Two new species of nivicolous Lamproderma (Myxomycetes) from the mountains of Europe and America

Abstract

As a result of the revision of European and American collections of genus Lamproderma two new nivicolous myxomycete species, Lamproderma argenteobrunneum and L. kowalskii, are described. The new species are characterized by the silvery-brown sporothecae, the areolate peridium and the ferruginous-brown spores in mass. They differ from one another mainly in spore size and ornamentation, the form of the capillitium and the stalk length and ratio of the stalk length to the total height of the sporocarp. The morphology of the new species was examined with light microscopy and scanning electron microscopy (SEM), and micrographs of relevant details are included. Lamproderma argenteobrunneum also was obtained in moist chamber culture, and the mature sporocarps displayed all features typical of field-collected samples. The known geographical distribution of L. argenteobrunneum includes the main ranges of the European alpine system (Alps, Carpathians, Pyrenees) as well as those of North America, while L. kowalskii has been recorded so far from several sites in California in the United States.

Full text

Two new species of nivicolous
Lamproderma
(Myxomycetes)
from the mountains of Europe and America
Anna Ronikier
1
Institute of Botany, Polish Academy of Sciences, Lubicz
46, 31-512 Krako´w, Poland
Carlos Lado
Real Jardı
´n Bota´nico, CSIC, Plaza de Murillo 2, 28014
Madrid, Spain
Marianne Meyer
Le Bayet, 73730 Rognaix, France
Diana Wrigley de Basanta
Real Jardı
´n Bota´nico, CSIC, Plaza de Murillo 2, 28014
Madrid, Spain
Abstract
:As a result of the revision of European and
American collections of genus
Lamproderma
two new
nivicolous myxomycete species,
Lamproderma argen-
teobrunneum
and
L. kowalskii
, are described. The new
species are characterized by the silvery-brown spor-
othecae, the areolate peridium and the ferruginous-
brown spores in mass. They differ from one another
mainly in spore size and ornamentation, the form of
the capillitium and the stalk length and ratio of the
stalk length to the total height of the sporocarp. The
morphology of the new species was examined with
light microscopy and scanning electron microscopy
(SEM), and micrographs of relevant details are
included.
Lamproderma argenteobrunneum
also was
obtained in moist chamber culture, and the mature
sporocarps displayed all features typical of field-
collected samples. The known geographical distribu-
tion of
L. argenteobrunneum
includes the main ranges
of the European alpine system (Alps, Carpathians,
Pyrenees) as well as those of North America, while
L.
kowalskii
has been recorded so far from several sites in
California in the United States.
Key words: Lamproderma fuscatum
, moist cham-
ber culture, Mycetozoa, Myxogastria, Protozoa,
SEM, species distribution, taxonomy
INTRODUCTION
The myxomycete genus
Lamproderma
Rostaf. was
described by Rostafin´ski (1873), who recognized nine
species (Rostafin´ski 1874). The genus is characterized
by globose, usually stipitate sporocarps, a persistent
and iridescent peridium, the presence of a columella,
the capillitium usually originating from the apex of
the columella and the dark brown to blackish spores
in mass. More than 135 y later the number of known
Lamproderma
species has increased considerably and
currently 44 species are recognized in the genus
(Lado 2008), about one-third of them described in
the past 20 y. More than half the known
Lamproderma
species belong to the well recognized ecological
group of nivicolous myxomycetes. Among them eight
were described or raised to species in the past decade,
and many have their type localities in the European
Alps (Bozonnet et al. 1991, 1995, 1997; Meyer et al.
1994; Poulain et al. 2002, 2003, 2005). In addition
studies of the type material of the older taxa (Moreno
et al. 2002, 2005; Poulain et al. 2003; Singer et al.
2003) have clarified the taxonomic situation of several
species. In the recent phylogenetic analysis of the
dark-spored myxomycetes it has been demonstrated
that
Lamproderma
is a paraphyletic genus and
suggested that the species with evanescent peridium
might represent a distinct group that should be
treated as a separate genus (Fiore-Donno et al. 2008).
During the study of the diversity of nivicolous
myxomycetes from the Pyrenees (Lado and Ronikier
2008, 2009) a collection belonging to genus
Lampro-
derma
was found, with a silvery-brown sporotheca, a
persistent and areolate peridium and ferruginous-
brown spores in mass, which were pale brown under
transmitted light. The same morphotype was found
independently in material from the Austrian and
French Alps, French Jura and the Polish Carpathians.
All these collections agreed in part with the descrip-
tion provided by Kowalski (1970) for species
L.
fuscatum
Meyl.
