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Aboveground species richness patterns of vascular plants, aphyllophoroid macrofungi, bryophytes and lichens were compared along an altitudinal gradient (80-310 m a.s.l.) on the Slantsevaya mountain at the eastern macroslope of the Polar Urals (Russia). Five altitudinal levels were included in the study: (1) Northern boreal forest with larch-spruce in the Sob' river valley habitats; (2-3) two levels of closed, northern boreal, larch-dominated forests on the slopes; (4) crook-stemmed forest; (5) tundra habitats above the timberline. Vascular plant or bryophyte species richness was not affected by altitudinal levels, but lichen species richness significantly increased from the river valley to the tundra. For aphyllophoroid macrofungi, species richness was highest at intermediate and low altitudes, and poorest in the tundra. These results indicate a positive ecotone effect on aphyllophoroid fungal species richness. The species richness of aphyllophoroid fungi as a whole was neither correlated to mortmass stocks, nor to species richness of vascular plants, but individual ecological or morphological groups depended on these parameters. Poroid fungal species richness was positively correlated to tree age, wood biomass and crown density, and therefore peaked in the middle of the slope and at the foot of the mountain. In contrast, clavarioid fungal species richness was negatively related to woody bio-and mortmass, and therefore peaked in the tundra. This altitudinal level was characterized by high biomass proportions of lichens and mosses, and by high litter mortmass. The proportion of corticoid fungi increased with altitude, reaching its maximum at the timberline. Results from the different methods used in this work were concordant, and showed significant patterns. Tundra communities differ significantly from the forest communities, as is also confirmed by nonmetric multidimensional scaling (NMDS) analyses based on the spectrum of morphological and ecological groups of aphyllophoroid fungi.
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Fungi
Journal of
Article
Relationship between Species Richness, Biomass and
Structure of Vegetation and Mycobiota along an
Altitudinal Transect in the Polar Urals
Anton G. Shiryaev 1, * , Ursula Peintner 2, Vladimir V. Elsakov 3, Svetlana Yu. Sokovnina 4,
Denis A. Kosolapov 3, Olga S. Shiryaeva 1, Nadezhda M. Devi 5and Andrei A. Grigoriev 6
1Vegetation and Mycobiota Biodiversity Department, Institute of Plant and Animal Ecology,
Ural Branch of the Russian Academy of Sciences, 8 March Str., 202, 620144 Ekaterinburg, Russia;
olga.s.shiryaeva@gmail.com
2Institute of Microbiology, Innsbruck University, Technikerstr. 25, 6020 Innsbruck, Austria;
ursula.peintner@uibk.ac.at
3Komi Scientific Centre, Northern Flora and Vegetation Department, Institute of Biology, Ural Branch of the
Russian Academy of Sciences, Kommunisticheskaya Str., 28, 167982 Syktyvkar, Russia;
elsakov@ib.komisc.ru (V.V.E.); kosolapov@ib.komisc.ru (D.A.K.)
4Arctic Research Station, Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of
Sciences, Zelenaya Gorka Str., 21, 629400 Labytnangi, Russia; sokovnina_su@ipae.uran.ru
5
Dendrochronology Department, Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy
of Sciences, 8 March Str., 202, 620144 Ekaterinburg, Russia; nadya@ipae.uran.ru
6
Geoinformation Technologies Department, Institute of Plant and Animal Ecology, Ural Branch of the Russian
Academy of Sciences, 8 March Str., 202, 620144 Ekaterinburg, Russia; grigoriev.a.a@ipae.uran.ru
*Correspondence: anton.g.shiryaev@gmail.com
Received: 13 November 2020; Accepted: 8 December 2020; Published: 9 December 2020


Abstract:
Aboveground species richness patterns of vascular plants, aphyllophoroid macrofungi,
bryophytes and lichens were compared along an altitudinal gradient (80–310 m a.s.l.) on the
Slantsevaya mountain at the eastern macroslope of the Polar Urals (Russia). Five altitudinal levels
were included in the study: (1) Northern boreal forest with larch-spruce in the Sob’ river valley habitats;
(2–3) two levels of closed, northern boreal, larch-dominated forests on the slopes; (4) crook-stemmed
forest; (5) tundra habitats above the timberline. Vascular plant or bryophyte species richness was
not aected by altitudinal levels, but lichen species richness significantly increased from the river
valley to the tundra. For aphyllophoroid macrofungi, species richness was highest at intermediate
and low altitudes, and poorest in the tundra. These results indicate a positive ecotone eect on
aphyllophoroid fungal species richness. The species richness of aphyllophoroid fungi as a whole
was neither correlated to mortmass stocks, nor to species richness of vascular plants, but individual
ecological or morphological groups depended on these parameters. Poroid fungal species richness
was positively correlated to tree age, wood biomass and crown density, and therefore peaked in
the middle of the slope and at the foot of the mountain. In contrast, clavarioid fungal species
richness was negatively related to woody bio- and mortmass, and therefore peaked in the tundra.
This altitudinal level was characterized by high biomass proportions of lichens and mosses, and by
high litter mortmass. The proportion of corticoid fungi increased with altitude, reaching its maximum
at the timberline. Results from the dierent methods used in this work were concordant, and showed
significant patterns. Tundra communities dier significantly from the forest communities, as is
also confirmed by nonmetric multidimensional scaling (NMDS) analyses based on the spectrum of
morphological and ecological groups of aphyllophoroid fungi.
Keywords:
biodiversity; fungal ecology; climatic gradient; productivity; flora; lichen; mosses;
life form; phytocoenology; plant–fungal interactions; timberline; tundra; Arctic greening
J. Fungi 2020,6, 353; doi:10.3390/jof6040353 www.mdpi.com/journal/jof
J. Fungi 2020,6, 353 2 of 22
1. Introduction
The consequences of global climate change are most obvious in the Arctic, where warming rates
are two to three times higher than the world average [
1
]. Vegetational changes are quite evident
at these high-latitudes, and get clearly manifested in the range expansion of typical boreal species
to the north, and in a reduction in Arctic-Alpine species [
2
,
3
]. Such a greening of vegetation takes
place throughout the Arctic [
4
,
5
]. Concomitantly, major changes were reported for the diversity and
composition of animals and vascular plants, but little attention has been paid to fungi up to now [
6
,
7
].
Climate change has had a significant impact on the mycobiota at high latitudes over the last
20 years. Long-term fruitbody monitoring studies proved that with warming, species richness and
yield of edible fungi increased in Europe, together with a prolongation of the fruiting season [
7
].
A migration of southern fungal species to the North was reported, with migration rates of about
500–700 km in 10–20 years [
8
]. Climate change is also aecting subarctic areas in Russia. As shown by
our recently published study carried out in the Polar Urals [
9
], the climate in the region has warmed by
2
C over the last 60 years. As a consequence, the species richness of aphyllophoroid fungi detected in
the Slantsevaya mountain area nearly doubled (from 157 to 257 species). At the same time mushrooms
appeared, whose appearance was obviously connected with the emergence of “new boreal” substrates,
which were not present before on the mountain, since the vegetation 60 years ago was forest tundra.
So the permafrost began to thaw 2 times deeper. At the same time the plant productivity increased
enormously: 21 times more woody biomass was produced, which resulted in a sucient amount of
large-sized dead wood (and not only many small spruces and larches). Furthermore, a distinct cover
of mesophilic tall grass developed, which overgrew the mossy plant communities of the moor tundra.
The newly recorded fungal species mostly represented typical boreal morphotypes (poroid) and
boreal ecological-trophic groups (mycorrhizal fungi, humus-inhabiting saprobes, wood-inhabiting
saprobes, etc.). Hand in hand with this increase in boreal species, the proportion of arctic-alpine
litter-inhabiting species decreased significantly.
