to its host, whether Salix or Dryas. The fungus lives on photosynthate sugars that leak out of roots, a tidy mutualism or so we thought. Now there is evidence that at least some Hebeloma species also have enzymes for decomposing willow leaves! How does this work? Imagine, willows emerging in spring from beneath the snow, developing leaves, making catkins and seeds, and producing enough carbs to feed the mycorrhizal fungi attending its roots. At some point, when it is warm enough and wet enough, mushrooms are produced to spread their spores. But the interaction is not over. In fall, usually late August in the alpine, dwarf willow leaves turn yellow, drop one whole one inch to the ground, and become captured in the tangle of prostrate branches. We now know that some Hebeloma species can decompose these leaves, capturing and recycling their nitrogen before they blow away (Cripps & Eddington 2005). Nutrients are passed back to the other hand of the fungus whose business is mycorrhizal exchange, and nutrients go back into the host. An efficient system that conserves scant alpine resources.

Identification of Hebeloma

Hebeloma collections are rather easy to identify to genus, but it is difficult to determine species as they overlap morphologically, and the literature had been poor before Henry and crew arrived on the scene. Hebeloma caps are usually rather flattish, smooth, sticky, tan, and often darker in the center and cream on the margin. Most smell like radish or raw potato. The brown spores can be verrucose (finely warted) to almost smooth, and cystidia are found on the edges but not the sides of gills (Vesterholt 2005).

In all, we found 17 species of Hebeloma in the Rocky Mountain alpine zone in Montana, Wyoming, and Colorado (Table 1). The molecular work put them in piles, and we matched the DNA to European specimens for names. Then I back-tracked and tried to make a key useful to those without access to molecular methods, and so that it was possible to at least narrow down the possibilities to a few species. I tried to use easily-observed features such as the color of the cap, presence of a veil, number of gills, and width of the stipe. After that, it might take microscopic measurements or ITS sequencing to really nail the specimen to a particular species. Here is a guide and some helpful hints for tackling Hebeloma the alpine, but keep in mind, the key likely does not include all species. First, it is best to only attempt to identify collections that are in good shape (not frozen, not dried out, not deteriorating), and that include both young and mature mushrooms. This is critical because the very first step is to determine if a veil is present, and this is more likely visible on young specimens. Secondly, are there are brown droplets along the gill edges? If the specimen lacks a veil and has brown droplets on the gills, it is in the Denudata (including Clypsydrioda) group, so named because the cap margin is 'nude'; these are the non-veiled Hebeloma species. Some lack droplets. If it has a veil, it is in the veiled Hebeloma group.

Non-veiled species of Rocky Mountain alpine Hebeloma

We found seven species of non-veiled species in the Rocky Mountain alpine zone. Three are comparatively large with caps 2-6 mm wide with 40-100 gills. The most common in our Rocky Mountain alpine is Hebeloma hiemale (which has been incorrectly called Hebeloma alpinum). This species has a cream, pinkish buff, to pale brownish cap, and it is the only species in this group with distinctly verrucose spores. It is widespread across our Rocky Mountain alpine sites, and is known from similar habitats in Europe, Greenland, Iceland, Scandinavia, Svalbard and Canada. Hebeloma velutipes has similar coloration but possesses a long, white, floccose stipe, and we have found it mostly in Dryas. It is known from Europe with deciduous trees, but Arctic and alpine records exist from Svalbard, and it was previously reported from the Beartooth Plateau (Beker et al. 2010, 2016). Hebeloma avellaneum is a rich brown color, and we found it in the krummholz zone always with spruce nearby, and indeed, it is known to associate with conifers and may not be a true alpine species (Kauffman & Smith 1933). The pale brown, clavate-stemmed Hebeloma alpinum itself turns out to be very rare and ours is the first molecularly confirmed report for the Rockies.