Lamproderma fuscatum
, according to the original
description (Meylan 1932), has a nonpersistent
peridium disappearing in small patches. This charac-
ter together with the funnel-shaped ends of the
capillitial threads was confirmed by an analysis and
new description of the lectotype (LAU) by Moreno et
al. (2002) and by observations made by M. Poulain
and M. Meyer (unpubl data). When these two
descriptions were compared with those provided by
Kowalski (1968, 1970, 1975) based on American
specimens, differences in the type of peridium
dehiscence and spore ornamentation were found.
Kowalski (1968, 1970) described the peridium of the
American collections as ‘‘thick, firm, persistent,
Submitted 7 Sep 2009; accepted for publication 3 Nov 2009.
1
Corresponding author. E-mail: a.ronikier@botany.pl
Mycologia,
102(3), 2010, pp. 718–728. DOI: 10.3852/09-223
#2010 by The Mycological Society of America, Lawrence, KS 66044-8897
718

splitting irregularly, but persisting as a cup at the base
of the sporangium’’ and the capillitium as ‘‘forming a
net with abundant sharp, pointed, free ends’’. In
addition Kowalski (1970) mentioned that he also
studied four of Meylan’s collections from Switzerland
and noted that in the European collections the spores
were spinulose while in USA material the spores were
minutely warted with the warts often slightly elongat-
ed. ‘‘This difference is constant; there is no overlap-
ping,’’ Kowalski said. ‘‘Although this discrepancy
probably shows some genetic divergence between
the two populations, I do not believe it is large
enough to warrant the separation of these popula-
tions into different taxa,’’ he said. Kowalski (1975)
also cited the differences in peridium characteristics
among the American collections with a persistent
peridium and the European collections with a
fugacious peridium that remains in small fragments.
The great differences in the descriptions of
L.
fuscatum
from Europe and America suggested that
different species were involved. The objective of this
paper was to provide a comprehensive revision of
both the European and the American specimens of
‘‘
L. fuscatum
’’ and establish their taxonomic position.
MATERIALS AND METHODS
We studied specimens collected from different localities in
the European mountains, deposited in the herbaria MA-
Fungi, KRAM, the private collection of Marianne Meyer
(coll. MM) or the private collection of Wolfgang Nowotny
(coll. Now). In addition we examined all collections
identified by Donald T. Kowalski (DTK) as ‘‘
Lamproderma
fuscatum
’’ deposited at UC (herbarium of the University of
California).
Observations and measurements of the morphological
characters were done under a stereoscopic microscope
Nikon SMZ 1500. The total height of the sporocarps as well
as the height and the width of the sporothecae were
measured. Whenever possible 10 sporocarps of each
collection were measured (212 sporocarps in total).
Observations and measurements of microscopic characters
were made on material mounted in Hoyer’s medium, under
a light microscope, Nikon Eclipse E-600. Permanent slides
of all examined collections are deposited in KRAM. Spore
measurements (50 per collection, 1600 in total) were made
under an oil immersion objective and include ornamenta-
tion. Values of spore size present in fewer than 1%of the
measurements are given in parentheses in the descriptions
provided below. The statistics were calculated with Statistica
6 software.
Critical point drying was used for scanning electron
microscopy (SEM) preparations, and specimens were
examined with a Hitachi S-3000N or Hitachi S-4700
scanning electron microscopes at 10–15 kV. SEM studies
of the collections were made at the Royal Botanic Garden of
Madrid and in the Laboratory of Field Emission Scanning
Electron Microscopy and Microanalysis, at the Institute of
Geological Sciences of the Jagiellonian University, Krako´ w.
A trial moist chamber culture was set up with pieces of the
substrate of a field collection of
Lamproderma
from the
Pyrenees (MA-Fungi 75785) without any sporocarps. Small
fragments of the substrate (plant stems) were placed on a
Whatman filter paper disk in a sterile, 9 cm diam plastic
Petri dish. The substrate was scattered with spores from a
mature sporocarp of the same collection. The material was
loosely covered with a second filter paper disk to simulate
conditions under melting snow. Distilled water was added to
thoroughly moisten both layers of filter paper and the
substrate, and excess water was poured off after 24 h. The
Petri dish was placed inside a plastic box in the center of a
laboratory refrigerator in the dark at 5 C. The culture was
maintained 3 mo (15-II-2007–21-V-2007). The culture was
examined at approximately weekly intervals during which
time it was exposed to light and an increase of temperature
for a maximum of 20 min.
