Title: Trial field key to the species of PHOLIOTA in the Pacific Northwest
Author: Ian Gibson
Company: Microsoft

SQUAMANITA in the Pacific Northwest
Prepared for the Pacific Northwest Key Council
by Ian Gibson, South Vancouver Island Mycological Society
Copyright  2007, 2017, 2019, 2023  Pacific Northwest Key Council

INTRODUCTION

The story of Squamanita is told best in a 1994 article in the Canadian Journal of Botany 72: 1812-1824. The article is appropriately titled “Squamanita contortipes, the Rosetta Stone of a mycoparasitic agaric genus.”, by S.A. Redhead, J.F. Ammirati, G.R. Walker, L.L. Norvell, and M.B. Puccio. While many wanderers in the woods will never see a mushroom of this genus, the account is fascinating.

In 1992, sampling was done in stands of old growth Sitka spruce and Western Hemlock on the Olympic peninsula in Washington. “Species X” was found growing on a Galerina mushroom and could not be found in keys of mycoparasitic mushrooms (those that are parasitic on other fungi). Several authors had suspected however that the genus Squamanita was also mycoparasitic. Squamanita mushrooms always have a tuber-like or at least swollen base that is different from the rest of the stem. One of the species, Squamanita contortipes, had some features of Cystoderma mushrooms and had in fact been described originally in that genus. The researchers borrowed the holotype (collection on which the original species description was base) from the University of Michigan. Species X had enough of the same characteristics to identify it as the same species. Now because of the new collections they were able to add information to the picture. They found that the stem of the holotype consisted of three zones, which corresponded in the new collections to the stem of the Galerina, the cap of the Galerina, and the stem of the Squamanita. Squamanita contortipes had been confirmed as mycoparasitic on Galerina.

The story of the genus Squamanita started with the description in 1918 of Lepiota odorata Cool, a species in the Netherlands having an odor of grapes, vinaceous colors, and a swollen base. 

In 1935 another species, odorless and yellow, initially termed Tricholoma X, made its appearance in Switzerland. Schreier incubated bulbs and showed they gave rise to mushrooms independent of the mycelium at the base of the bulbs. This eventually was named Squamanita schreieri, the genus being based on the presence of a basal bulb. 

When Bas was monographing the genus Squamanita in 1965, Alexander Smith brought to his attention an atypical Cystoderma. Smith and R. Singer had completed a world-wide monograph of Cystoderma in 1945 and added this species from Mount Hood National Forest in Oregon in 1948. They had named it Cystoderma paradoxum. The species name paradoxum expressed their puzzlement. “There are still some questions to be answered in regard to this fungus. One is whether or not it really grows from very decayed mushrooms or is truly terrestrial. S-25003 gave some evidence of having come from a decayed fruiting body of a fleshy fungus but the remains were too far gone for any identification.” The base of the stem had a surface layer with spherical cells called spherocysts (typical of Cystoderma), but the surface layer of the cap was an atypical filamentous layer. 

Bas realized that Cystoderma paradoxum was a Squamanita, as was another species, Squamanita pearsonii, previously misdiagnosed as Cystoderma paradoxum. The genus was redescribed, specifying that the fruitbodies arise from “simple to compound sclerotial bodies” which they termed “protocarpic tubers”. (A sclerotial body is a more or less rounded mass of hyphae, usually underground, that may give rise to mycelium or a fruitbody.) Despite the inclusion of seven species, further mysteries remained. For example, “The interpretation of veils and velar remnants offers a real problem in Squamanita … To summarize it may be said that in the genus Squamanita probably three veils are potentially present.”. Bas also mentioned the fact that three of the seven Squamanita species appeared to produce chlamydospores abundantly on or just below the outside layer of the bulb. These thick-walled asexual spores are rather rare in gilled mushrooms.

Successive collectors (P. James, J. Pitt) noted later that the collections seemed to be growing on Cystoderma amianthinum, and Reid speculated in 1983 that S. paradoxa might be a parasite on C. amianthinum. Later a Squamanita was found in Japan in association with Phaeolepiota aurea, growing on basal masses bearing the characteristic horned spherocysts typical of P. aurea, suggesting that this Squamanita might also be mycoparasitic.

As a result of finding Squamanita contortipes in Washington, the picture of the genus became more clear. The collections of S. contortipes appeared to be growing on two different species of Galerina. Drawing together various lines of evidence, the authors of the 1994 Canadian Journal of Botany article concluded that for the majority of described Squamanita species, the bodies at the bases were in fact parasitized gilled mushrooms. The proposed hosts included Cystoderma (S. paradoxa, S. pearsonii), Galerina (S. contortipes), Phaeolepiota (S. phaeolepioticola nom. prov.), and possibly Amanita (S. schreieri) and Kuehneromyces (S. fimbriata). In 1997, Vizzini and Girlanda presented evidence that Squamanita umbonata is a parasite of Inocybe oblectabilis. Squamanita umbonata was described in 1914 from Pennsylvania and also recorded from New York, Massachusetts, and Rhode Island. 
 