The last three non-veiled species, have smaller caps, 1-2 cm wide, 20-40 gills, and thin stipes 2-4 mm in diameter. Hebeloma aurantioumbrinum caps are pinkish buff to orange brown and often have a delicate white crenate margin (Beker at al. 2016). This species has likely gone under the name H. pusillum which is not an alpine species because of its small size. Hebeloma subconcolor has a brown cap with a distinctly grayish cast. We only report two collections found by L. Gillman from Colorado. It also occurs in the Alps, Greenland, Iceland and Scandinavia. The last species in this group, Hebeloma vaccinum has a reddish brown cap and stipe, and was only found once in the Rockies. It was first described from the Carpathian Mountains of Slovakia, and it occurs in Greenland and Europe (Eberhardt et al. 2015).

Microscopically section Denudata is also characterized by cystidia that are swollen on top (clavate) and spores that are almond-shaped (amygdaliform).


Cap color



Non-veiled, often with gill droplets

Caps small (2-4 cm), with ˂40 gills

1. Hebeloma vaccinum Romagn.

Red brown

Reddish stipe


2. Hebeloma aurantioumbrinum Beker, Vesterh. & U. Eberh.

Pinkish buff

White crenate margin

A, P, G

3. Hebeloma subconcolor Bruchet

Grayish brown

White fibers on stipe


Caps larger (2-6 cm), with 40-100 gills

4. Hebeloma hiemale Bres.

Pinkish, buff, Isabella

Verrucose spores

A, P, R, D, B

5. Hebeloma avellaneum Kauffman

Orange brown


C, S

6. Hebeloma velutipes Bruchet

Pinkish buff

Long floccose stipe

D, S

7. Hebeloma alpinum (J. Favre) Bruchet

Pale brown

Short stem


Veiled, often with dark stipe base

Spores elliptical

8. Hebeloma marginatulum (J. Favre) Bruchet


Hoary, inrolled cap

A, R, P

9. Hebeloma alpinicola A.H. Sm., V.S. Evenson & Mitchel

Red brown

Cespitose, sand case

D, S

10. Hebeloma dunense L. Corb. & r. Heim

Pinkish buff

Stipe fibrils in zones

A, R, P

11. Hebeloma mesophaeum (Pers.) Quιl.

Yellow brown

Spores small


12. Hebeloma excedens (Peck) Sacc.

Pinkish buff

Cuticle exceeds cap


  Spores almond-shaped (amygdaliform)

13. Hebeloma oreophilum Beker & U. Eberh.


Stipe 3-8 mm


14. Hebeloma hygrophilum Poumarat & Corriol


Stipe 1-4 mm, in moss


15. Hebeloma nigellum Bruchet


Stipe 1-4 mm, in moss

S, P

16. Hebeloma spetsbertgense Beker & U. Eberh.


Stipe 1-4 mm, in moss



Veiled species of Rocky Mountain alpine Hebeloma

We report nine species of veiled Hebeloma (section Hebeloma) from the Rocky Mountain alpine (Table 1), and these are more difficult to distinguish from one another. The caps are often but not always two-toned, darker in the center and paler at the margin. Stipes are often black or dark at the base. They fall into two groups depending on if they have elliptical or almond-shaped (amygdaliform) spores, but sans a microscope, I found that those with almond-shaped spores, mostly have very thin long stipes.

Of those with very thin stipes and almond-shaped spores, three species are usually found nestled in moss, a good identifying character; however, they cannot be distinguished from each other without microscopic examination. All have thin stipes (1-4 mm in diameter) and fewer than 40 gills. Hebeloma nigellum is the most common typical alpine species and was called Hebeloma kuehneri in previous works, but these are now synonymized. Hebeloma hygrophilum was first described from subalpine habitats and ours are the first records from the alpine. We report only one instance of Hebeloma spetsbergense, a Svalbard species (Beker et al 2018). The last species in this group, Hebeloma oreophilum, has a wider stipe (3-8 mm) and more gills (over 40) than the other three, but its micro fits this group. It is known from alpine and Arctic areas of the Carpathians, Canada, Greenland, Scandinavia, and Svalbard (Eberhardt et al. 2015).