RESULTS
More than 30 collections of ‘‘
Lamproderma fuscatum
’’
from Europe and America were studied, and it was
confirmed that the material described by Kowalski
(1970) in his monograph was not conspecific with the
L. fuscatum
described by Meylan (1932). The detailed
description provided by Kowalski (1968, 1970) fits the
characters of one morphotype found by us in many
European mountains. In addition in the American
material identified by Kowalski as ‘‘
L. fuscatum
’’ a second
morphotype was found with distinguishing characters in
spores, capillitium and columella. No species from genus
Lamproderma
has been described with a similar set of
characters, and therefore we conclude that the two
morphotypes represent two different new species.
Lamproderma argenteobrunneum A. Ronikier, Lado
& Mar. Mey., sp. nov. FIGS. 1A–C, 2
MycoBank 515370
Sporocarpia in gregibus dispersis, cum stipitibus brevibus,
vel paene sessilia, 0.78–2.24 mm alta. Sporotheca 0.62–
1.6 mm diam, globosa vel ovata. Peridium permanens,
argenteo-griseum, chalybaeo-brunneo-griseum, cum aureis
nitoribus (imprimis in parte inferiore sporothecae), relative
crassum. Stipes brevis, 0.04–0.64 mm, atro-griseus, lucens.
Hypothallus membranaceus, discoides, translucidus, auran-
tiaco-brunneus vel brunneo-ruber. Columella fere dimidiam
partem sporothecae attingens, anguste conica ad conica,
circa apicem se coartans (vel raro se dividens). Capillitium
constanter ferrugineo-brunneum, mediocriter densum vel
densum, in superiore parte columellae oriens, rigidum.
Sporae ferrugineo-brunneae in massa, subbrunneae luce
transmissa, globosae (8–)9–11(–12) mm diam, in superficie
non dense ornatae brevibus cristis quae spinis junctis
intermixtis cum solitariis spinis formantur. Plasmodium
ignotum. Species prope nivem liquefactam fructificans.
RONIKIER ET AL.: NIVICOLOUS
L
AMPRODERMA
SPECIES 719

Sporocarps in loose groups, shortly stipitate or
almost sessile (FIGS 1A, 2A), total height 0.78–
2.24 mm. Sporotheca subglobose to slightly ovoid,
0.62–1.6 mm diam, silvery-brown, sometimes with
golden reflections mainly at the bottom. Peridium
single, membranous, persistent, thick, splitting irreg-
ularly and often persisting as a cup at the base of the
sporotheca, brownish and usually with an areolate
FIG. 1. Characteristic features of the two new
Lamproderma
species. A–C.
Lamproderma argenteobrunneum
—HOLOTYPE
(Lado 6792). A. Sporocarps. B. Peridium (inner side) in light microscope. C. Spores in light microscope. D–F.
Lamproderma
kowalskii
—HOLOTYPE (DTK 6408). D. Sporocarps. E. Peridium (inner side) in light microscope. F. Spores in light
microscope. Bars: A, D 51 mm, B–C, E–F 510 mm.
720 MYCOLOGIA

pattern at lower part under transmitted light
(FIG. 1B). Stalk short, erect, 0.04–0.64 mm long, dark
brown, shining, occasionally absent. Hypothallus
membranous, discoid, translucent, orange-brown or
red-brown. Columella reaching about half the spor-
otheca height, conical to narrowly conical (FIG 2B).
Capillitium uniformly ferruginous-brown, dense, orig-
inating from the upper part of the columella, rigid,
primary branches with membranous expansions,
capillitial threads at peripheries with many pointed
free ends (FIG. 2C). Spores in mass ferruginous-
brown, pale brown by transmitted light, globose, (8–)
9–11(–12) mm diam, ornamented with loosely ar-
ranged, short, curved ridges and some isolated spines
between the ridges (FIGS 1C, 2D–F). Plasmodium
unknown.
HOLOTYPE. SPAIN. Le´ rida: Naut Ara´n, Salardu´,
Aiguamotx, La Muntanyeta, 42u379470N, 0u549480E,
2000 m, on pteridophyte, 29-VI-1994,
leg. C. Lado &
S. Santamarı
´a
, Lado 6792 (MA-Fungi 75785).
Isotypes
at KRAM (M-1292), and in the private collection of M.
Meyer (MM 30500).
Specimens examined
. AUSTRIA. Steiermark: Altaussee,
Loser, 1300 m, on branch of living shrub, 17-V-2002,
leg. W.
Nowotny
, Now 11693/2 (MM 28459); Now 11776. Altaussee,
Loser, 1500 m, on branch of living shrub, 30-V-1997,
leg. W.