Surprisingly, for a few places in the Polar Urals, it was reported that neither the vegetation,
biomass stock nor aphyllophoroid fungal species richness and their ecomorphological structure were
aected by climate change [
10
,
11
]. This clearly shows that the emergence of new (boreal) fungal
species is primarily associated with a change in the vegetation structure and the amount of available
plant biomass (biotic factors), and not to the increase in temperature (abiotic factor). The influence
of climate on the diversity of aphyllophoroid fungi of the Polar Urals was presented in our previous
article [
9
]. In this context, we are now addressing key factors of the vegetation structure and biomass
stock, which are shaping subarctic fungal communities. Based on the previous study [
9
], changes in the
above-ground mycobiota occur in the sequential order: first, temperatures and precipitation increase.
In response, the permafrost thaws deeper and the microbial soil activity increases. The vegetation also
changes at this stage: its greening, the borealization, takes place. With increased plant productivity,
the plant biomass and the especially woody mortmass also increases. The structure of the aboveground
mycobiota changes only from this time on.
The Subarctic is one of the simplest organized ecosystems of the planet. Thus, it can serve
as a model ecosystem for assessing the influence of basic biotic factors on aphyllophoroid fungal
communities. The following globally relevant hypotheses (H) can be addressed in a straight-forward
way: H1: Species richness of aphyllophoroid fungi is positively correlated to substrate availability.
Thus, the richest mycobiota develops in the floristic richest regions [
11
,
12
]. H2: Fungal and vascular
plant species richness decreases with altitude in the Polar Urals [
13
]. H3: The species richness of
heterotrophic fungi is positively correlated to the volume of mortmass [
14
,
15
]; the higher the mortmass
of trees, the higher the species richness of wood-destroying fungi, and the higher the mortmass of the
litter, the higher the species richness of litter saprobes. H4: Fungal species richness, especially richness of
J. Fungi 2020,6, 353 3 of 22
wood-degrading fungi, is positively related to forest age and crown density [
16
,
17
]. H5: Fungal species
forming large fruitbodies are associated either to bigger large-sized woody substrates (wood-degrading
fungi), or to deeper soil thawing (mycorrhizal fungi) [18,19].
The aim of this study was to address the biotic factors influencing the aboveground species richness
and the ecological-morphological structure of aphyllophoroid fungi communities along an altitudinal
transect of the Polar Urals. These data should serve as a solid base for modeling future developments
in the Arctic. Accurate prediction should not only include changes in vegetation (representing the
productive part), but also changes in aphyllophoroid fungal communities (representing the destructive
part).
2. Materials and Methods
2.1. Study Area
The study area is located where the Sob’ river cuts through the eastern slope of the Polar Urals at
the territory of the Yamal-Nenetsk Autonomous District in Russia. The river flows from northwest to
southeast, with the valley framed from west and southwest by Rai-Iz mountain, and from north and
northeast by the Slantsevaya mountain. The area is located 30 km north of the Arctic Circle (N 66
54
0
;
E 65
44
0
) and the border between Europe and Asia, 60 km east of Vorkuta town (Komi Republic),
50 km west of Salekhard town (capital of Yamal-Nenetsk Autonomous District) and 30 km west of
Labytnangi town (Figure 1). The study site has an area of 10 km
2
(the width of the river valley with
mountain slopes is 2 km and 5 km length along the river).
J. Fungi 2020, 6, x FOR PEER REVIEW 3 of 22
especially richness of wood-degrading fungi, is positively related to forest age and crown density
[16,17]. H5: Fungal species forming large fruitbodies are associated either to bigger large-sized
woody substrates (wood-degrading fungi), or to deeper soil thawing (mycorrhizal fungi) [18,19].
The aim of this study was to address the biotic factors influencing the aboveground species
richness and the ecological-morphological structure of aphyllophoroid fungi communities along an
altitudinal transect of the Polar Urals. These data should serve as a solid base for modeling future
developments in the Arctic. Accurate prediction should not only include changes in vegetation
(representing the productive part), but also changes in aphyllophoroid fungal communities
(representing the destructive part).
2. Materials and Methods
2.1. Study Area
The study area is located where the Sob’ river cuts through the eastern slope of the Polar Urals
at the territory of the Yamal-Nenetsk Autonomous District in Russia. The river flows from northwest
to southeast, with the valley framed from west and southwest by Rai-Iz mountain, and from north
and northeast by the Slantsevaya mountain. The area is located 30 km north of the Arctic Circle (N
66°54; E 65°44) and the border between Europe and Asia, 60 km east of Vorkuta town (Komi
Republic), 50 km west of Salekhard town (capital of Yamal-Nenetsk Autonomous District) and 30
km west of Labytnangi town (Figure 1). The study site has an area of 10 km2 (the width of the river
valley with mountain slopes is 2 km and 5 km length along the river).
Figure 1. Map of the investigated area in the Polar Urals. The study area is marked as a
white square.
The digital relief model of the study area was taken from ArcticDEM
(http://www.pgc.umn.edu/data/arcticdem/). This model is used for topographic correction of figures
of crown density, relief and types of vegetation.
Monthly meteorological records covering the period from 1892 to 2018 are available from the
nearest weather station of Salekhard (N 66°32, E 66°32; 35 m a.s.l.). These data indicate a negative
average annual temperature (6.4 °C) and a mean annual precipitation of 415 mm, of which 45% falls
Figure 1.
Map of the investigated area in the Polar Urals. The study area is marked as a white square.
The digital relief model of the study area was taken from ArcticDEM (http://www.pgc.umn.edu/
data/arcticdem/). This model is used for topographic correction of figures of crown density, relief and
types of vegetation.
Monthly meteorological records covering the period from 1892 to 2018 are available from the
nearest weather station of Salekhard (N 66
32
0
, E 66
32
0
; 35 m a.s.l.). These data indicate a negative
average annual temperature (
6.4
C) and a mean annual precipitation of 415 mm, of which 45% falls
J. Fungi 2020,6, 353 4 of 22
as snow (Figure 2). The region is characterized by a complex wind regime dominated by westerly
winds, with an average wind speed of 8.5–8.8 m/s in winter, and 6.5–7.0 m/s in summer.
J. Fungi 2020, 6, x FOR PEER REVIEW 4 of 22
as snow (Figure 2). The region is characterized by a complex wind regime dominated by westerly
winds, with an average wind speed of 8.5–8.8 m/s in winter, and 6.5–7.0 m/s in summer.
Figure 2. Climagram for Salekhard weather station (1892–2018). The blue line represents the
long-term average sum of precipitation, red columns are the average monthly temperatures.
There has been almost no economic activity in the study area over the last 60 years. A small
village (14 houses) was located here from 1940–1950, where the construction workers of the
Salekhard–Vorkuta railway lived, which currently crosses the Polar Urals from east to west. At the
moment, anthropogenic activity here is restricted to transhumance by the local Nenets driving herds
of reindeer during winter. Under the Slantsevaya mountain there are two houses (rail station 141
km) in which two people permanently live [9].
The response of the vegetation to climate warming is well studied in the Polar Urals [2,9,20–22].
Over the 60 years that have passed since the beginning of these long-term monitoring studies, the
climate has changed significantly in the Slantsevaya mountain are: the average annual summer
temperature has increased by 1.8 °C, and the winter temperature by 2.0 °C, and, as a consequence,
the length of the growing season has increased by 7 days. The biomass of the dominating tree species
has increased significantly. For Picea obovata Lebed. from 0.22 to 4.64 t/ha, and for Larix sibirica Lebed.
from 28.34 to 97.60 t/ha. The crown density of the trees has also increased by 20% [9,22]. Photographs
taken in 1962 and in 2020 on the slopes of Slantsevaya mountain show a drastic transformation of the
vegetation in the river valley and on the mountain slopes from forest-tundra to north boreal forest
[2], and impressively document the rising of the upper forest boundary by 50 m over 58 years
(Figure 3). Particularly noteworthy is the afforestation of the gentle slope in the front part of the
image, as it is clearly associated with an increase in density and productivity of these larch stands. A
similar trend was noted in the neighboring mountains [2,20].
