I>Pholiota olivaceophylla , a forgotten name for a common snowbank fungus, and notes on Pholiota nubigena</I

Abstract

A name has been found for a common species in Pholiota subg. Flammuloides fruiting during and soon after snowmelt in the subalpine Abies forests of California: Pholiota olivaceophylla is characterized by rather pale slime-covered basidiocarps, relatively
pale brown ellipsoid to slightly phaseoliform spores, 6.0–8.5 × 3.5–5.0 μm, with an inconspicuous germ pore, and abundant lageniform pleurocystidia. The ITS sequence of the type collection of Ph. olivaceophylla matches those of recent collections. From phylogenetic
analyses and morphology, it is clear that the secotioid Nivatogastrium nubigenum [= Pholiota nubigena] is nested within Pholiota; this species has retained ballistospores and the typical curved sterigmata for active spore dispersal.

Full text

ISSN (print) 0093-4666 © 2015. Mycotaxon, Ltd. ISSN (online) 2154-8889
MYCOTAXON
http://dx.doi.org/./.
Volume 130, pp. 517–532 April–June 2015
Pholiota olivaceophylla, a forgotten name for a common
snowbank fungus, and notes on Pholiota nubigena
N S, N H. N,  E C. V*
1 25 Prospect Hill Rd, Royalston MA 01368-9206, USA
2 Department of Plant Biology, 250 Biological Sciences, University of Minnesota,
1445 Gortner Ave., St. Paul, MN 55108, USA
3111 Koshland Hall #3102, University of California Berkeley, Berkeley CA 94720-3102, USA
* C : ecvellinga@comcast.net
A — A name has been found for a common species in Pholiota subg. Flammuloides
fruiting during and soon aer snowmelt in the subalpine Abie s forests of California: Pholiota
olivaceophylla is characterized by rather pale slime-covered basidiocarps, relatively pale
brown ellipsoid to slightly phaseoliform spores, 6.0–8.5 × 3.5–5.0 µm, with an inconspicuous
germ pore, and abundant lageniform pleurocystidia. e ITS sequence of the type collection
of Ph. olivaceophylla matches those of recent collections. From phylogenetic analyses and
morphology, it is clear that the secotioid Nivatogastrium nubigenum [=Pholiota nubigena]
is nested within Pholiota; this species has retained ballistospores and the typical curved
sterigmata for active spore dispersal.
K  — Abies magnica, biodiversity, Strophariaceae
Introduction
e genus Pholiota (Fr.) P. Kumm. is generally characterized by (pale) yellow
to brown basidiocarps with (in most species, notably excepting the type) a
viscid to gelatinous, oen scaly, pileus, an annulus, rusty to dark brown smooth
to slightly rough spores with a germ pore, cheilocystidia and pleurocystidia
(in a number of species as chrysocystidia), and typically lignicolous habit (e.g.,
Jacobsson 2009). Smith & Hesler (1968), in their overview of North American
species of Pholiota, used a rather broad genus concept but a narrow species
concept and gave descriptions of 205 species for North America, 163 of which
were described as new. Subsequently, several of these species were shown to
be synonyms of each other or to belong to other genera that even Smith &
Hesler (1968) recognized as distinct, e.g., Agaricus L. and Stropharia (Fr.) Quél.

518 ... Siegel, Nguyen, & Vellinga
1e name Flammula (Fr.) P. Kumm., published in 1871, is a later homonym of Flammula
(Webb ex Spach) Fourr. from 1868, a genus in the Ranunculaceae; Donk (1962) considered
the latter to be invalid, but his point of view is not followed by later authors such as
Jacobsson (2012). A proposal for conservation of the fungal genus Flammula has been put
forward by Redhead (2013).
(Jacobsson 1990, 1997; Noordeloos 1999; Norvell & Redhead 2000; Redhead
1984a,b). In modern treatments of Pholiota for various regions in Europe with
narrower genus concepts, 24–28 species are recognized (Holec 2001, Jacobsson
2009, Noordeloos 2011, Holec & Kolařík 2014, Holec et al. 2014) [excluding,
among others, Crassisporium Matheny et al., Flammula1 (Fr.) P. Kumm.,
Flammulaster Earle, Hemipholiota (Singer) Bon, Hemistropharia Jacobsson &
E. Larss., Kuehneromyces Singer & A.H. Sm., Meottomyces Vizzini, Phaeolepiota
Maire ex Konrad & Maubl., Phaeonematoloma (Singer) Bon, Phaeomarasmius
Scher., and a number of Tubaria species, comprising 40–50 species]. e
reasons for the discrepancy in species totals between Europe and North America
are multiple; it is due partly to a strong dierence in both genus and species
concepts and reliance on poorly documented earlier descriptions in order to be
comprehensive or partly reects variation in fresh basidiocarp characteristics
leading to multiple descriptions of species. e aspect of the basidiocarps
changes dramatically due to weather – the slimy species are dry during dry
weather; furthermore, in the species of Pholiota subg. Flammuloides A.H. Sm.
& Hesler the pleurocystidia show considerable variation in incrustation, wall
thickness, and coloration among collections of the same species (see below).
As a result species recognition based on morphology alone can be challenging.
Many new species described by Smith & Hesler (1968) were based on only
one collection, and the authors probably underestimated the variability of the
species they described.
A common snowbank species in Pholiota subg. Flammuloides (with a
gelatinous pileus surface and conspicuous lageniform pleurocystidia but
without chrysocystidia) was regularly found in California’s Red Fir (Abies
magnica A. Murray bis) zone in the Sierra Nevada and Southern Cascade
mountains. For a number of years the fungus was considered undescribed
(Arora 1986), but a scrupulous combing of Smith & Hesler’s 1968 Pholiota
monograph turned up one possible name: Pholiota olivaceophylla. is species
was described based on one collection, occurring ‘on and near very rotten
Shasta r log, Mt. Shasta, Calif. June 1954’ (Shasta r is the vernacular name for
A. magnica var. shastensis Lemmon). Besides being collected at the right time
and place, the morphology also ts our unnamed species, except for the color
of the lamellae. We never found olivaceous tinges in the (young) lamellae of