Nowotny
, Now 8683/3. Altaussee, Loser, 1200–1300 m, on
branch of living shrub, 10-V-1998,
leg. W. Nowotny
, Now
9456; Now 9459. Altaussee, Loser, 1100–1150 m, on branch
of living shrub, 10-V-2008,
leg. W. Nowotny
, Now 14513.
Obero¨ sterreich: Ebensee, Feuerkogel, 1550 m, on dead
plant stems, 29-V-1993,
leg. W. Nowotny
, Now 5406/1. Bad
Ischl, Hoisnradalm, 850–950 m, on branch of living shrub,
FIG. 2. Microphotographs of
Lamproderma argenteobrunneum
from scanning electron microscope—HOLOTYPE (Lado
6792). A. Sporocarp. B. Columella and primary branches of the capillitium with membranous expansions. C. Peripheral part of
capillitium. D–F. Spores. Bars: A 5500 mm, B 5300 mm, C 5100 mm, D–F 510 mm.
RONIKIER ET AL.: NIVICOLOUS
L
AMPRODERMA
SPECIES 721

23-IV-2005,
leg. W. Nowotny
, Now 13171/1. Tirol: Scharnitz,
Karwendeltal, 1500–1600 m, on branch of living shrub, 14-V-
2002,
leg. W. Nowotny
, Now 11599/1. FRANCE. Ain: Grand
Colombier, 1400 m, on twig of deciduous tree, 2-V-1988,
leg.
J. Bozonnet
, No. JB O05023 (MM 8789). Grand Colombier,
on dry herbaceous plants, 5-V-1995,
leg. J. Bozonnet
, No. JB
V05056 (MM 30171). Grand Colombier, on dead leaf, 18-V-
1985,
leg. J. Bozonnet
, No. JB L05182 (MM 30173). Grand
Colombier, 1300 m, on dead twig of
Fagus sylvatica
, 17-IV-
1995,
leg. M. Meyer
(MM 8421; KRAM M1491). Innimond,
Le Grand Pertuis, 1080 m, on dead twig of
Fagus sylvatica
, 5-
IV-1995,
leg. J. Bozonnet
, No. JB V04054 (MM 30170). Teillat
Corniche du Valromey, 1150 m, on dead twig of deciduous
tree, 14-IV-1988,
leg. J. Bozonnet
, No. JB O04142 (MM
30172). Savoie: Celliers, 1850 m, on living twig of
Alnus
viridis
, 1-VI-1993,
leg. M. Meyer
(MM 7421; KRAM M-1488).
Me´ ribel, vers l’altiport, 45.4078uN, 06.5780uE, 1700 m, on
dead twig of
Picea excelsa
, 27-V-1995,
leg. M. Meyer
(MM
8500). Fontaine-le-Puits, Barrage de la Coche, 45u289110N,
06u309020E, 1450 m, on leaf and dead twig of
Fagus
sylvatica
, 28-IV-1992,
leg. M. Meyer
(MM 15295; KRAM M-
1490; MA-Fungi 35146). Les Arcs, 2000 m, on branch of
Rhododendron ferrugineum
, 9-V-2003, (MM 23268; KRAM M-
1487). Col de la Madeleine, 1800 m, on twig of
Alnus viridis
,
3-VI-2000,
leg. B. Martin
, No. JLBM 2028 (MM 27142). Jura:
Les Rousses, Bois d’Amont, on dead stem of herbaceous
plant, 20-V-1991,
leg. J. Duc
, No. JLBM 462 (MM 6833).
POLAND. The Carpathians: Tatry Mountains, a gully in
Mała Koszysta mountain toward Waksmundzka Polana
meadow, 49u159030N, 20u039280E, 1630 m, on living shoots
of
Salix silesiaca
,
leg. A. Ronikier & M. Ronikier
, 1-VI-2008
(KRAM M-1482). USA. California: Butte County, 4 miles
above Stirling City, 4000 ft. (1219 m), on bark, 9-V-1969,
leg.
D.T. Kowalski
, DTK 10016 (UC 1408212, as
L. fuscatum
).
Washington: Olympic National Park, Hurricane Ridge,
5200 ft. (1585 m), on twigs, 27-VI-1968,
leg. D.T. Kowalski
,
DTK 9576 (UC 1408234, as
L. fuscatum
). Olympic National
Park, Hurricane Ridge, 5200 ft. (1585 m), on twigs, 24-VI-
1968,
leg. D.T. Kowalski
, DTK 9361 (UC 1408277, as
L.
fuscatum
). Mount Rainier National Park, Bench Lake Trail,
4500 ft. (1372 m), on twig, 13-VI-1968,
leg. D.T. Kowalski
,
DTK 8630 (1408271, as
L. fuscatum
).