2.2. Sampling Sites and Altitudinal Gradient
Plant communities were studied on an altitudinal gradient (transect) on the western/
southwestern slope of the Slantsevaya mountain (Figure 4), ranging from the Sob’ river valley to the
mountain tundra (80–310 m a.s.l.). The altitudinal gradient included 5 altitude levels: level I (80 m
a.s.l.) closed the north boreal forest in the Sob’ river valley; level II (170 m a.s.l.) the middle part of
the slope with the closed north boreal forest; level III (230 m a.s.l.), the upper limit of the closed
forest; level IV (260 m a.s.l.) the mountain crooked forest; level V (310 m a.s.l.) mountain bush
tundra.
Figure 2.
Climagram for Salekhard weather station (1892–2018). The blue line represents the long-term
average sum of precipitation, red columns are the average monthly temperatures.
There has been almost no economic activity in the study area over the last 60 years. A small village
(14 houses) was located here from 1940–1950, where the construction workers of the Salekhard–Vorkuta
railway lived, which currently crosses the Polar Urals from east to west. At the moment, anthropogenic
activity here is restricted to transhumance by the local Nenets driving herds of reindeer during winter.
Under the Slantsevaya mountain there are two houses (rail station 141 km) in which two people
permanently live [9].
The response of the vegetation to climate warming is well studied in the Polar Urals [
2
,
9
,
20
22
].
Over the 60 years that have passed since the beginning of these long-term monitoring studies, the climate
has changed significantly in the Slantsevaya mountain are: the average annual summer temperature
has increased by 1.8
C, and the winter temperature by 2.0
C, and, as a consequence, the length of the
growing season has increased by 7 days. The biomass of the dominating tree species has increased
significantly. For Picea obovata Lebed. from 0.22 to 4.64 t/ha, and for Larix sibirica Lebed. from 28.34
to 97.60 t/ha. The crown density of the trees has also increased by 20% [
9
,
22
]. Photographs taken
in 1962 and in 2020 on the slopes of Slantsevaya mountain show a drastic transformation of the
vegetation in the river valley and on the mountain slopes from forest-tundra to north boreal forest [
2
],
and impressively document the rising of the upper forest boundary by 50 m over 58 years (Figure 3).
Particularly noteworthy is the aorestation of the gentle slope in the front part of the image, as it is
clearly associated with an increase in density and productivity of these larch stands. A similar trend
was noted in the neighboring mountains [2,20].
2.2. Sampling Sites and Altitudinal Gradient
Plant communities were studied on an altitudinal gradient (transect) on the western/southwestern
slope of the Slantsevaya mountain (Figure 4), ranging from the Sob’ river valley to the mountain tundra
(80–310 m a.s.l.). The altitudinal gradient included 5 altitude levels: level I (80 m a.s.l.) closed the north
boreal forest in the Sob’ river valley; level II (170 m a.s.l.) the middle part of the slope with the closed
north boreal forest; level III (230 m a.s.l.), the upper limit of the closed forest; level IV (260 m a.s.l.) the
mountain crooked forest; level V (310 m a.s.l.) mountain bush tundra.
J. Fungi 2020,6, 353 5 of 22
Figure 3.
Comparison of the development of vegetation on the Slantsevaya mountain over 58 years
(1962–2020) based on photographs. The rise of the upper forest border, and an increase in the tree
crown density are evident.
J. Fungi 2020, 6, x FOR PEER REVIEW 5 of 22
Figure 3. Comparison of the development of vegetation on the Slantsevaya mountain over
58 years (1962–2020) based on photographs. The rise of the upper forest border, and an
increase in the tree crown density are evident.
Figure 4. Map of Slantsevaya mountain with the studied altitudinal levels as well as
parameters of forest crown density. Color legend: blue 1—water (Sob’ river), beige
2grass communities, orange 3—stones; yellow to dark green transitional colors represent
tree crown density (%).
Figure 4.
Map of Slantsevaya mountain with the studied altitudinal levels as well as parameters of forest
crown density. Color legend: blue 1—water (Sob’ river), beige 2—grass communities, orange 3—stones;
yellow to dark green transitional colors represent tree crown density (%).
J. Fungi 2020,6, 353 6 of 22
Within each altitudinal level, five plots of 400 m
2
(20 m
×
20 m) were established for our
phytocoenological investigations. Thus, the sum plots an area of 2000 m
2
for each level (Figure S1).
Within each altitudinal level, the dierence in altitude of the plots was plus/minus 8 m. On average,
there was a distance of 20 m between each plot. Areas were not included in the study if they had open
zones with a crown density diering by more than 20% from the model plots. This was the case if bogs
occurred between forest plots. Thus, each altitudinal level has a total area of 3600 m
2
(20 m
×
180 m).
In total, along the entire altitude gradient, studies were carried out on an area of 18,000 m
2
(1.8 ha).
The plots included a complex of the most typical phytocenoses for each altitudinal level.
2.3. Species Richness and Biomass for Vascular Plants, Bryophytes and Lichens
Field work was carried out in August 2020. On each trial plot, geobotanical descriptions
were carried out according to the standard technique [
23
]: the species composition of plants
for the herb-dwarf shrub and the moss-lichen aboveground layers, and the projective cover and
the height of the tiers were taken into account. Vascular plant species were assigned to seven
functional groups: tall shrubs (Duschekia fruticosa (Rupr.) Pouzar, Salix phylicifolia L., et al.),
shrubs (Betula nana L., Vaccinium uliginosum L., et al.), dwarf shrubs (Atragene sibirica L., Dryas octopetala L.,
Vaccinium myrtillus L., et al.), evergreen ericoid (Andromeda polifolia L., Empetrum hermaphroditum
Hagerup, et al.), forbs (Aconitum septentrionale Koelle, Dryopteris carthusiana (Vill.) HP Fuchs,
Equisetum arvense L., Rubus chamaemorus L., et al.), grasses (together with sedges—Calamagrostis sp.,
Carex sp., Luzula wahlenbergii Rupr.,
Poa sp., et al.
), ericoid plants (Lycopodium dubium Zoega), as well as
bryophyts and lichens. A more detailed description of the belonging of herbaceous plant species to a
specific functional group can be found in [
24
]. Trees are excluded from this list, as they were studied
separately, in the dendrochronology section. The assignment of vascular plant species to six life forms
(phanerophytes, hemicryptophytes, chamaephytes, geophytes, therophytes, cryptophytes) follows [
25
].
The species richness of bryophytes and lichens was estimated for the most common aboveground
species only (epilithic species excluded).
Species were subdivided into separate functional groups and life forms, and then their biomass
was assessed. Inside three plots at each altitudinal level, three mini-plots (altogether nine in the level)
with a size of 50 cm
×
50 cm (0.25 m
2
) were studied. All plants growing at the survey mini-plots
were harvested, sorted by groups and dried in laboratory drying cabinets to dry-weight constancy.
Moreover, leaf and grass litter, woody litter and fallen branches, conifer cones and tree-bark were
collected. Samples were weighed on a Kern 440-33 N balance with an accuracy of 0.1 g. For the
herb-dwarf shrub layer, the analysis was carried out individually for dierent life forms and functional
groups of vascular plants and litter. The dry-weight of these samples was combined into total mortmass.
The biomass and mortmass were also studied for the all moss-lichen aboveground layer (green mosses,
Sphagnums and lichens), and the projective cover was calculated. The projective cover and weight
for dierent functional groups and life forms were calculated as the sum of coverings or masses of
individual species. Mean and standard error are calculated for 5 plots within each elevation.