Pholiota olivaceophylla & P. nubigena (U.S.A.) ... 519
our specimens (P  2). Subsequently, the microscopic features of the type of
Ph. olivaceophylla were examined and the ITS sequences of the type and recent
collections were compared. Here, based on a wide sampling from dierent
locations within California, we present a thorough description of the species
with a photograph, and we place the ITS sequences in the context of the whole
genus to evaluate the taxonomic position of the species.
Pholiota olivaceophylla is considered a snowbank fungus as described by
Cooke (1944, 1955). Snowbank fungi depend on the moisture provided by the
melting snow for the development of their basidiocarps, and many are able
to fruit under the snow. Pholiota olivaceophylla starts fruiting in this way, but
continues fruiting aer snow melt. e fungus long known as Nivatogastrium
nubigenum is another example of this ecological group. e snowbank fruiting
habit seems to be restricted to the western North American mountains and has
not been encountered in Europe. Cripps (2009) gave an overview of the more
common snowbank species; with the description of Baeospora occidentalis
L.J. Hutchison & Kropp from Utah (Hutchison et al. 2012), the number of
known snowbank fungi has already increased.
Materials & methods
M—Standard methods for describing basidiocarps were applied, using the
terminology of Vellinga & Noordeloos (1999). Color annotations in the macroscopical
descriptions follow Kornerup & Wanscher (1967). Microscopical observations were
made from dried material rehydrated in 10% ammonia. e notation [81, 4, 3] indicates
that measurements were made on 81 spores in four samples in three collections; spores
were observed and measured from deposits on the stipe apex, and at least 20 spores
were measured per collection in side view; also for a few collections, at least 20 spores
per collection were measured in frontal view. e following abbreviations are used:
L = number of lamellae, l = number of lamellulae between two lamellae, avl = average
length, avw = average width, Q = quotient of length and width, and avQ = average
quotient. e genus name Pholiota is abbreviated as Ph. Collections are in UC, except
the type collection (in MICH). Herbarium abbreviations are according to iers (2015,
continuously updated). [For full collection information (including Genbank accession
numbers) see http://mycotaxon.com/vol/130/Siegel_Table1.pdf ]
DNA   —Collections for this study were made specically
during the Yosemite National Park fungus survey, and during the National Forest
Service surveys in the southern Cascade Range in California. We extracted DNA using a
modied Sigma Extract-N-Amp kit (Sigma Aldrich, St. Louis, MO) for dried mushrooms
and WhatmanTM FTATM Plant cards (Whatman Ltd) for dried tissue embedded in the
cards following manufacturer’s instructions. e nrITS region was amplied with the
ITS1F/ITS4 primer set using an MJ PTC-100™ thermocycler (Applied Biosystems, Foster
City, CA, USA) under conditions previously described (Gardes & Bruns 1993). PCR

520 ... Siegel, Nguyen, & Vellinga
products were cleaned using 0.5 µL of ExoSAP IT (USB Corp, Cleveland, OH, USA) per
reaction and cycled at 37°C for 45 min, followed by 80°C for 15 min. Sequencing was
performed using Big Dye chemistry and an ABI PRISM 3700 Genetic Analyzer (both
from Applied Biosystems, Foster City, CA, USA). Sequences were edited and contigs
were assembled using Sequencher 4.7 (Gene Codes Corporation, Ann Arbor, MI, USA),
and deposited in GenBank.
A   —e nrITS sequences newly produced for this
paper, plus all nrITS1-5.8S-ITS2 sequences of Pholiota, Flammula, and Nivatogastrium
species and their environmental counterparts from GenBank (as of October 2013), were
aligned with the program MAFFT version 7 (Katoh et al. 2002), and visually optimized.
Two sequences in GenBank, GU234152 and GU234164, were excluded as they show
92% BLAST similarity with a Conocybe teneroides collection (JF08598), and are not
close to Pholiota. e aligned sequence database was analyzed by maximum likelihood
method (ML) using the on-line program RAxML version 7.7.1 (Stamatakis et al. 2008);
100 rapid ML bootstraps were performed, and bootstrap values are included in the
ML tree of P  1. Pholiota lignicola [≡ Kuehneromyces lignicola (Peck) Redhead] and
Flammula sp. (coll. UC1861000) were chosen as outgroup taxa.
Results
e ITS alignment consists of 131 sequences (25 newly produced and 22
from California collections) and is 801 base pairs long. e resulting maximum
likelihood tree shows that Pholiota olivaceophylla is well supported (100%)
(P  1; see http://mycotaxon.com/vol/130/Siegel_Plate1.pdf for a larger
online version). Its closest relatives in our analyses are a collection from
Scandinavia labeled Ph. “spumosa” and the isotype of Ph. ferrugineolutescens
A.H. Sm. & Hesler from northern coastal California. Pholiota olivaceophylla
belongs to a clade that corresponds with the morphologically delineated
subg. Flammuloides to which other common Californian taxa, such as Ph.
velaglutinosa A.H. Sm. & Hesler, Ph. highlandensis (Peck) Quadr. & Lunghini,
and Ph. spumosa (Fr. : Fr.) Singer belong. Nivatogastrium nubigenum, which
forms secotioid basidiocarps, falls in the middle of subg. Flammuloides, close to
a collection of an agaricoid Pholiota from Yosemite National Park and Pholiota
sp. FJ717493 from Canada. Flammula is separate from Pholiota, as already
shown by Gulden et al. (2005), and Matheny et al. (2015) in their work on
various brown-spored groups, and in more wide-ranging works on Agaricales
as a whole (e.g., Matheny et al. 2007, Moncalvo et al. 2002). Subgenera Pholiota
and Flammuloides are clearly separate as well (P  1).
Discussion
e coverage of the genus Pholiota in terms of ITS sequences is far from
complete; some groups are well represented, but as a whole there is obviously
much work to be done at all taxonomic levels. e goal of our phylogenetic