Etymology.
From Latin:
argentum
5silver,
brunneus
5brown. The epithet refers to the characteristic
silvery-brown sporotheca.
Habitat.
On plant remnants (ferns), decaying wood,
branches of dead or living trees and bushes (
Alnus
viridis
,
Fagus sylvatica
,
Picea abies
,
Salix silesiaca
,
Rhododendron ferrugineum
) near melting snow.
Distribution.
Known from the mountains of Europe:
the Alps, Carpathians, Jura and Pyrenees (Austria, France,
Poland, Spain) and North America (USA) (FIG.5).
Moist chamber culture.
Six stipitate sporocarps with
scanty peridium but with the typical areolate pattern
on the peridial remnants at the base of the sporothe-
cae were obtained from the moist chamber culture 21
May 2007, just over 3 mo after the culture was set up.
They had brown capillitium with many free ends and
well developed spores that were constant in shape,
measurement and ornamentation. All characters
agreed with those of the field specimen (MA-Fungi
75785) used to supply the spores and the substrate for
the culture. The plasmodium was not observed.
Lamproderma kowalskii A. Ronikier, Lado & Mar.
Mey., sp. nov. FIGS. 1D–F, 3
MycoBank 515371
Sporocarpia in gregibus dispersis, cum stipite, 1.32–
2.02 mm alta. Sporotheca 0.82–1.28 mm diam, globosa.
Peridium permanens, in fragmentis irregularibus fractum,
praeter basim tanquam poculum permanentem, argenteo-
griseum, chalibaeo-brunneo-griseum, plerumque cum aur-
eis repercussis. Stipes circa tam altus quam sporotheca,
0.42–0.9 mm, atrobrunneus, lucens. Hypothallus membra-
naceus, discoides, translucidus, aurantiaco-brunneus vel
brunneo-ruber. Columella circa dimidiam partem sporothe-
cae attingens, cylindracea, plerumque ad apicem se
dividens. Capillitium constanter ferrugineo-brunneum,
densum, imprimis ad columellae apicem oriens, leviter
flexuosum. Sporae ferrugineo-brunneae in massa, subbrun-
neae luce transmissa, globosae 8–9.5(–10) mmdiam,
brevibus spinis dense ornatae. Plasmodium ignotum.
Species prope nivem liquefactam fructificans.
Sporocarps in loose groups, stipitate (FIGS 1D, 3A),
total height 1.32–2.02 mm. Sporotheca globose, 0.82–
1.28 mm diam, silvery-brown. Peridium single, membra-
nous, persistent, splitting irregularly and persisting as a
cup at the base of the sporotheca, brownish under
transmitted light and with an areolate pattern at lower
part (FIG.1E). Stalk erect, 0.42–0.9 mm long, dark
brown, shining. Hypothallus membranous, discoid,
translucent, orange-brown or red-brown. Columella
reaching about half the sporotheca height, cylindrical
(FIG. 3B). Capillitium uniformly ferruginous-brown,
dense, originating mainly from the apex of the columella,
flexuose, capillitial threads at peripheries with many
pointed free ends (FIG.3C).Sporesinmassferruginous-
brown, pale brown by transmitted light, globose, 8–9.5
(–10) mmdiam,ornamentedwithdenselyarranged,short
spines (FIGS.1F,3D–F).Plasmodiumunknown.
HOLOTYPE. USA. California: Tehama County,
Well’s Cabin Camp ground, 6300 ft. (1920 m), on
twigs, 24-VI-1967,
leg. D.T. Kowalski
, DTK 6408 (UC
1408233, as
L. fuscatum
).
Specimens examined
. USA. California: Tehama County,
3 miles W of Child’s Meadow, 5200 ft. (1585 m), on dead
wood, 20-V-1967,
leg. D.T. Kowalski
,DTK6169(UC
1408279, as
L. fuscatum
). Tehama County, 3 miles E of
Mineral, on decayed wood,
leg. D.T. Kowalski
, DTK 6161
(UC 1408235, as
L. fuscatum
). Tehama County, 1 mile S of
Lassen National Park, on dead twigs, 28-V-1966,
leg. D.T.
Kowalski
, DTK 3173 (UC 1408269, as
L. fuscatum
). Siskiyou
County, Mount Shasta, 7600 ft. (2316 m), on dead twigs,
leg.