Meso- and nanophanerophyts also include woody plants of the herbaceous-shrub layer. In this
case, macro-phanerophytes (for example, Larix sibirica,Picea obovata,Betula pubescens, etc.) were
separately considered as an element of the first tree layer. The methodology for studying the structure
of the tree layer and the dendrochronological work are described below.
2.4. Data Sampling and Processing for Dendrochronological Studies
The structure of the tree layer and its biomass and mortmass were studied at all five altitudinal
levels (Figure 4). At each level, inside the same 5 plots, were tested 3–5 plots with a size of
20 m ×20 m
,
on which the structure of the grass-dwarf shrub and moss-lichen layers was also assessed. At level II,
the dendrochronological study was carried out in part, while we present data on biomass only.
J. Fungi 2020,6, 353 7 of 22
The morphometric parameters were measured for a total of 694 trees and undergrowth units,
and the plant age was calculated for each of them. The trees on the lower levels (I and II) were studied
in 2020, but the data from the upper levels (III-V) were taken from our previous studies [9,22].
On each plot, the exact locations of each tree and understory plant were recorded, as well as their
height, basal diameter, diameter at an altitude 1.3 m, crown diameter in two mutually perpendicular
directions using a tape measure (0.5 m accuracy), a telescopic ruler (1.0 m accuracy) and digital
rangefinder (accuracy 0.3 m). Tree ages were determined based on wood samples (cores) taken at the
stem base using a Haglof borer, or by taking a transect with a handsaw (less than 3 cm in diameter).
Each wood sample was glued to a wooden strip, cleaned with a shaving blade, and pigmented with
white powder to enhance ring boundary contrasts [
26
]. Growth ring counting and core dating were
carried out according to generally accepted methods [
26
,
27
] under laboratory conditions. All wood
samples were measured on a semi-automatic machine Lintab 6 (F. Rinn S.A., Heidelberg, Germany) [
28
].
To identify false and missing rings, wood samples were dated according to the generalized tree-ring
chronology for the study site [
3
,
29
]. Trees less than 1.5 m and of an age less than 30 years were
attributed to saplings.
If the collected drill holes did not reach the center of the trunk, the age of the tree was extrapolated
based on local tree ring patterns. The ratio of tree age to height was determined using a regression
equation. Using this data, corrections could be calculated to determine the more accurate age of each of
the trees we examined with a diameter >3–4 cm [
26
]. We made sure that no significant number of dead
trees or stump remains remained at the site after the trees were felled. We could not find any signs of
fire in our drill cores. From this, we conclude that no forest fires have occurred on the test plots in the
last 400 years. Other unfavorable factors can also be excluded due to the structure of the annual rings.
The aboveground tree biomass was estimated for the two most widespread tree species in the
study area: Siberian larch (Larix sibirica) and common spruce (Picea obovata) according to methods
described before [
21
,
22
,
29
]. For the upper forest boundary and the upper enclosed forest, the tree
biomass estimates were conducted at the border of the trial-plots. The so-called model trees (n=33)
were felled and sectioned. The stem biomass was determined with hand scales with accuracy 50 g.
The fresh weight of leafless branches, needles and generative organs were determined separately with
a digital weight (accuracy 0.01 g). All subsamples were then oven-dried at 106
C to stable weight.
The drying time ranged from several hours to days. Then, the masses of all these biomass fractions were
summarized. Allometric functions between the total tree biomass (dry-weight) and the tree diameters
at base height were calculated [
22
]. Using these data together with the tree ages, the annual biomass
accumulation could be calculated for each tree. The calculations were based on the following formula:
Dn=(Rn/Rfinal)×Dfinal
D
n
is the computed tree diameter in a certain year; R
n
is distance from the tree core to a certain
annual ring; R
final
is the current tree radius; and D
final
is the current tree diameter. Now, based on this
database, the aboveground biomass of larch and spruce per hectare could be reliably determined based
on the measurements carried out on the trees growing in our plots. In addition, the biomass of birch
trees (Betula pendula) was determined based on previously published relationships and equations [
21
]
for the plot levels I and II. The significance of birch for the structure of the stand increased significantly
at lower levels, but at upper levels, large-stemmed birch trees occurred sporadically or were absent.
The mortmass parameters were studied for coarse woody debris (CWD, diameter more than 5 cm:
dead trees) and fine woody debris (FWD, less than 5 cm: branches, thin trees, cones and bark pieces)
at all altitudinal levels in 2020. Mortmass was determined based on measurements of dead wood
volume and its density for each species, separately. For CWD, the mortal mass was calculated for dead
fallen and standing trees. On the high-altitude profile (V), dead trees were found only scattered in the
mountain tundra, and there were only branches of shrubs (Betula nana,Salix spp.), while at the foot of
the mountain, dead trees prevailed over shrubs.
J. Fungi 2020,6, 353 8 of 22
2.5. Fungal Sampling
Aphyllophoroid fungi were used in this study as a model group for macromycetes. The first
samples in the study area were collected by S.G. Shiyatov and N.T. Kazantseva in 1959, but regular
research began in 1961. The results of 60 years of mycological monitoring in the Sob’ river valley
and on the slopes of the Slantsevaya mountain were recently published [
9
]. These baseline data
were now complemented by our most recent data from August 2020, when we carried out extensive
sampling along the altitudinal gradient established in this study. A list of aphyllophoroid fungi and
the distribution of species by altitudinal levels is given in Table S1. Furthermore, the list of species
includes information concerning fruitbody types, ecological strategies and height groups.
Fruitbody types, or morphotypes, of aphyllophoroid fungi include three major species-rich groups
(corticioids, poroids and clavarioids), and some smaller groups (e.g., cantharelloids, thelephoroids and
stipitate hericioids). These groups are good indicators of bioclimatic conditions: in the tundra without
autochthonous woody substrates, clavarioids are dominant; in shrub tundra with many dierent small
twigs, corticioids on Betula nana bushes as well as a lot of clavarioids on dierent grasses and herbs are
dominating. In the boreal forests with many big coniferous and deciduous tree trunks, poroids have a
big share of the aphyllophoroid species richness.
Ecological strategies of aphyllophoroid fungi include three basic types. Parasites (on alive trees,
shrubs, grasses and mosses), mutualistic symbionts (ectomycorrhiza-forming and basidio-lichens)
and saprobs (on deadwood, humus and litter). Fungi growing on dead grass, leaves, needles,
mixed decaying litter, twigs less than 1 cm in diameter, as well as on wood in its final decay stage 5
(representing individual fibers) or on a separate bark (for example, inside the birch bark) were defined
as litter saprobs. Among the saprobes, we did not distinguish between species with substrate types on
mosses, as there were only two species and there were no dynamics. Despite the fact that parasites
develop on dierent substrates, we did not subdivide this group into separate substrate groups,
because almost all species were collected on wood, and only one species on grasses. We also considered
symbionts as a single group, since there are were only two species of basidiolichens, and they were
found only in the mountain tundra.
A few fungi are mixotroph (e.g., genus Tomentella—ectomycorrhizal and litter/wood saprobes,
Osteina obducta (Berk.) Donk—wood and soil saprobs, etc.) In this case, they were listed in both groups.
In order to obtain generalized data, the respective shares were normalized to a common denominator
(100%). In general, the ratio of these three ecological groups varies significantly depending on the
latitudinal-zonal position of the studied region [9].
Height groups, or fruitbody size, were estimated only for species with negatively geotropic fruit
bodies >2 mm (clavarioids, cantharelloides, thelephoroids and stipitate hydnoids). They are divided
into three groups: group I—fruit bodies up to 3 cm high, group II—up to 8 cm and group III—more than
8 cm high. Small-fruiting species (group I) prevail in the arctic tundra, while in rich hemiboreal and
nemoral forests with tall trunk trees, the proportion of large-fruiting species (groupIII) is high [9,10].