Pholiota olivaceophylla & P. nubigena (U.S.A.) ... 521
0.04
JF961364 Pholiota filamentosa China
HG007979 Pholiota mixta PRM909924 EUR
FJ464595 Pholiota adiposa China
HQ222029 Pholiota virescentifolia holotype TENN020591 TN
KC122886 Pholiota spumosa UC1999286 CA
HG007986 Pholiota lubrica PRM899117 EUR
HQ604745 “Galerina” sp. UBC F19719 BC
KC122896 Pholiota terrestris UC1859859 CA
JF908590 Pholiota jahnii MCVE16840 EUR
DQ494679 Nivatogastrium nubigenum WTU CA
HG007978 Pholiota mixta PRM897292 EUR
FJ213506 environmental sample Korea
HQ832448 Pholiota aff. astragalina TENN TN
HQ604756 Pholiota terrestris UBC F19759 BC
JF908586 Pholiota astragalina MCVE14531 EUR
HQ222028 Pholiota tennesseensis holotype TENN018848 TN
FJ596860 Pholiota squarrosoides TENN61692 TN
KC122892 Pholiota cf. brunnescens UC1999269 CA
JF961360 Pholiota abietis China
JN021069 Pholiota cf. spumosa TRTC156869 Ont
KC122893 Flammula sp. UC1860901 CA
KC122879 Pholiota spumosa UC1998527 CA
JQ283961 Pholiota squarrosoides China
KC122882 Pholiota olivaceophylla UC1999268 CA
AY251300 Pholiota adiposa Korea
HG007985 Pholiota chocenensis holotype PRM895066 EUR
AF345654 Pholiota spumosa Korea
HM439573 Fungal sp. China
KC122877 Pholiota velaglutinosa UC1859567 CA
EF619735 environmental sample NC
HG007982 Pholiota spumosa PRM885615 EUR
KF878377 Pholiota mixta UC1999441 AK
KC122888 Pholiota olivaceophylla UC1999285 CA
KC122876 Pholiota lenta gr. UC1999282 CA
FJ467351 Pholiota adiposa China
KC122885 Pholiota olivaceophylla UC1999272 CA
AY618246 Pholiota spumosa EUR
KF878376 Pholiota highlandensis UC1999437 CA
JQ283958 Pholiota adiposa China
JF908581 Pholiota gummosa MCVE6610 EUR
HG007983 Pholiota spumosa PRM897683 EUR
HQ222017 Pholiota abieticola holotype TENN001400 NC
JQ283955 Pholiota adiposa China
JF908584 Pholiota cerifera MCVE12065 EUR
JF961363 Pholiota sp. China
JF961351 Pholiota adirondackensis China
JQ283956 Pholiota adiposa China
KC122895 Pholiota olivaceophylla UC1998643 CA
AY251304 Pholiota nameko Korea
JF908578 Pholiota lubrica MCVE4586 EUR
AY251301 Pholiota carbonaria Korea
JF908575 Pholiota conissans MCVE395 EUR
JF961353 Pholiota lubrica China
KF878378 Pholiota sp. UC1999439 AK
AM981221 environmental sample EUR
HG007981 Pholiota spumosa PRM897147 EUR
AY251303 Pholiota squarrosa-adiposa Korea
HQ222024 Pholiota caespitosa holotype TENN015908 TN
AM902027 environmental sample EUR
JF961356 Pholiota alabamensis China
FJ213522 environmental sample Korea
KF878380 Pholiota cf. decorata UC1999442 AK
JF908591 Pholiota squarrosoides MCVE17140 EUR
AY805621 Pholiota spumosa EUR
HQ222027 Pholiota olivaceodisca holotype TENN017778 TN
JQ283954 Pholiota adiposa China
JF719544 Pholiota adiposa Korea
JF908585 Pholiota scamba MCVE13482 EUR
AB470888 Pholiota adiposa China
HQ222025 Pholiota castanea type TENN020269 TN
KC122890 Pholiota spumosa UC1861020 CA
KC122883 Pholiota olivaceophylla UC1999281 CA
FJ755222 Pholiota adiposa China
JF908580 Pholiota gummosa MCVE6555 EUR
JF961358 Pholiota squarrosa-adiposa China
KC122887 Pholiota terrestris UC1860187 CA
GU934596 Pholiota carbonaria EUR
HG007984 Pholiota lubrica PRM857179 EUR
FJ596877 Pholiota squarrosoides TENN61728 TN
FJ596862 Pholiota sp. TENN61700 TN
FJ717493 Pholiota sp. BC
JF961349 Pholiota aurivelloides China
FJ596859 Pholiota squarrosoides TENN61692 TN
AB301612 Pholiota lubrica BRC 32453 EUR
KC122878 Pholiota olivaceophylla UC1999284 CA
AM930992 Pholiota sp. EUR
AY251306 Pholiota lucifera Korea
HG007980 Pholiota spumosa PRM901623 EUR
KC122880 Flammula sp. UC1861000 CA
AY281022 Pholiota lenta H EUR
HG007976 Pholiota highlandensis PRM888152 EUR
KF878379 Pholiota sp. UC1999438 NC
JQ283960 Pholiota adiposa China
HG007987 Pholiota lubrica PRM915546 EUR
KC122894 Pholiota olivaceophylla UC1998508 CA
KF878381 Pholiota olivaceophylla holotype MICH290502 CA
AY781268 Pholiota spumosa EUR
EU715686 Pholiota mixta Mex
HQ222026 Pholiota ferrugineolutescens isotype TENN028897 CA
JQ411813 Pholiota sp. China
JF961357 Pholiota limonella China
KC122881 Pholiota sp. UC1999274 CA
KC176331 environmental sample MI
KC122889 Pholiota olivaceophylla UC1999283 CA
FJ810180 Pholiota adiposa China
KC122884 Pholiota spumosa UC1999270 CA
FJ596876 Pholiota squarrosoides TENN61728 TN
JF908587 Pholiota pinicola MCVE16607 EUR
HQ222016 Pholiota burkei holotype TENN028812 AL
HG007977 Pholiota brunnescens E55717 EUR
JF908582 Pholiota lenta MCVE7100 EUR
JF908577 Pholiota spumosa MCVE3533 EUR
JN021068 Pholiota cf. spumosa TRTC156870 Ont
FJ810174 Pholiota nameko China
FR686575 Pholiota squarrosa China
HQ436122 Pholiota adiposa China
EU685975 environmental sample Peru
JF908588 “Pholiota” (Kuehneromyces) lignicola MCVE16608 EUR
HQ832449 Pholiota multicingulata PDD97861 NZ
KC122891 Pholiota cf. brunnescens UC1998624 CA
JF440578 Pholiota highlandensis EUR
JF908576 Pholiota flavida MCVE618 EUR
HG007974 Pholiota highlandensis PRM887239 EUR
HG007975 Pholiota highlandensis PRM895180 EUR
JF908583 Pholiota chocenensis MCVE11237 EUR
JN021067 Pholiota cf. spumosa TRTC156829 Ont
EU652950 Pholiota adiposa China
HQ533029 Pholiota multicingulata PDD95841 NZ
JN230706 Pholiota squarrosa China
JQ283957 Pholiota adiposa China
HG007988 Pholiota gallica holotype MPU EUR
100
71
100 91
71
73
98
100
98
82
83
99
95
99
63
100
100
100
83
100
83
70
100
71
100
86
98
85
99
70
100
90
97
92
69
100
91
100
85
100
100
100
85
94
98
96
89
99
99
98
Flammula
subg. Flammuloides
subg. Pholiota
P . ITS maximum likelihood tree of the genus Pholiota. Numbers on branches are ML
bootstrap values >69. Each terminal leaf is annotated as: GenBank accession; Taxon name;
Herbarium accession; Location. Location abbreviations: AK = Alaska, AL = Alabama, BC = British
Columbia (Canada), CA = California, EUR = Europe, Mex = Mexico, MI = Michigan,
NC = North Carolina, NZ = New Zealand, Ont = Ontario (Canada), TN = Tennessee. Newly
produced sequences are in bold.