D.T. Kowalski
, DTK 7453 (UC 1408275, as
L. fuscatum
).
Tehama County, Morgan Summit, 5750 ft. (1753 m), dead
722 MYCOLOGIA

conifer twigs, 16-IV-1987,
leg. R.L. Critchfield Sr
, No. 2950
(MM 1685; NENB15269, as
L. fuscatum
).
Etymology.
In honor of Donald T. Kowalski, the
monographer of genus
Lamproderma
and collector of
almost all specimens of the new species examined by us.
Habitat.
On dead wood and twigs (coniferous) near
melting snow.
Distribution.
Known from the mountains of Califor-
nia (USA) (FIG. 5).
DISCUSSION
Morphology.—
The two new species have silvery-brown
sporothecae, with a hardly iridescent and areolate
peridium (FIG. 1B, E), and ferruginous-brown spores
in mass. These characters make them easy to
recognize from other
Lamproderma
species. Although
L. argenteobrunneum
and
L. kowalskii
seem to be
similar, numerous differentiating characters may be
found after detailed examination of them. Macro-
scopically
Lamproderma argenteobrunneum
is more
robust in general habit and it usually has subglobose
to slightly ovoid sporothecae (slightly higher than
wide) while
L. kowalskii
is more delicate and usually
has globose sporothecae. Moreover
L. argenteobrun-
neum
can be recognized by having a shorter stalk no
more than 0.64 mm (sometimes the stalk is absent)
and especially a much lower ratio of stalk length to
FIG. 3.
Lamproderma kowalskii
by scanning electron microscope—HOLOTYPE (DTK 6408). A. Sporocarp. B. Columella
and primary branches of the capillitium without membranous expansions. C. Peripheral part of capillitium. D–F. Spores. Bars:
A5500 mm, B 5300 mm, C 5100 mm, D–F 510 mm.
RONIKIER ET AL.: NIVICOLOUS
L
AMPRODERMA
SPECIES 723

the total height of the sporocarp (av. 0.19) than is the
case of
L. kowalskii
(av. 0.38) (FIG. 4B, C). The two
species can be readily distinguished microscopically
by the spore size (FIG.4A) and ornamentation,
covered with short, curved and loosely arranged
ridges in
L. argenteobrunneum
(FIGS. 1C, 2D–F) and
densely covered with spines in
L. kowalskii
(FIGS. 1F,
3D–F). Further differentiating characters may be
found in columella and capillitium (see TABLE I).
Lamproderma argenteobrunneum
is characterized by a
conical to narrowly conical columella (FIG. 2B) while
L. kowalski
has a cylindrical columella (FIG. 3B). The
capillitium in
L. argenteobrunneum
is moderately
dense, rigid, dark brown and with membranous
expansions at the primary branches (FIG. 2B–C) vs.
dense, flexuose and without membranous expansions
at the primary branches in
L. kowalski
(FIG. 3B–C).
All Kowalski’s specimens identified by him as
L.
fuscatum
(see list of collections under this species in
Kowalski 1970) turned out to be one of the two new
species described above, but one collection (USA:
California: Tehama County, Well’s Cabin Camp-
ground, 6300 ft. [1920 m], on twigs, 24-VI-1967,
leg.
D.T. Kowalski
, DTK 6375 [UC 1408232]) is similar to
L. kowalskii
in all aspects (general habit, ratio of stalk
length to the total height of the sporocarp, color of
the sporotheca, shape of columella and capillitium
and spore ornamentation) except for the larger spore
size, (10.5–)11–12 mm diam. This material might be a
large-spored form of the latter, but a taxonomic
evaluation was impossible because only one collection
is available.
The two new species could be confused with two
other
Lamproderma
species,
L. cacographicum
Bozon-
net, Mar. Mey. & Poulain and
L. fuscatum
(TABLE I),
because they have macroscopically similar color.
Lamproderma fuscatum
has ferruginous-brown spores
in mass, but it is distinguished from the two new
species by an evanescent peridium, dehiscing in small
patches, a capillitium with funnel-shaped capillitial
ends and warted spores (Meylan 1932, Neubert et al.
2000, Moreno et al. 2002, M. Poulain and M. Meyer
unpubl data). Although macroscopically similar
L.
fuscatum
seems to be unrelated to the two new
species. They are characterized by a persistent
peridium, therefore it is most likely that they belong
to the group of species forming a monophyletic clade
of ‘‘
L. ovoideum
group’’ as defined by Fiore-Donno et
al. (2008), while
L. fuscatum
belongs to the geneti-
cally distant clade of ‘‘
L. atrosporum
group’’ that
could be treated as a separate genus.