Parasitism alone would be insufficient to recognize a genus. Several gilled mushrooms are parasitic on other mushrooms (Collybia, Asterophora, Psathyrella epimyces, and Volvariella surrecta, to name some in the Pacific Northwest). Two additional features were found to characterize the genus Squamanita: chlamydospore production in the hosts, and the contemporaneous production of colorless and pigmented basidiospores.

The story is not finished. Three described species are still poorly known. Squamanita squarrulosa was described from New Zealand. In 1998 Squamanita citricolor was described from Zaire. In 1999 Squamanita granulifera was described from South America. The hosts for all of these are unknown.

“Seven species have yet to be described: 1) Squamanita tropica nom. prov. from Malaysia (Bas, 1965); 2) S. nepaliensis Bas, Tulloss & Bhandary nom. prov. from Nepal (Rodham Tulloss, pers. comm.); 3) S. phaelepioticola nom. prov. from Japan (Nagasawa et al., 1990; Redhead et al., 1994); 4) Squamanita sp. from Guyana (Cathie Aime, pers. comm; listed on GBIF); 5) Squamanita calyptrata Matsuda & Bas (listed in GBIF); 6) an unnamed Squamanita sp. recorded from Japan (listed in GBIF); 7) Squamanita cettoiana M.M. Moser from Italy (Moser, 1978).” (Griffith(1)).

In 2007, molecular evidence was presented that Hebeloma mesophaeum is a host for Squamanita odorata. In 2010, Matheny and Griffith presented molecular evidence confirming Cystoderma amianthinum as a host for S. paradoxa. In 2019, Griffith et al. showed that the same species was a host for S. pearsonii. Other species and hosts will be no doubt be documented in future. Which other Galerina species may be hosts for Squamanita contortipes? 

A case can be made that at least some Squamanita species should have their current names in Dissoderma. Four species reported from the Pacific Northwest were checked in MycoBank and the online Species Fungor on October 17, 2023 (contortipes, odorata, paradoxa, and pearsonii). Current names were in the genus Dissoderma in MycoBank, but in the genus Squamanita in Species Fungorum.

Any wanderer in the woods, if lucky as well as observant, might make a new discovery about this intriguing genus.

KEY TO SQUAMANITA IN THE PACIFIC NORTHWEST

1a	Fragrant odor of grapes; cap and stem light purplish gray with coarse dark purplish gray scales, light purplish gray gills; growing from ochraceous amorphous gall; basidiospores 6.5-8.5(9.3) x 4.2-6.2 um, not amyloid	Squamanita odorata
1b	No grape odor; cap, stem and gills with gray or purplish gray colors, but may be either fibrillose or scaly; growing from Galerina or from stem-like gall; spores otherwise	2

2a	Cap gray or purplish gray, the disc at times with tiny recurved scales, mycenoid, fragile, 3-15 mm across; growing on Galerina or stem-like gall; basidiospores amyloid, round or nearly round, 5-7.2 x 5-6.6 um	Squamanita contortipes
2b	Cap not as above: may be more robust or larger, may have coarse scales over the whole cap; known galls stem-like; spores elliptic, not amyloid	3

3a	Cap grayish to violaceous lilac with strongly contrasting dark purple recurved scales centrally; gills whitish; chlamydospores globose, pitted, brownish yellow, basidiospores 7.2-8.9(10.1) x 4.3-5.1(6) um, ellipsoid to elongate	Squamanita pearsonii
3b	Cap pallid lilac to violaceous drab and matted to appressed fibrillose centrally; gills very pale dull purplish; chlamydospores irregularly subglobose, smooth, pale yellow brown, basidiospores (8.5) 9-10 (11) x 4.5-6 um, ellipsoid	Squamanita paradoxa
                                                                                                                   