522 ... Siegel, Nguyen, & Vellinga
analysis was not to deliver a thorough hypothesis on the evolution and
phylogenetic relationships of Pholiota taxa, but to show the grouping and
position of Ph. olivaceophylla and Ph. nubigena in general terms. As is clear
from P 1, species concepts are in need of reconsideration, as identical
sequences have been produced from collections that had been identied as
dierent species (e.g., in the Ph. adiposa clade), and the same name had been
applied to collections that belong to dierent clades (e.g., Ph. spumosa).
Sequencing of type collections, as started by Matheny and co-workers (in
TENN), should be expanded to all species described by Smith & Hesler (1968),
and neotypes and epitypes should be selected and presented with their sequence
data. Holec et al. (2014) also suggested increased sampling and sequencing
eorts to better understand the diversity and variability of the species.
Striking is that Pholiota castanea A.H. Sm. & Hesler (ITS GenBank
HQ222025 from the type collection), described as the only other species in
stirps Olivaceophyllae, from the Great Smoky Mountains National Park, is
not closely related to Ph. olivaceophylla (P  1), but is close to the recently
described European Ph. chocenensis Holec & M. Kolařík. Pholiota castanea and
Ph. olivaceophylla stand out among the species in subg. Flammuloides because
of their non-gelatinized subhymenium (Smith & Hesler 1968).
Based on an analysis of a 6-locus database of the Agaricales as a whole,
the secotioid N. nubigenum is a sister taxon to Pholiota squarrosa (Vahl : Fr.)
P. Kumm., the only agaricoid Pholiota species included in that analysis (Matheny
et al. 2007); it is a sister taxon to Pholiota multicingulata E. Horak in another
study of the Agaricales based on a 4-locus database (Matheny et al. 2015). In
the present ITS analysis, Ph. nubigena (as Nivatogastrium nubigenum in P
1) clearly nests within Pholiota subg. Flammuloides. Redhead (2014) proposed
the new combination of this species in Pholiota.
Taxonomy
Pholiota olivaceophylla A.H. Sm. & Hesler, N. Am. Species Pholiota: 236. 1968.
P –
P (30–)40–80(–100) mm, convex to broadly convex, becoming
applanate, occasionally wavy or lobed in age; margin inrolled when young,
becoming even, undulating in age, oen with veil remnants when young; surface
smooth, viscid when wet, becoming tacky, oen with debris stuck to it, shiny
when dry, creamy-orange, pale orange-bu to pale orange-tan when young,
becoming creamy-bu to tan, oen with darker orange-tan streaks or patches;
slime pale orange. L, L = about 50–60, l = 1–3, close to subdistant,
adnate with decurrent tooth, 7–10 mm wide, pale tan to bu (5B3–5C4) when
young, becoming tan, light brown to pale olive-brown, with even concolorous