Microscopically this group has cheilocystidia that are swollen on top and bottom, and the spores are amygdaliform, finely verrucose, and dextinoid. The second group of veiled Hebeloma species have wider stipes (4-8 mm), and elliptical, smoothish spores. The first two, Hebeloma marginatulum and Hebeloma alpinicola have dark brown caps. Hebeloma marginatulum is more common, although most collections are from Colorado. It can be recognized by its hoary covering and persistently in-rolled margin. It has been mistaken for Hebeloma bruchettii, a famous alpine fungus, which is now folded into Hebeloma mesophaeum (Beker et al. 2016). It is considered to be restricted to arctic and alpine habitats and occurs in Canada, Greenland, Scandinavia, Svalbard, the Alps, and the Carpathians (Eberbardt et al. 2015, Beker et al. 2016). Hebeloma alpinicola is more reddish brown and fruitbodies are often in clusters with the base encased in sand. It is a North American Smith species and is part of a complex that is mostly subalpine and still needs to be sorted out (Smith et al. 1983).

The last three species in this group have a paler coloration than those described above, but the cap center can be darker. Hebeloma mesophaeum is thought to be a common species and is often reported from alpine and other habitats as a default species. However, we found only two collections from Colorado in what is likely a complex. Caps appear to be more yellowish brown or ocher than other species in this group which are more pinkish. Smith described a number of subalpine varieties that still need to be addressed (Smith et al. 1983). Hebeloma bruchettii is now considered part of this complex. The species itself is recognized by its rather small spores that are less than 10 microns long. However, the second species here, Hebeloma excedens, also has small spores. It has a more uniform pinkish buff coloration, the cuticle can exceed the margin, and there are fibrils in zones on the stipe. Hebeloma excedens was first described by Peck, a North American mycologist and may be widespread across North American in non-alpine habitats (Peck 1872). The last species, Hebeloma dunense has a similar rather uniform pinkish buff coloration, and also fibrils on the stem, but our specimens have rather decurrent gills. It was originally described from low elevation dunes, and more recently was recognized from Arctic and alpine habitats with willows (Beker et al. 2016).

Microscopically this last group also has cheilocystidia that are swollen on top and bottom, and the spores are rather small, smooth, and not dextrinoid.

Alpine and Arctic host plants of Hebeloma species

In the Rocky Mountain alpine zone, the main host plants for our Hebeloma species are: dwarf willows Salix reticulata and S. arctica, shrub willows, Salix glauca and S. planifolia, and in the Rose family Dryas octopetala. Betula rotundifolia is rare and we only connected one of our Hebeloma species to this host. In other Arctic and alpine areas, these Hebeloma species are primarily reported with Salix species. However, only Hebeloma alpinum, H. aurantioumbrinum, H. subconcolor, H. marginatulum, H. oreophilum, H. nigellum, and H. spetsbergense appear to be restricted to Arctic and alpine habitats (Beker et al. 2016). The other species, including Hebeloma avellaneum, H. dunense, H. excedens, H. hiemale, H. hygrophilim, H. mesophaeum, H. vaccinum and H. velutipes are also found at lower elevations and in other habitats, and should be looked for in our subalpine forests. All of the species have been confirmed to have intercontinental distributions except Hebeloma alpinicola, H. avellaneum and H. excedens which so far remain as North American species; this is the first time they have been reported from alpine habitats, however krummholz conifers were present for some collections.

The distribution of various ectomycorrhizal host plants in the Rocky Mountain alpine have been shaped by glaciation, topography, parent rock, and climate. A view from the North Pole shows Arctic areas as more contiguous than is generally considered, and corridors during interglacial periods stretched from the Rockies to Siberia allowing migration and genetic mixing. It remains to be seen how altered climate will affect these species and especially with shrub encroachment imminent (Geml et al. 2015).


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Systematics of the ectomycorrhizal genus Lactarius in the Rocky Mountains alpine zone. Mycologia 108(2): 414–440.
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A review of the genus Hebeloma in Svalbard. Mycoscience 59(4): 303-309.
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