The fungi were collected at the same five altitudinal levels, each with an area of 20 by 180 m
(Figure 4). Averaging over the plots within these levels was not done. The fruitbodies collected in 2020
were deposited in the following mycological collections: Institute of Plant and Animal Ecology UrB
RAS, Ekaterinburg (SVER) and Institute of Biology, Komi SC UrB RAS, Syktyvkar (SYKO).
2.6. Data Analysis
Ordination analyses were carried out on non-metric multidimensional scaling (NMDS) in the
ExStatR program [
30
]; the statistical package R (V. 3.5.2) was used for visualization [
31
]. The significance
of dierences between groups was calculated based on the nonparametric Kruskal–Wallis test—a
comparison of median values. Data were tested for significant dierences based on nonparametric
Kruskal–Wallis tests, Spearman rank correlation (rs) and the Monte Carlo method (U).
J. Fungi 2020,6, 353 9 of 22
3. Results
3.1. Vegetation Cover and Plant Communities
The highest species richness of vascular plants was detected in the river valley (46 species), and the
lowest in the tundra (26). In the intermediate altitudinal layers, the number of species varied from 37
to 38 (Table 1).
Table 1.
Number of vascular plant species detected at the dierent altitudinal levels of the Slantsevaya
mountain. Data are presented as richness of plant functional groups, bryophyte and lichen richness
and plant life forms.
Altitudinal Level
I II III IV V
Altitude (m a.s.l.) 80 170 230 260 310
Vascular plants species richness 46 38 37 38 26
Functional groups
Tall shrubs 2 5 3 4 1
Shrubs 8 4 6 3 5
Dwarf shrubs 1 1 1 1 1
Evergeen ericoids 1 2 3 1 7
Forbs 28 23 19 26 5
Grasses 5 2 4 2 6
Ericoids 1 1 1 1 1
Bryophytes and lichens
Bryophytes 8 7 4 4 7
Lichens 0 0 0 0 21
Life forms
(meso +nano) Phanerophytes 9 8 8 6 6
Hemicryptophytes 21 15 15 20 9
Chamaephytes 7 9 8 7 9
Geophytes 5 2 3 2 2
Therophytes 2 3 2 2 0
Cryptophytes 1 1 1 1 0
Note: altitudinal level: I—river valley, II—middle part of the slope, III—upper limit of closed forest, IV—mountain
crooked forest, V—mountain shrub tundra.
The altitudinal level I is characterized by a closed north boreal forest in the Sob’ river valley,
with Picea obovata,Betula pendula and Larix sibirica.Duschekia fruticosa and occasional Sorbus sibirica
Hedl. shrubs are dominated by Ribes rubrum L. and scattered Betula nana,Juniperus communis L.,
Lonicera caerulea L., Rosa acicularis Lindl., Salix phylicifolia and Vaccinium uliginosum. Among the
dwarf shrubs, Atragene sibirica L. and Vaccinium vitis-idea L. are present. The dominant grasses are
Calamagrostis sp., Equisetum arvense,Geranium pretense L. Dominant mosses are Hylocomium splendens
(Hedw.) Bruchetal and Dicranum spp.
In the middle part of the slope (altitudinal level II), communities of closed north boreal forest
with Larix sibirica and Picea obovata are dominating. The understory consists of Betula pendula,
Duschekia fruticosa,Salix phylicifolia and Sorbus sibirica. The shrub layer is formed by Linnaea borealis L.,
and single Lonicera caerulea,Ribes rubrum,Rosa acicularis. Dominant shrubs are Andromeda polifolia,
Vaccinium myrtillus, and V. vitis-idea. The dominant herbs are Aconitum septentrionale,Calamagrostis sp.,
J. Fungi 2020,6, 353 10 of 22
Chrysosplenium sibiricum (Ser. ex DC.) A.P. Khokhr., and Dryopteris carthusiana. Dominant mosses are
Dicranim spp. and Hylocomium splendens,Polytrichum spp., Sanionia uncinata (Hedw.) Loeske.
In the upper limit of the closed forest (altitudinal level III), Larix sibirica dominates, with only
single individuals of Picea obovata. The undergrowth consists of Duschekia fruticosa and Sorbus sibirica.
The shrub layer is unevenly formed from Betula nana, singly Linnae aborealis,Lonicera caerulea,
Rosa acicularis,Salix pyrolifolia. Shrubs are represented by Empetrum hermaphroditum,Ledum palustre L.,
Vaccinium myrtillus,V. vitis-idea. The dominating herbs are Aconitum septentrionale,Calamagrostis sp.,
Cardamine amara L. and Poa sp. The ground cover is formed by mosses of the genera Dicranim,
Polytrichum and by Hylocomium splendens.
The crooked forest belt (altitudinal level IV) consists of larch and spruce, and thickets of
Duschekia fruticosa and Salix hastata L. Betula nana and Salix phylicifolia are present in the shrub layer.
Among the shrubs, the most abundant ones are Vaccinium myrtillus and V. vitis-idea. In the thickets
of Duschekia fruticosa and Salix hastata, the shrub layer is missing. The dominant grass species at
this altitude level are Aconitum septentrionale,Calamagrostis sp., Cardamine amara,Equisetum arvensis,
Rubus saxatilis L. Genus Dicranim,Mnium, and Hylocomium splendens dominate among the mosses.
The mountain-tundra belt (altitudinal level V) is a shrub tundra with grasses, lichens and mosses,
as well as a hilly bog. In the communities of the mountain-tundra belt, Larix sibirica,Picea obovata
and Duschekia fruticosa occur as single trees. Betula nana and Vaccinium uliginosum, and scattered
Salix phylicifolia form the shrub layer. Among the shrubs, Andromeda polifolia,Empetrum hermaphroditum
and Ledum decumbens dominate. The dominant grasses are Bistorta major Gray., Calamagrostis sp.,
Rubus chamaemorus. Dominant mosses are Hylocomium splendens,Ptilidium ciliare,Sphagnum sp.
Among the lichens, the most abundant ones are Cladonia amaurocraea (Flörke) Schaer, C. arbuscula
(Wallr.) Flot., C. rangiferina (L.) FH Wigg., C. stygia (Fr.) Ruoss, C. uncialis (L.) Weber ex FH Wigg.
The vertical distribution of vegetation on the studied mountain is similar to the neighboring mountain
ranges [13].
All investigated plant communities had a well-developed projective ground cover (>80%).
The largest proportion of litter and undergrowth (up to 17%) was found in the lower part of the
mountain forest belt. Rock outcrops were only found in the mountain tundra belt. Insignificant areas
of bare soil (0.7–3.6%) were identified at all levels (Table S2).
The tundra belt had the smallest cover of grass-dwarf shrub layer (F (4.18) =9.40; p<0.01); otherwise
there were no dierences in projective cover between dierent altitudinal levels. Tundra phytocenoses
had a significantly lower projective cover of grass than any other studied level (
F (4.18) =25.01
;
p<< 0.01
). Here, the largest projective cover of the moss-lichen layer was 90–100% (
F (4.18) =8.55
;
p<0.01
), and only in these communities did lichens contribute to layer formation (PP up to 50%)
(F (4.18) =16.59; p<0.01). Moreover, there is a significantly higher projective cover of shrubs
(
F (4.18) =3.88
;
p=0.02
) and evergreen ericoid plants (F (4.14) =3.25; p=0.04) in the tundra, while the
share of forbs (
F (4.18) =9.48
;p<0.01) and cereals (F (4.18) =4.08; p=0.02) is minimal. The maximum
cover of forbs was found in the upper part of the mountain forest (F (4.18) =9.48;
p<0.01
). In the
middle part of the mountain-forest belt, the maximum coverage of grasses (F (4.18) =0.08;
p=0.02
)
and ericoid plants (
F (4.6) =0.83;
p=0.01) occurred. Ground lichens are absent in forest communities.