Pholiota olivaceophylla & P. nubigena (U.S.A.) ... 523
P . Pholiota olivaceophylla (UC1999285). Photo by Noah Siegel
edges. S 50–90 × 10–18 mm, equal or enlarged at base, whitish when
young, covered with pale orange-bu slimy veil except for apex, becoming o-
white to dingy tan with pale orange streaks, dry and white above veil, becoming
dingy tan in age, at base covered with fuzzy white mycelium that binds to
organic matter, stued when young, becoming hollow in age. P  a
mucilaginous cortina, breaking up and leaving remnants around pileus margin
and a faint very pale orange ring that becomes brown with spores. C
white to pale cream in pileus, watery-white to pale tan in stipe, becoming tan to
pale brown. O musty, herbaceous. T   mild. C : 5%
KOH on pileus pale yellowish orange, on upper stipe orange, little reaction on
lower stipe, on pileus context bright orange, becoming orange-brown, on stipe
context orangish. S  color medium brown.
B in side view [200, 10, 10] 5.9–8.3 × 3.5–4.4 µm, avl × avw
= 6.4–7.3 × 3.9–4.1 µm, Q = 1.45–1.95, ellipsoid to oblong, some slightly
phaseoliform, in frontal view [40, 2, 2] 6.0–7.6 × 3.4–4.4 µm, avl × avw = 6.4–6.8
× 4.0–4.2 µm, Q = 1.4–1.9, avQ = 1.55–1.8, relatively thin-walled; germ pore
and hilar appendage inconspicuous. B –29 × 5–8 µm, 4-spored, with
basal clamp connection. L  sterile. C –65 × 8–15
µm, with 4–6 µm wide neck, lageniform, utriform, or clavate, a few similar in
shape and size to pleurocystidia, variously incrusted, with coarse material or

524 ... Siegel, Nguyen, & Vellinga
P . Pholiota olivaceophylla. a. Cheilocystidia; b. pleurocystidia (both from UC UC1999268).
Scale bars = 10 µm. Drawing by ECV.
with some small pieces, in some collections with yellow contents in ammonia.
P 48–91 × 10–17.5 µm, with 4–10 µm wide neck, lageniform,
very abundant, protruding from hymenium, variable in size and ornamentation,
yellow in ammonia in some collections, with or without an apical covering
of crystalline material, or with amorphous matter inside, or without any
inclusions, with slightly thickened walls in lower part of neck. H
 not pigmented. S not gelatinized. P an ixocutis
of cylindrical non-colored hyphae, 2–5 µm wide; subpellis a cutis of cylindrical
to slightly inated hyphae, 5–10 µm wide with brown walls. S a
cutis of cylindrical colourless hyphae, 4–11 µm wide, without caulocystidia.
C  present in all tissues.
S : USA: C, Siskiyou Co., Modoc National Forest,
north slope of Black Mountain, near junction of Forest Road 44N33 & 44N12, in Abies
magnica & A. concolor forest, 29 May 2012, E.C. Vellinga (UC 1999279); in A. magnica
& A. concolor forest on small branches and thick du near melting snow, 29 May 2012,
N. Siegel (UC 1999281; GenBank KC122883); in A. magnica & A. concolor forest on
conifer wood, 29 May 2012, E.C. Vellinga (UC 1999285; GenBank KC122888); in A.
magnica & A. concolor forest on conifer wood & twigs, 29 May 2012, E.C. Vellinga (UC
1999276); in A. magnica & A. concolor forest, 29 May 2012, N. Siegel (UC 1999280);

Pholiota olivaceophylla & P. nubigena (U.S.A.) ... 525
P . Pholiota olivaceophylla. a. Spores; b. basidia; c. cheilocystidia; d. pleurocystidia
(all from UC1999272). Scale bars = 10 µm. Drawing by ECV.
Mount Shasta, on and under rotten A. magnica log, 1 June 1954, W.B. Cooke (MICH
290502, holotype; GenBank KF878381); Mount Shasta, near Clear Creek Trailhead, in
A. magnica forest, 28 May 2012, E.C. Vellinga (UC 1999277); Trout Creek area, in A.
magnica and A. concolor forest, on conifer wood and twigs, 28 May 2012, E.C. Vellinga
(UC 1999283; GenBank KC122889); Six Shooter Butte, in A. magnica forest, on conifer
wood, 27 May 2012, E.C. Vellinga (UC 1999278); Shasta National Forest, Trout Butte
area, 28 May 2012, N. Siegel (UC 1999284; GenBank KC122878); Tuolumne Co.,
Yosemite National Park, Crane Flat, north of gas station, in mixed coniferous forest, on
conifer wood, 4 June 2010, N. Siegel (UC 1999268; GenBank KC122882); Tamarack Flat
Road near Tioga Road, 37.7966°N 119.8655°W, in A. magnica forest, on conifer wood,
5 June 2010, D. Viess (UC 1999272; GenBank KC122885); Mariposa Co., Yosemite
National Park, Glacier Point Road, 37.67333°N 119.6523°W, in mixed coniferous forest,
30 May 2010, M. Schubert (UC 1998508; GenBank KC122894); Glacier Point Road,
Summit Meadow, 37.6650°N 119.6997°W, in P. jereyi, P. lambertiana, & Abies forest, on
litter, 30 May 2012, N.H. Nguyen (UC 1998643; GenBank KC122895).
H  —Solitary, scattered, or in small groups and clusters
on small buried branches, woody debris, thick du, or well rotted logs, in Abies
concolor (Gordon) Lindl. ex Hildebr. and A. magnica forests at 1700–2200 m
asl, fruiting near melting snowbanks or areas with snow cover, occasionally
fruiting under snow, May–June. Widespread in the Sierra Nevada and southern
Cascades in California.