Lamproderma cacographicum
is the only previously
described species of genus
Lamproderma
character-
ized by a silvery-brown sporotheca, but it is easily
distinguishable from the two new species by its larger
spores (12–15 mm diam) with a characteristic orna-
mentation of crests forming a subreticulate pattern
(TABLE I; Bozonnet et al. 1997, Moreno et al. 2002).
The areoles of the peridium in the two new species
usually are easily visible under the light microscope
(oil immersion) at the base of the sporotheca. In most
specimens they densely cover the peridial surface.
However in some collections (MM 6833, 8421, 28409,
30173, Now 11693/2, DTK 10016, 8630, 9361) they
are scattered and difficult to observe or even may be
lacking. Such a characteristic peridium structure has
not been noted in the literature for any other
FIG. 4. Comparison of spore size and stalk length/total
sporocarp height ratio of
Lamproderma argenteobrunneum
and
L. kowalskii
. A. Box plots for spore size. B. Box plots for
stalk length/total sporocarp height ratio. La 5
L.
argenteobrunneum
, Lk 5
L. kowalskii
,¤5average, box 5
standard deviation, vertical line 5extreme values (dotted
line reaches the values present in less than 1%of
measurements). C. Scatter diagram of the relation of spore
size and stalk length/total sporocarp height ratio for
L.
argenteobrunneum
(&) and
L. kowalskii
(#).
724 MYCOLOGIA

Lamproderma
species, but we did observe it in all
studied collections (more than 30) of
L. cacographi-
cum
and also in two collections of
L.
cf.
aeneum
Mar.
Mey. & Poulain (MM 27521, MM 30849).
Lampro-
derma aeneum
can be easily recognized by the thin
and strongly iridescent, bluish-violet peridium (Pou-
lain et al. 2002) and the spores, which are dark brown
in mass. It differs from
L. kowalskii
by its larger
spores, 9.5–11(–11.5) mm, and from
L. argenteobrun-
neum
by the verrucose spore ornamentation.
FIG. 5. World distribution of
Lamproderma argenteobrunneum
(N) and
L. kowalskii
(#).
RONIKIER ET AL.: NIVICOLOUS
L
AMPRODERMA
SPECIES 725

Moist chamber culture.—
Conditions of the culture of
L. argenteobrunneum
differed from those widely used
for non-nivicolous myxomycetes. For the latter the
incubation temperature is usually around 20 C (room
temperature) and cultures are kept in diffuse light in
an approximately 12 h light/dark regime (e.g.
Ha¨rko¨ nen 1977, McHugh 2005, Novozhilov and
Schnittler 2008, Wrigley de Basanta et al. 2009). In
an attempt to simulate conditions under melting
snow the substrate material for
L. argenteobrunneum
was placed between moist filter paper disks and
incubated in the dark at 5 C. It is not clear whether
the initiates of the new sporocarps produced in the
moist chamber culture were the spores added to the
substrate or whether the plant remains already
carried undetected dormant stages of the life cycle,
such as sclerotia or microcysts that later gave rise to
fruiting. Attempts to germinate spores from the same
collection on agar were not successful. The moist
chamber culture was established in 2007, but the
collection (MA-Fungi 75785) that was used to supply
the substrate and spores was made in 1994, 13 y
earlier. The dormancy of the resistant stages of the
life cycle of this myxomycete, whether as spores, cysts
or sclerotia, was considerable. In the experiment by
Erbisch (1964) on spores of a few non-nivicolous
species it was demonstrated that they are able to
germinate even after 75 y. Investigation is under way
to determine spore viability, dormancy, germination
and the moist chamber culture of nivicolous
myxomycete species (D. Wrigley de Basanta unpubl
data).
Few reports on the culture of nivicolous myxomy-
cetes are available in the literature, and the method of
culture has not been established. A report of the
moist chamber culture of a nivicolous myxomycete
was published by Marx (1998), who obtained sporo-
carps of
Trichia sordida
Johannesen after nearly 2 mo
incubating a substrate at 12–16 C. A report in the
literature of another typically nivicolous species,
Comatricha suksdorfii
Ellis & Everh., was isolated in
moist chamber culture (Dulger et al. 2007), but the
identification of the collection seems to be doubtful,
and it might represent a non-snow bank species. The
specimen was collected at 39 m, and although
nivicolous myxomycetes may occur outside mountains
(Novozhilov 1986) the locality of this report from a
lowland area of the Mediterranean region is doubtful
for a snow bank species. Dulger et al. (2007) used the
standard method for moist chamber cultures and
incubated the culture at 25 C. The collection
reported by these authors unfortunately was not
available for study, therefore we were not able to
check the identity of the specimen. In addition there
are two reports of agar culture of nivicolous myxo-
mycetes either from spore to spore (Kowalski 1971) or
from spores to myxamoebae (Wikmark et al. 2007).