The main parameters of the projective cover of the grass-shrub and moss-lichen cover on the Slantsevaya
mountain are similar to those of other studied mountains on the eastern slope of the Polar Urals [
32
,
33
].
The distribution of dierent life forms of plants correlates with the distribution of functional
groups. The plant communities of the tundra belt have a high proportion of nanophanerophytes
(
F (4.13) =5.63
;p=0.01) (Table S2). The smallest proportion of hemicryptophytes was found in
the tundra communities and floodplain forests (F (4.18) =12.44; p<0.01). Floodplain forests had
significantly higher proportions of geophytes than the other altitudinal levels of tundra and the
upper and lower levels (F (4.14) =4.75; p=0.01). Tundra communities have the lowest proportion of
therophytes compared floodplain forests (F (4.13) =1.92; p=0.03), and also have significantly lower
proportions of cryptophyte to forests communities at lower levels (F (4.11) =1.60; p=0.03).
J. Fungi 2020,6, 353 11 of 22
Evergreen ericoid plants form significantly higher phytomass in tundra communities than in
forest communities of dierent altitudes (F (4.8) =8.40; p=0.01), and the proportion of fallen branches
and cones is also significantly lower here (F (4.11) =11.98; p<0.01). Grasses form the highest biomass
in mid-level phytocenoses (F (4.9) =4.74; p=0.03) (Table 2).
Table 2. Vascular plant aboveground biomass (g/m2) of dierent functional groups and life forms.
Altitudinal Level
I II III IV V
Functional group
Tall shrubs +
Shrubs 7.8 ±0 2.2 ±0.8 9 ±3.8 5.7 ±4 13.8 ±4.6
Dwarf shrubs 6.4 ±4.8 144.4 ±0 0.2 ±0 0 44.6 ±41.7
Evergreen ericoids 39.2 ±10.4 5 ±3.8 1.2 ±1 0 70.2 ±14.9
Ericoids 9.6 ±0 28.2 ±2.5 26.2 ±0 36.2 ±33.4 0
Grasses +Forbs 75.1 ±16.1 425.4 ±230.6 134.9 ±49.2 165.5 ±38.8 7.7 ±1.6
Life form
(meso +nano)
Phanerophytes 7.6 ±3.6 0 57.6 ±47.2 0 49.7 ±17.6
Hemicryptophytes 29.7 ±7.2 140 ±106.5 81.9 ±17.3 102.9 ±38 6.6 ±1.5
Chamaephytes 38.4 ±17.8 348.9 ±163.8 70.1 ±52.7 81 ±20.9 103.6 ±44
Geophytes 60.4 ±13.4 25.2 ±22.6 71.2 ±32.6 31 ±19.7 14.8 ±14
Therophytes 12.8 ±6.7 7.8 ±5.4 13 ±2.2 3.6 ±0 0
Cryptophytes 0.1 ±0 0 0 0.7 ±0.3 3.2 ±0
Note: altitudinal level: I—river valley, II—middle part of the slope, III—upper limit of closed forest, IV—mountain
crooked forest, V—mountain shrub tundra.
The biomass fraction of meso- and nanophanerophytes is maximum in the middle level of forests,
and is minimum in the phytocenoses of the lower levels (F (4.8) =6.1; p=0.02). The cryptophyte biomass
decreases significantly with the transition from the tundra to the upper forest line, and from the upper
forest line to other investigated levels of mountain forests (F (4.7) =27.94; p<0.01). The maximum
biomass of hemicryptophytes was found at level II (Table S3). The distribution of plant biomass along
mountain belts is similar to the indicators established for other East-European Subarctic mountain
regions [34].
3.2. Trees
With the increasing altitude, the tree species richness decreases (macrophanerophyts): six species
were found in the river valley, four at timberline, and only two species in the mountain tundra
(Larix sibirica and Picea obovata). The average morphometric and areal characteristics of the tree stands
decrease with altitude (Table S4). For the two most common tree species in the area (L. sibirica and
P. obovata), the average base diameter decreases by a factor of 3, height by a factor of 6, age by a factor
of 3 and crown density by a factor of 9.
With the increasing altitude, the proportion of larch by a factor of 2 and the aboveground biomass
of forest stands decreases by a factor 58. In the floodplain of the Sob’ river, a significant proportion of
birch is present in the stand, making up almost half of all trees (Table S5). This explains the proportional
decrease in the biomass of larch and spruce in this site.
Plant biomass prevails over mortmass at all forest levels of the transect (forests: 3.33–2.67 times
higher), but mortmass prevails in the tundra (3.8 times higher). The sum of the plant biomass with the
mortmass gives the total aboveground phytomass, which decreases with altitude by 3 times (Table 3).
J. Fungi 2020,6, 353 12 of 22
CWD and FWD form more than half of the whole mortmass at lower altitudinal levels, but in the
mountain tundra only 2%, whereas litter biomass is absolutely dominating.
Table 3.
Distribution of aboveground plant mortmass, biomass and total phytomass (t/ha) along the
altitudinal gradient.
Altitudinal Level
Parameter I II III IV V
Plant mortmass
CWD 9.6 10.7 8.5 7.1 0.2
FWD 9.5 8.7 7.5 6.6 0.7
Litter 16.5 20.0 22.5 28.9 45.5
Sum: 35.6 39.4 38.5 42.6 46.4
Plant biomass
Alive trees 107.7 114.6 102.25 100.67 1.73
Grasses +bushes 9.33 15.32 7.11 6.54 5.23
Lichens +mosses 1.62 0.31 0.56 0.35 6.56
Sum: 118.65 130.33 116.48 113.75 12.19
Ratio plant biomass/mortmass 3.33 3.31 3.02 2.67 3.81
Total aboveground phytomass
Sum of plant biomass and mortmass 154.25 169.73 154.98 156.35 58.59
Note: altitudinal level: I—river valley, II—middle part of the slope, III—upper limit of closed forest, IV—mountain
crooked forest, V—mountain shrub tundra. CWD—coarse woody debris; FWD—fine woody debris.
The total mortmass of CWD and FWD is similar at all forest levels due to the small number of dead
trees. Coarse woody debris (CWD) is significantly lower in the taiga compared to forests. In the study
area, CWD decreases by a third from the valley to the upper forest boundary, and in the mountain
tundra, there is a sharp drop to almost zero t/ha (Table 3). Fine wood debris (FWD) dropped by almost
2/3, in the tundra even to 0.7 t/ha (due to the presence of dead branches of willow and birch). In the
mountain tundra, the FWD was higher than the CWD. The highest litter mass is produced in the tundra
(especially hummock bogs), where it is almost three times higher than in the valley forests. The sum of
the plant biomass with the mortmass gives the total aboveground phytomass, which decreases with
altitude by a factor 3 (Table 3).
A similar trend was reported for zonal plant communities during the transition from northern
forests to forest-tundra and subarctic tundras [
35
]. Here, CWD and FWD accounted for 54% of mortmass
at lower altitudinal levels, but for only 2% in the mountain tundra. On the other hand, the litter mass
in the tundra accounted for 98% of the mortmass, and decreased to 46% in the valley. Plant biomass
prevails over mortmass at all forest levels of the transect (factor 3.33–2.67), but mortmass reaches
the highest ratio at the mountain-tundra level (factor 3.81). The excess of mortmass over biomass
is also shown in some high-altitude communities of the Altay-Sayan mountains [
36
,
37
], the tundra
communities of Fennoscandia [38], and the zonal tundra habitats of the Yamal peninsula [39].