526 ... Siegel, Nguyen, & Vellinga
P . Pholiota olivaceophylla. a. Spores; b. cheilocystidia; c. pleurocystidia
(all from UC1998643). Scale bars = 10 µm. Drawing by ECV.
e type collection was in good condition, and the dried specimens of recent
collections look very similar. e following characters were noted for the type
collection (P  6):
S [20, 1] 6.4–7.8 × 3.4–4.7 µm in side-view, avl × avw = 7.0 × 3.9 µm,
Q = 1.67–1.89, avQ = 1.8, elongate, slightly phaseoliform, pale brown, with
inconspicuous germ pore and hilar appendage. B 20–23 × 5.0–6.5 µm,
4-spored, with basal clamp connection. C present, dicult
to observe, lageniform. P abundant, 63-80 × 11–16 µm,
lageniform, with 15–35 µm long cylindrical, rarely ventricose neck, oen
slightly pinched in near the wider part, with or without yellowish contents,
slightly thick-walled.
A  :
Flammula sp.: USA: C, Mariposa Co., Yosemite National Park, White Wolf
campground, 37.869383°N -119.646585°W, in A. concolor and P. contorta forest, on
conifer wood, 18 Aug. 2010, P.G. Werner (UC 1860901; Genbank KC122893); Yosemite
National Park, Glacier Point Road, 37.7065°N -119.5890°W, in Pinus contorta forest, 29
Oct. 2011, L. Rosenthal (UC 1861000; Genbank KC122880).
Pholiota cf. brunnescens: USA: C, Mariposa Co., Yosemite National Park,
Mariposa Grove loop trail, 37.50568°N -119.60847°W, in mixed coniferous forest,

Pholiota olivaceophylla & P. nubigena (U.S.A.) ... 527
P . Pholiota olivaceophylla. a. Spores; b. basidia; c. cheilocystidium; d. pleurocystidia
(all from holotype). Scale bars = 10 µm. Drawing by ECV.
29 May 2010, N.H. Nguyen (UC 1998624; Genbank KC122891); Tuolumne Co.,
Yosemite National Park, Tamarack Flat Road, 37.7966°N -119.8655°W, in P. ponderosa,
Pseudotsuga menziesii & Calocedrus decurrens forest, N. Siegel, 5 June 2010 (UC
1999269; Genbank KC122892).
Pholiota cf. decorata: USA: A, Anchorage Co., Girdwood, Iditarod Trail, in
forest with Picea sitchensis and Tsuga, 31 Aug. 2012, E.C. Vellinga 5567b (UC 1999442;
Genbank KF878380).
Pholiota highlandensis: USA: C, Mendocino Co., Mendocino, o Wheeler
Street, on burnt ground under Pinus, 2 Jan. 2013, N. Siegel (UC 1999437; Genbank
KF878376).
Pholiota lenta s.l.: USA: C, Yuba Co., Bullard’s Bar Recreation Area,
Hornswaggle Campground, 39.4146°N -121.1205°W, mixed conifer forest, on
coniferous wood, 10 Dec. 2011, E.C. Vellinga (UC 1999282; Genbank KC122876).
Pholiota mixta: USA: A, Kenai Peninsula, Hope, along Palmer Creek Road, 3
Sept. 2012, E.C. Vellinga 5580b (UC 1999441; Genbank KF878377).
Pholiota sp.: USA: A, Kenai Peninsula, Hope, along Palmer Creek Road, 3 Sept.
2012, E.C. Vellinga 5578b (UC 1999439; Genbank KF878378); C, Yosemite
National Park, Highway 120, in A. magnica forest, on conifer wood, 30 Sept. 2011,
D. Rust (UC 1999274; Genbank KC122881); N C, Mount Mitchell State
Park, on conifer wood, 22 Sept. 2012, D. Viess (UC UC 1999438; Genbank KF878379).

528 ... Siegel, Nguyen, & Vellinga
Pholiota spumosa: USA: C, Alameda Co., Berkeley, along Euclid Avenue,
on Pinus bark chips in garden, 18 March 2012, E.C. Vellinga (UC 1999286; Genbank
KC122886); Mariposa Co., Yosemite National Park, Wawona Meadow Loop Trail,
37.523056°N -119.636111°W, on buried conifer wood, 29 May 2010, E.P. Blanchard
(UC UC 1998527; Genbank KC122879).
Pholiota terrestris: USA: C, Marin Co., Point Reyes National Seashore,
Olema Trail, 37.9917°N -122.7580°W, in Ps. menziesii & hardwood forest, 9 Dec.
2006, K. Takeoka (UC 1859859; Genbank KC122896); Point Reyes National Seashore,
Bayview Trail, 38.0608°N -122.8564°W, in P. m u r i c a t a forest, 29 Dec. 2007, Aletheap
(UC 1860187; Genbank KC122887).
Pholiota velaglutinosa: USA: C, Marin Co., Point Reyes National Seashore,
Mount Vision, 38.1016°N -122.8947°W, in P. muricata forest, 10 Dec. 2005, Murray (UC
1859567; Genbank KC122877).
C—e data noted from the type collection concur with those given
by Smith & Hesler (1968) and t well the modern data for the collections from
California’s mountain ranges. An image of A.H. Smith’s original notes can be
found in Mycoportal (http://mycoportal.org).
Pholiota olivaceophylla commonly fruits in May and June during and just
aer snowmelt in the Abies forests of the Sierra Nevada and Cascade ranges.
It can easily be distinguished from the other common species in Pholiota
subg. Flammuloides fruiting at the same time in the mountains. For example,
Ph. highlandensis and Ph. brunnescens A.H. Sm. & Hesler grow on recent burns,
have smaller basidiocarps and deeper brown, thick-walled spores. Species in
the Ph. spumosa complex enjoy bright yellow colors in the basidiocarps, and
have brown thick-walled spores with a distinct germ pore, which are similar in
size to those of Ph. olivaceophylla.
e European species Ph. elegans Jacobsson comes close in overall
appearance, but diers in habitat (mainly in virgin, oen deciduous, forests and
fruiting in autumn), and slightly smaller, distinctly phaseoliform-amygdaloid
spores, 5.0–6.7(–7.0) µm long (Holec 2001).
e North American species in Pholiota subg. Flammuloides are in serious
need of revision, and interpretation of many species described by Smith and
Hesler (1968) is challenging. However, some species yield to interpretation and
appear to be close to Ph. olivaceophylla in their pale colors, but dier in critical
characters: the pale species Ph. avopallida A.H. Sm. & Hesler has spores 5–6
µm long, and Ph. agglutinata A.H. Sm. & Hesler has a white veil, and was found
in late summer. ere are, as far as we know, no other spring-fruiting mountain-
dwelling species described. McClenaghan (1991) in her overview of northern
California species gave a relatively short description of Ph. olivaceophylla based
on one collection (which we have not studied), and stressed the olivaceous
lamellae that turn to dark brown with age, characters we did not observe in the