Geographical distribution.—
Nivicolous myxomycetes
constitute a clearly distinguishable ecological group of
TABLE I. Distinguishing characters of the two new species of
Lamproderma
and previously described macroscopically
similar species
Character
L. fuscatum
(from
Moreno et al. 2002)
L. argenteobrunneum L. kowalskii
L. cacographicum
(from
Bozonnet et al. 1997)
Sporotheca (form) Globose to subglobose Subglobose to slightly
ovoid
Globose Globose to ovoid
Sporotheca (color) Rusty brown Silvery-brown Silvery-brown Silvery-brown
Peridium Evanescent in small
patches, not areolate
Persistent, typically
areolate
Persistent, typically
areolate
Persistent, areolate
Stipe length Up to 1 mm 0.04–0.64 mm 0.42–0.9 mm 0–1 mm
Columella (form) Cylindrical Conical to narrowly
conical
Cylindrical Obconical
Capillitium Ferruginous, with
membranous
expansions at the
primary branches,
with funnel-shaped
capillitial ends
Dark brown, rigid,
with membranous
expansions at the
primary branches,
with pointed free
ends
Brown, flexuose,
without membranous
expansions at the
primary branches,
with pointed free
ends
Dark brown, hyalines at the
ends, with membranous
expansions at the
primary branches, with
pointed free ends
Spores (color in
mass)
Ferruginous-brown Ferruginous-brown Ferruginous-brown Dark brown
Spore size (9–)10–11 mm (8.0–)9–11(–12) mm 8–9.5(–10) mm (10.5–)12–15 mm
Spore
ornamentation
Minutely warted Loosely arranged short,
curved ridges and
spines
Densely spinulose Crests forming a
subreticulate pattern
726 MYCOLOGIA

species requiring specific micro-environmental condi-
tions for the development of fruit bodies (Lado 2004).
These conditions can be found under long persisting
snow, at the edges of snow banks and in places where
the snow has just melted. As demonstrated by Ronikier
and Ronikier (2009) nivicolous species are not alpine
or arctic-alpine geographically but can be considered
mountain species. Most data on the occurrence of
nivicolous species are available from European moun-
tains (e.g. Meylan 1914, 1932; Bozonnet 1984; Meyer
1986; Poulain et al. 2003, 2005; Moreno et al. 2003;
Lado et al. 2005; Sa´nchez et al. 2007; Lado and
Ronikier 2008, 2009; Ronikier et al. 2008), but many
species also have been reported from North America
(e.g. Kowalski 1971, 1975) and Asia (e.g. Tamayama
2000) in the northern hemisphere. Of the two species
described here
L. argenteobrunneum
is characterized by
wide geographical distribution (FIG. 5) but the other,
L. kowalskii
, seems to be restricted to a reduced region
of North America (FIG. 5).
The species known so far from limited areas, such as
Diacheopsis pauxilla
Mar. Mey. & Poulain or
Dianema
inconspicuum
Poulain, Mar. Mey. & Bozonnet (Meyer
and Poulain 1998, Poulain et al. 2000) from the Alps,
are recently described species, so their distribution is
not yet fully known. The increasing number of reports
of nivicolous species from the southern hemisphere
(e.g. Stephenson and Johnston 2003; Stephenson et al.
2007a, 2007b; Stephenson and Shadwick 2009) and the
similarity in their myxobiota suggest that most nivico-
lous myxomycetes are characterized by a worldwide but
fragmented distribution, associated with the moun-
tains of the world.
ACKNOWLEDGMENTS
We thank Jean Bozonnet for translation of the Latin
diagnoses, the curator of UC for loan of the Kowalski
collections of
Lamproderma
, Wolfgang Nowotny for provid-
ing us with his specimens, Jakub Cies´lak for help with the
statistical analysis and two anonymous reviewers for their
valuable comments on the manuscript. This project was
partly supported by the European Community Program
‘‘Structuring the European Research Area’’, under
SYNTHESYS at the Real Jardı´n Bota´ nico (CSIC), granted
to Anna Ronikier, and by the Ministry of Science and
Innovation of Spain (project CGL2008-00720/BOS).
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