3.3. Fungi
During research in 2020, 18 new species of aphyllophoroid fungi were identified for the study areas:
Athelia bombacina (Link) Pers., Botryobasidium botryosum (Bres.) J. Erikss., B. laeve (J. Erikss.) Parmasto,
Clavicorona taxophila (Thom) Doty, Datronia mollis (Sommerf.) Donk, Gloeocystidiellum leucoxanthum
(Bres.) Boidin, Hydnum rufescens Pers., Hyphodontia arguta (Fr.) J. Erikss., H. breviseta (P. Karst.)
J. Erikss., Kavinia alboviridis (Morgan) Gilb. & Budington, Leptosporomyces fuscostratus (Burt) Hjortstam,
J. Fungi 2020,6, 353 13 of 22
Phanerochaete laevis (Fr.) J. Erikss. & Ryvarden, Phlebia nitidula (P. Karst.) Ryvarden, Phlebiella borealis
K.H. Larss. and Hjortstam, Polyporus choseniae (Vassilkov) Parmasto, Thelephora caryophyllea (Schae.)
Pers, Tomentella stuposa (Link) Stalpers, Tomentellopsis echinospora (Ellis) Hjortstam (Table S1).
Taking into account the whole 60-year investigation period at the Slantsevaya mountain, a total of
281 aphyllophoroid fungal species were identified in an area of only 10 km
2
[
9
]. Together with fungi
collected in areas with a anthropogenic impact only [
40
42
], the total number is 294 species. Thus,
this site is certainly one of the best studied northern areas in Russia concerning aphyllophoroid fungi.
For comparison, 400 species are known from the Murmansk province (north of the Arctic Circle) on
an area of 145,000 km
2
[
43
], and 550 species were reported from mid-boreal forests of the Republic of
Karelia on 172,400 km2[44].
On the investigated altitudinal gradient, 157 species were identified (Table S1). The number of
fungal species is significantly negatively correlated with altitude (rs=0.9, p=0.037): from the river
valley towards the tundra, the number of aphyllophoroid fungal species decreases from 106 to 30
(Table 4). The same general dynamics was also observed for the morphological forms of aphyllophoroid
fungi (Figure 5A). However, morphological forms showed dierent dynamics depending on altitudinal
level (Figure 5B). Thus, the proportion of clavarioid fungi is maximally positively associated with
altitude (r
s
=0.97, p=0.0048), and that of poroids is strongly negatively correlated to it (r
s
=
1.0,
p<0.001
). No correlation was found for corticoid fungi (r
s
=0.21, p=0.74), although this parameter
decreases within the forest zone towards the lowlands (from 49.1% to 36.7%), and is strongly correlated
with altitude (rs=1.0, p<0.001).
Table 4.
Species richness and proportion (%) of aphyllophoroid fungi belonging to dierent
morphological forms, to dierent ecological strategies, having dierent substrate preferences or
with dierent fruitbody size groups.
Altitudinal Level
I II III IV V
Altitude (m a.s.l.) 80 170 230 260 310
Species richness 90 106 84 55 30
Morphological form
Corticioids 33/36.7 42/39.6 35/41.7 27/49.1 11/36.7
Poroids 29/32.2 29/27.4 22/26.2 8/14.5 1/3.3
Clavarioids 28/31.1 35/32.1 27/32.1 20/36.4 18/60.0
Ecological strategy and substrate groups
Saprobs 110/87.4 131/88.4 107/90.7 70/90.9 29/91.9
Wood 56/45.5 68/45.9 55/46.6 35/45.4 8/23.5
Litter 47/36.2 53/35.8 44/37.3 31/40.3 18/53.5
Soil 7/5.7 10/6.7 8/6.8 4/5.2 3/9.1
Parasites 5/3.9 5/3.5 3/2.5 2/2.6 1/2.6
Symbionts 11/8.7 12/8.1 8/6.8 5/6.5 3/5.5
Fruitbody size
I 16/48.0 19/51.3 17/62.9 14/70.0 16/88.8
II 13/40.4 15/40.6 10/37.1 6/30.0 2/11.2
III 4/11.6 3/8.1 0 0 0
Note: altitudinal level: I—river valley, II—middle part of the slope, III—upper limit of closed forest, IV—mountain
crooked forest, V—mountain shrub tundra.
J. Fungi 2020,6, 353 14 of 22
J. Fungi 2020, 6, x FOR PEER REVIEW 14 of 22
Figure 5. Relationship between aphyllophoroid fungal species richness at different
altitudinal levels (I–V) and the structure of the mycobiota. (A) Species richness of fungal
morphological groups (corticoid, poroid, clavarioid); (B) Proportion of fungal
morphological groups; (C) Species richness of fungal ecological groups (wood, litter or soil
saprobes, parasites, mycorrhizal); (D) Proportion of fungal ecological groups.
3.4. Biotic Factors Influencing Aphyllophoroid Species Richness
3.4.1. Plant Diversity
Aphyllophoroid fungal species richness is not correlated to plant diversity (rs = 0.05, p = 0.93)
(Figure 6A). However, a positive correlation was found between aphyllophoroid fungal species
richness and richness of tree species (rs = 0.95, p = 0.013), but there was no relationship to forbes and
grass species richness (p = 0.39 and 0.56, respectively). Moreover, a reliable relationship was detected
between aphyllophoroid fungal species richness and therophytes (rs = 0.89, p = 0.04), and poroid
fungal species were a significantly correlated with mesophanerophyte (rs = 0.83, p = 0.02) and tree
diversity (macrophanerophyes) (rs = 0.95, p = 0.014). Moreover, clavarioid fungal species richness
was significantly related to tree species richness (macrophanerophyes) (rs = 0.84, p = 0.005), while no
such correlation was found for corticioids. With an increase in the proportion of phanerophytes, the
proportion of clavarioids decreases, which is similarly shown for the Urals in the natural zones of
the subzones [10]. The number of clavarioids is related to the number of geophyte species (rs = 0.84, p
= 0.005). The number of tree species is most strongly related to the number of parasitic and
wood-destroying fungi (p = 0.01), and with the sum of all saprobes (rs = 0.81, p = 0.05). Moreover, the
number of species of height group 3 (high-size fruitbodies) is positively associated with the number
of tree species (p = 0.03).
Figure 5.
Relationship between aphyllophoroid fungal species richness at dierent altitudinal levels
(I–V) and the structure of the mycobiota. (
A
) Species richness of fungal morphological groups (corticoid,
poroid, clavarioid); (
B
) Proportion of fungal morphological groups; (
C
) Species richness of fungal
ecological groups (wood, litter or soil saprobes, parasites, mycorrhizal); (
D
) Proportion of fungal
ecological groups.
The diversity of individual morphological forms of aphyllophoroid fungi changes in a clear
correlation with altitude, even though the most species-rich altitudinal level is level II and not I.
3.4. Biotic Factors Influencing Aphyllophoroid Species Richness
3.4.1. Plant Diversity
Aphyllophoroid fungal species richness is not correlated to plant diversity (r
s
=
0.05, p=0.93)
(Figure 6A). However, a positive correlation was found between aphyllophoroid fungal species richness
and richness of tree species (r
s
=0.95, p=0.013), but there was no relationship to forbes and grass
species richness (p=0.39 and 0.56, respectively). Moreover, a reliable relationship was detected
between aphyllophoroid fungal species richness and therophytes (r
s
=0.89, p=0.04), and poroid
fungal species were a significantly correlated with mesophanerophyte (r
s
=0.83, p=0.02) and tree
diversity (macrophanerophyes) (r
s
=0.95, p=0.014). Moreover, clavarioid fungal species richness
was significantly related to tree species richness (macrophanerophyes) (rs=0.84, p=0.005), while no
such correlation was found for corticioids. With an increase in the proportion of phanerophytes,
the proportion of clavarioids decreases, which is similarly shown for the Urals in the natural zones of
the subzones [
10
]. The number of clavarioids is related to the number of geophyte species (
rs=0.84
,
p=0.005). The number of tree species is most strongly related to the number of parasitic and
wood-destroying fungi (p=0.01), and with the sum of all saprobes (r
s
=0.81, p=0.05). Moreover,
the number of species of height group 3 (high-size fruitbodies) is positively associated with the number
of tree species (p=0.03).