Pholiota olivaceophylla & P. nubigena (U.S.A.) ... 529
P . Pholiota nubigena. a. Spores; b. basidia; c. pleurocystidia (all from UC1998744).
Scale bars = 10 µm (note dierent scale for c than in the other gs.). Drawing by ECV.
many specimens we collected. Other characters (including the location and the
time of collecting) do t with our concept of Ph. olivaceophylla.
e pleurocystidia of Ph. olivaceophylla are highly variable in size, in
contents, and in ornamentation among collections (P 3–6); how this is
inuenced by age of the basidiocarps and environmental variables is unknown.
ere is no overlap in pleurocystidium size among the collections with the
shortest and those with the longest pleurocystidia. Constant are the relatively
thin walls and relatively pale brown color of the spores under the microscope,
and inconspicuous germ pore and hilar appendage. Spore color is a much
better character at species level than pleurocystidium shape and size, but it is a
qualitative character, and thus harder to assess.
Pholiota nubigena (Harkn.) Redhead, Index Fungorum 148: 1. 2014. P 
≡ Secotium nubigenum Harkn., Bull. California Acad. Sci. 1(4): 257. 1886.
≡ Nivatogastrium nubigenum (Harkn.) Singer & A.H. Sm., Brittonia 11: 224. 1959.
C—Pholiota nubigena shares both the hallmarks for subg.
Flammuloides and the habitat with Ph. olivaceophylla. e pleurocystidia are

530 ... Siegel, Nguyen, & Vellinga
numerous and lageniform with a very long neck without yellow inclusions
(chrysocystidia are absent), the spores are larger than those of Ph. olivaceophylla
(based on our observations on collection UC 1998744 [25, 1, 1] 7.8–10.8 ×
4.9–6.2 µm in side-view), with a medium brown, medium thick wall, a distinct
hilar appendage, and a hardly visible germ pore (P 7a).
e spores are asymmetrical in side view, and the basidia have sterigmata
typical for ballistospore dispersal (P 7b). Pholiota nubigena grows, like
Ph. olivaceophylla, on conifer wood, and is widespread in the western North
American mountains, with records from the southern Sierras northwards into
Idaho and the Rocky Mountains in Montana (http://mycoportal.org retrieved
12 February 2015).
S : USA: C, Mariposa Co., Yosemite NP, Glacier Point
Road, 37.6687°N 119.6113°W, M.G. Wood, 30 May 2010, M.G. Wood (UC 1998744).
Phylogenetically Ph. nubigena falls in the middle of subg. Flammuloides, and a
relationship with Pholiota — which has been proposed in the past, both prior to
(e.g. Singer & Smith 1959, Smith & Hesler 1968) and subsequent to molecular
analyses (Matheny et al. 2007, 2015) — is again conrmed here.
Acknowledgments
Matthew Foltz and Patricia Rogers at MICH were so kind as to arrange the loan
of the type of Ph. olivaceophylla. Alex Grote and Sara Zlotnik helped produce some of
the DNA sequences. is work was partially funded by the Shasta-Trinity and Lassen
National Forest as part of Northwest Forest Plan strategic surveys. Comments by the
reviewers, Drs Scott A. Redhead and Joe F. Ammirati, and by the nomenclature editor
Dr. Shaun Pennycook, on earlier versions are highly appreciated.
Literature cited
Arora D. 1986. Mushrooms demystied. 2nd ed. Berkeley: Ten Speed Press. 959 p.
Cooke WB. 1944. Notes on the ecology of the fungi of Mount Shasta. e American Midland
Naturalist 31: 237–249. http://dx.doi.org/10.2307/2421394
Cooke WB. 1955. Subalpine fungi and snowbanks. Ecology 36: 124–130.
http://dx.doi.org/10.2307/1931437
Cripps C. 2009. Snowbank fungi revisited. Fungi 2(1): 47–53.
Donk MA. 1962. e generic names proposed for Agaricaceae. Beih. Nova Hedwigia 5: 1–320.
Gardes M, Bruns TD. 1993. ITS primers with enhanced specicity for basidiomycetes –
application to the identication of mycorrhizae and rusts. Molecular Ecology 2: 113–118.
http://dx.doi.org/10.1111/j.1365-294X.1993.tb00005.x
Gulden G, Stensrud K, Shalchian-Tabrizi K, Kauserud H. 2005. Galerina Earle: a polyphyletic
genus in the consortium of dark-spored agarics. Mycologia 97: 823–837.
Holec J. 2001. e genus Pholiota in central and western Europe. Libri botanici 20: 1–220.
Holec J, Kolařík M. 2014. Pholiota gallica nom. nov., based on Pholiota lubrica var. obscura.
Mycotaxon 127: 161–171. http://dx.doi.org/10.5248/127.161