SPECIES DESCRIPTIONS

Squamanita contortipes   (A.H. Sm. & D.E. Stuntz) Heinem. & Thoen
FRUITBODY mycenoid, fragile, fleshy, forming on the cap of Galerina fruitbody (up to three per Galerina), turning it into a gall which may look somewhat like the Galerina cap or may be transformed into a form where it looks like an extension of the Squamanita stem. CAP 0.3-0.5(1.5) cm across, parabolic to somewhat bell-shaped (mycenoid), fragile; gray, or dull purplish on disc and paler lilac-gray toward margin; fine recurved scales centrally, more fibrillose toward margin and scales more appressed, becoming farinose (mealy) toward margin, partially translucent-striate, margin scalloped and with hanging grayish hair-like fibrils; flesh grayish. GILLS broadly adnate, subdistant to distant (with 1 tier of subgills), broad, thickish; pale gray to dull purplish. STEM 0.5-3.5 cm x 0.1-0.35 cm, equal with slightly swollen base; gray like cap; scaly with squarrose, coarse, fibrous scales on lower two thirds, above which there are fine striations. FRUITING single to tufted on logs or in moss under conifers, forming on cap of Galerina species or from stem-like gall. SPORE COLOR whitish. MICROSTRUCTURES spores 5-7.2 x 5-6.6 microns, nearly round or round, smooth, colorless (but scattered dark ones on older gills), amyloid; basidia 4-spored; pleurocystidia absent, cheilocystidia clubshaped, 25-55 x 15-20 microns but unevenly distributed and absent along some edges; clamps present; also chlamydospores colorless, warted to partially ridged, mostly intercalary, in host cap tissue at stem base.

Squamanita odorata  (Cool) Bas  
FRUITBODY distinguished by coarsely scaly purplish cap and stem, similarly colored gills, ochraceous amorphous gall from which it arises, strong grape-like odor, and amyloid spores. CAP 1-4.5 cm across, obtusely bell-shaped to convex expanding but usually retaining broad umbo, sometimes with depressed center; brownish purple to purplish gray or lilac-gray often darkening with age; densely scaly or fibrillose-scaly, the scales rather coarse, pointed, and recurved, less scaly toward margin which may be merely densely fibrillose and torn; flesh lilac gray to whitish in cap and stem but ochraceous buff in gall. GILLS adnate or notched, 20-28 reaching stem, 1-3 subgills between each pair of gills, 5-7 mm broad, rather thick, more or less interveined, violaceous lilac-gray, edges concolorous. STEM 1.0-3.5 cm x (0.2)0.3-1.0(1.5) cm, cylindric or widening slightly downward; color similar to cap, satiny-fibrillose in upper part, lower part with 2-4 incomplete rings of more or less erect, floccose-fibrillose, dark violaceous gray-brown scales, similar to those on cap, stem arising from gall-like, usually marginate, ochraceous bulb, often fused with other bulbs or with several bulbs seated on a common basal one, each bulb 1-3.0 cm x 0.6-2.5 cm, nearly spherical to ellipsoid, rather soft, outside of bulb may be felted. ODOR like ripe grapes or grape juice, or like the artificial grape flavouring in candy and soft drinks, or like Hebeloma sacchariolens; gall smells radish-like. TASTE mild; gall reminiscent of Hebeloma species. FRUITING It fruits in wooded areas, usually where soil structure disturbed; in 2007, molecular evidence was presented that Hebeloma mesophaeum is a host. SPORE COLOR white to dingy pinkish or dingy yellowish. MICROSTRUCTURES basidiospores 6.5-8.5(9.3) x 4.2-6.2 um, broadly ellipsoid, smooth, colorless to slightly dingy, not amyloid and not dextrinoid; basidia (2)3-4-spored; pleurocystidia and cheilocystidia absent; some septa with clamps.
 
Squamanita paradoxa  (A.H. Sm. & Singer) Bas
FRUITBODY The grayish to purple gray cap is appressed-fibrillose, at the margin sometimes appressed-fibrillose-scaly/ Gills are pale dull purplish. The stem is similarly colored to the cap and fibrillose or somewhat scaly. At the base is an ochraceous brown stem-like gall. CAP 0.8-3.5 cm across, convex to flat-convex, often with broad low umbo, sometimes flat or even slightly depressed in center, pallid lilac to dark violaceous or lilac gray; appressed-fibrillose, at margin sometimes appressed-fibrillose-scaly, only slightly translucent-striate when wet; flesh in stem and cap grayish violaceous, grayish lilac, or pale brownish drab, in gall pale with ochraceous brown outline. GILLS arcuate-adnate, subdecurrent, broadly adnate or adnexed, subdistant, 10-24 reaching stem, 0-3 subgills between each pair, broad, thick, sometimes anastomosing, intervenose, lilaceous-gray to brownish violaceous (slightly paler than cap), edge concolorous. STEM 0.8-2.5 cm x 0.1-0.6 cm, nearly equal; pale lilac to pale violaceous; fibrillose to somewhat scaly; arising from stem-like to spindle-shaped gall, 2-6 cm x 0.4-1.8 cm, ochraceous brown, granular-warty, often confluent with other such galls or on a common basal body, sometimes lower parts of gall whitish-felted. ODOR mild, or perfume-like when young and fetid when old. TASTE mild. FRUITING growing on mushroom (probably Cystoderma) which it transforms into a stem-like gall. SPORE COLOR white. MICROSTRUCTURES spores (8.5)9-10(11) x 4.5-6 microns, elliptic, smooth, nonamyloid (may be slightly dextrinoid); basidia 4-spored; cystidia absent; clamps abundant; also chlamydospores irregularly subglobose, smooth, pale yellow brown, in tissue of gall.