Pholiota olivaceophylla & P. nubigena (U.S.A.) ... 531
Holec J, Kolařík M, Bizio E. 2014. Pholiota chocenensis—a new European species of
section Spumosae (Basidiomycota, Strophariaceae). Mycological Progress 13: 399–406.
http://dx.doi.org/10.1007/s11557-013-0926-2
Hutchison LJ, Kropp BR, Hausner G. 2012. Baeospora occidentalis, a new snowbank agaric from
western North America. Mycoscience 53: 139–143.
http://dx.doi.org/10.1007/s10267-011-0142-3
Jacobsson S. 1990. Pholiota in northern Europe. Windahlia. 19: 1–86
Jacobsson S. 1997. New observations on Pholiota. Windahlia 22: 23–28.
Jacobsson S. 2008. Pholiota P. Kumm. 837–844, in: H Knudsen, J Vesterholt (eds). Funga nordica.
Agaricoid, boletoid and cyphelloid genera. Copenhagen: Nordsvamp.
Jacobsson S. 2012. Flammula (Fr.) P. Kumm. Pholiota P. Kumm. 936–937, 955–964, in: H Knudsen,
J Vesterholt (eds). Funga nordica. Agaricoid, boletoid, clavarioid, cyphelloid and gastroid
genera. Copenhagen: Nordsvamp.
Jacobsson S, Larsson E. 2007. Hemistropharia, a new genus in Agaricales. Mycotaxon 102: 235–240.
Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple
sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059–3066.
http://dx.doi.org/10.1093/nar/gkf436
Kornerup A, Wanscher JH. 1967. Methuen handbook of colour. 2nd ed. London: Methuen & Co
Ltd. 243 p.
Matheny PB, Moreau P-A, Vizzini A, Harrower E, De Haan A, Contu M, Curti M. 2015.
Crassisporium and Romagnesiella: two new genera of dark-spored Agaricales. Systematics and
Biodiversity 13: 28–41. http://dx.doi.org/10.1080/14772000.2014.967823
Matheny PB, Curtis JM, Hofstetter V, Aime MC, Moncalvo J-M, Ge Z-W, Yang Z-L, Slot JC,
Ammirati JF, Baroni TJ, Bougher NL, Hughes KW, Lodge DJ, Kerrigan RW, Seidl MT, Aanen
DK, DeNitis M, Daniele GM, Desjardin DE, Kropp BR, Norvell LL, Parker A, Vellinga EC,
Vilgalys R, Hibbett DS. 2007 [“2006”]. Major clades of Agaricales: a multilocus phylogenetic
overview. Mycologia 98: 982–995. http://dx.doi.org/10.3852/mycologia.98.6.982
McClenaghan SC. 1991. A systematic study of the genus Pholiota in California. Master’s thesis,
Humboldt State University, Arcata, CA, USA. 160 p. [unpublished]
Moncalvo JM, Vilgalys R, Redhead SA, Johnson JE, James TY, Catherine Aime M, Hofstetter V,
Verduin SJ, Larsson E, Baroni TJ, Greg orn R, Jacobsson S, Clémençon H, Miller OK. 2002.
One hundred and seventeen clades of euagarics. Molecular Phylogenetics and Evolution 23:
357–400. http://dx.doi.org/10.1016/S1055-7903(02)00027-1
Noordeloos ME. 1999. Pholiota. 80–107, in: ME Noordeloos et al. (eds). Flora agaricina neerlandica
4. Rotterdam/Brookeld: A.A. Balkema.
Noordeloos ME. 2011. Strophariaceae s.l. 1. Fungi Europaei 13. Alassio: Edizioni Candusso. 648 p.
Norvell LL, Redhead SA. 2000. Stropharia albivelata and its basionym Pholiota albivelata.
Mycotaxon 76: 315–320.
Redhead SA. 1984a. Additional Agaricales on wetland Monocotyledoneae in Canada. Canadian
Journal of Botany 62: 1844–1851. http://dx.doi.org/10.1139/b84-251
Redhead SA. 1984b. Mycological observations, 4–12: on Kuehneromyces, Stropharia, Marasmius,
Mycena, Geopetalum, Omphalopsis, Phaeomarasmius, Naucoria and Prunulus. Sydowia 37:
246–270.
Redhead SA. 2013. (2128) Proposal to conserve the name Flammula (Fr.) P. Kumm. (Fungi:
Agaricales) against Flammula (Webb ex Spach) Fourr. (Spermatophyta: Ranunculaceae).
Taxon 62: 401–402. http://dx.doi.org/10.12705/622.16
Redhead SA. 2014. Nomenclatural novelties. Index Fungorum no. 148: 1.

532 ... Siegel, Nguyen, & Vellinga
Singer R, Smith AH. 1959. Studies on secotiaceous fungi –V. Nivatogastrium gen. nov. Brittonia
11: 224–228.
Smith AH, Hesler LR. 1968. e North American species of Pholiota. New York: Hafner. 402 p.,
90 pl.
Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML web-
Servers. Systematic Biology 75: 758–771. http://dx.doi.org/10.1080/10635150802429642
iers B. 2015 (continuously updated). Index Herbariorum: A global directory of public herbaria
and associated sta. New York Botanical Garden’s Virtual Herbarium.
http://sweetgum.nybg.org/ih/
Vellinga EC, Noordeloos ME. 1999. Glossary. 6–12, in: ME Noordeloos et al. (eds). Flora agaricina
neerlandica 4. Rotterdam/Brookeld: A.A. Balkema.