Squamanita pearsonii  Bas
FRUITBODY The grayish to violaceous lilac cap has strongly contrasting purple scales centrally that are curved upwards. Gills are whitish. At the base is an ochraceous yellow stem-like gall. CAP 1.0-2.5 cm across, conic-bellshaped becoming convex to flat; grayish to violaceous lilac; centrally with strongly contrasting, darker purple, recurved scales that are pointed and rather narrow, the scales more appressed and scattered toward margin, margin fringed; flesh thin and light violet in cap, paler in stem, and yellow in gall. GILLS broadly adnate, sometimes also notched, 20-25 reaching stem, 1-3 subgills between each pair of gills, moderately broad, interveined, white when young, purple-brown when old, edges concolorous, smooth to slightly scalloped. STEM 2.0-3.0 cm x 0.3-0.6 cm, cylindric or widening slightly downward, with swollen, sometimes slightly marginate, turnip-like to spindle-shaped basal gall about 2.0 cm x 0.8 cm, main part of stem lilac to purple-brown with dark purple, recurved to slightly recurved scales on lower two thirds, fibrillose to granulose-punctate on the upper part, basal gall cream-yellow to ocher-yellow, somewhat fibrillose under a pale thin pruinose covering (chlamydospores). ODOR and TASTE unknown. FRUITING clustered, up to several fruiting bodies growing out of a common bulb, in meadows, parks, gardens, under hardwoods or conifers, likely on transformed Cystoderma mushroom material. SPORE COLOR unknown. MICROSTRUCTURES basidiospores 7.2-8.9(10.1) x 4.3-5.1(6) um, broadly elliptic, smooth, colorless, dextrinoid (brown-yellow); basidia 2- to 4-spored;pleurocystidia and cheilocystidia not seen; septa with clamps; chlamydospores 10-15 x 8-12 microns on gall, round to nearly round, 3-layered, colorless to red-brown, appearing finely verrucose or pitted. 

REFERENCES

Arora, David.  1986  Mushrooms Demystified   Second Edition.  Ten Speed Press, Berkeley.
Bas, C.  1965.  “The Genus Squamanita.”  Persoonia 3(3): 331-359.
Bas C., D. Thoen.  1998.  “Squamanita citricolor, a new species from central Africa.”  Persoonia 17: 135-139.
Breitenbach, J., Kränzlin, F.  1995.   Fungi of Switzerland  Volume 4 Agarics  Second Part. Edition Mykologia Lucerne.
Griffith, Gareth W., Krzysztof Piotr Gajda, Andrew P. Detheridge, Brian Douglas, John Bingham, Alex Turner, Victoria Bowmaker, Debbie A. Evans, William G. McAdoo, Bryn T.M. Dentinger. 2019. “Strangler unmasked: Parasitism of Cystoderma amianthinum by Squamanita paradoxa and S. pearsonii.” Fungal Ecology 39: 131-141. 
Matheny, P. Brandon, and Gareth W. Griffith. 2010. “Mycoparasitism between Squamanita paradoxa and Cystoderma amianthinum (Cystodermateae, Agaricales).” Mycoscience 51 (6) 456-461.
Mondiet, Nicolas, Marie-Pierre Dubois, Marc André Selosse.  2007.  “The enigmatic Squamanita odora (Agaricales, Basidiomycota) is parasitic on Hebeloma mesophaeum,”  Mycological Research 111:  599-602.
Redhead, S.A., J.F. Ammirati, G.R.Walker, L.L.Norvell, M.B.Puccio.  1994.  “Squamanita contortipes, the Rosetta Stone of a mycoparasitic agaric genus.”  Can. J. Bot. 72: 1812-1824.
Smith, Alexander H, Rolf Singer. 1948.  “Notes on the genus Cystoderma.”  Mycologia 40: 454-460.
Smith, Alexander H., Smith Helen V., Weber, Nancy S.  1979.  How to Know the Gilled Mushrooms.  Wm. C. Brown Company, Dubuque, Iowa.
Stuntz, D.E., B.F. Isaacs.  1962.  “Northwestern Fungi I.”  Mycologia 54: 272-297.
Vizzini, S., M Girlanda. 1997. “Squamanita umbonata (Sumst.) Bas, a mycoparasite of Inocybe oblectabilis (Britz.) Sacc.— preliminary note.” Allionia 35: 171-175.

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