J. Fungi 2020,6, 353 15 of 22
J. Fungi 2020, 6, x FOR PEER REVIEW 15 of 22
Figure 6. Vascular plant richness, fungal richness and total mortmass at different altitudinal
gradients I–V. (A) 1—Vascular plant species richness; 2—Fungal species richness; (B) 1—Total
mortmass; 2—Species richness of saprobic aphyllophoroid fungi.
3.4.2. Altitudinal Levels
The richest aphyllophoroid mycobiota occurred in levels I and II, with highest crown density
indices (rs = 0.9–0.95, p = 0.002), and the highest values of CWD and FWD. In contrast, thereto has
tundra with the poorest aphyllophoroid fungal communities, which appeared to be related to the
low crown density, minimal mortmass of CWD and FW and the highest amounts of lichen, moss and
litter biomasses (Table 3).
Altitudinal levels had a large impact on fungal community structure: the most antagonistic
characteristics were found between the altitudinal levels V (tundra) and II (the closest forest stand)
(Figure 7), where distinct differences in fungal morphological forms were detected. The poorest
fungal communities were found in the altitudinal level V with richest lichen diversity. Axis 1 in the
ordination represents stock characteristics and the stand density of forest communities. Level II,
located in the middle part of the mountain slope, is the oldest north-boreal coniferous forest with the
highest tree crown densities (80–90%) and high amounts of woody biomass (>130 t/ha). The
aphyllophoroid species richness of altitudinal level II was shaped by a maximum species richness of
grasses and bushes, and the highest amounts of CWD and FWD.
The aphyllophoroid fungal species richness in altitudinal level V, in which litter saprobs are
clearly dominating, can be explained by the high litter mortmass and the high biomass of lichens and
bryophytes (Figure 8). In the tundra, biomass is generally low and consists of thin twigs and leaves
and individual blades of grass. This resulted in a prevalence of small-size fruitbodies.
Figure 6.
Vascular plant richness, fungal richness and total mortmass at dierent altitudinal gradients
I–V. (
A
) 1—Vascular plant species richness; 2—Fungal species richness; (
B
) 1—Total mortmass;
2—Species richness of saprobic aphyllophoroid fungi.
3.4.2. Altitudinal Levels
The richest aphyllophoroid mycobiota occurred in levels I and II, with highest crown density
indices (r
s
=0.9–0.95, p=0.002), and the highest values of CWD and FWD. In contrast, thereto has
tundra with the poorest aphyllophoroid fungal communities, which appeared to be related to the low
crown density, minimal mortmass of CWD and FW and the highest amounts of lichen, moss and litter
biomasses (Table 3).
Altitudinal levels had a large impact on fungal community structure: the most antagonistic
characteristics were found between the altitudinal levels V (tundra) and II (the closest forest stand)
(Figure 7), where distinct dierences in fungal morphological forms were detected. The poorest fungal
communities were found in the altitudinal level V with richest lichen diversity. Axis 1 in the ordination
represents stock characteristics and the stand density of forest communities. Level II, located in the
middle part of the mountain slope, is the oldest north-boreal coniferous forest with the highest tree
crown densities (80–90%) and high amounts of woody biomass (>130 t/ha). The aphyllophoroid species
richness of altitudinal level II was shaped by a maximum species richness of grasses and bushes,
and the highest amounts of CWD and FWD.
The aphyllophoroid fungal species richness in altitudinal level V, in which litter saprobs are
clearly dominating, can be explained by the high litter mortmass and the high biomass of lichens and
bryophytes (Figure 8). In the tundra, biomass is generally low and consists of thin twigs and leaves
and individual blades of grass. This resulted in a prevalence of small-size fruitbodies.
J. Fungi 2020,6, 353 16 of 22
J. Fungi 2020, 6, x FOR PEER REVIEW 16 of 22
Figure 7. Relationship of the richness of morphological groups of fungi with biomass and
mortmass of vegetation. Axis 1—biomass of the tree layer, Axis 2—morphological groups
of fungi
. I–V represent the altitudinal levels.
3.4.3. Plant Biomass
Due to the heterotrophic nutritional mode of aphyllophoroid fungi, it would be obvious to
assume a close relationship between the species richness of saprobic fungi and the amount of
mortmass. However, such a relationship was not found (r
s
= 0.7, p = 0.188) (Figure 6B), nor was
mortmass related to the total number of aphyllophoroid fungi (r
s
= 0.68, p = 0.236).
Figure 8. Relationship between different ecological groups of fungi or groups with substrate
preference with plant biomass and mortmass in the altitudinal levels (I–V).
Figure 7.
Relationship of the richness of morphological groups of fungi with biomass and mortmass of
vegetation. Axis 1—biomass of the tree layer, Axis 2—morphological groups of fungi. I–V represent
the altitudinal levels.
J. Fungi 2020, 6, x FOR PEER REVIEW 16 of 22
Figure 7. Relationship of the richness of morphological groups of fungi with biomass and
mortmass of vegetation. Axis 1—biomass of the tree layer, Axis 2—morphological groups
of fungi
. I–V represent the altitudinal levels.
3.4.3. Plant Biomass
Due to the heterotrophic nutritional mode of aphyllophoroid fungi, it would be obvious to
assume a close relationship between the species richness of saprobic fungi and the amount of
mortmass. However, such a relationship was not found (r
s
= 0.7, p = 0.188) (Figure 6B), nor was
mortmass related to the total number of aphyllophoroid fungi (r
s
= 0.68, p = 0.236).
Figure 8. Relationship between different ecological groups of fungi or groups with substrate
preference with plant biomass and mortmass in the altitudinal levels (I–V).
Figure 8.
Relationship between dierent ecological groups of fungi or groups with substrate preference
with plant biomass and mortmass in the altitudinal levels (I–V).
3.4.3. Plant Biomass
Due to the heterotrophic nutritional mode of aphyllophoroid fungi, it would be obvious to assume
a close relationship between the species richness of saprobic fungi and the amount of mortmass.
However, such a relationship was not found (r
s
=
0.7, p=0.188) (Figure 6B), nor was mortmass
related to the total number of aphyllophoroid fungi (rs=0.68, p=0.236).
J. Fungi 2020,6, 353 17 of 22
A relationship was detected only between for certain trophic (substrate) groups of fungi and
certain mortmass fractions. For example, the number of corticoid, poroid and clavarioid fungi was
closely related to CWD and FWD (p<0.05), while clavarioids were strongly related to litter mortmass
(r
s
=0.97, p=0.004), showing the strongest positive correlation (r
s
=1, p=0) when considering
proportions (proportion of litter to the total mortmass and proportion of clavarioid species to the total
number of aphyllophoroid fungi).
Aphyllophoroid fungal species richness was clearly related to biomass (r
s
=1, p<0.001), but no
relationship was found between the number of fungal species and the total aboveground plant biomass
(r
s
=0.6, p=0.284). A significant positive relationship exists to total aboveground biomass (
rs=0.9
,
p=0.037).
Wood-decaying fungi were significantly correlated to the amounts of CWD and FWD (
rs=1.00
,
p<0.001), while litter saprobes were strongly correlated to litter mortmass (r
s
=0.9, p=0.037).
The proportion of wood-decaying saprobes was stable at all four altitudinal levels with forests
(45.4–46.6%).
The biomass of living trees was also positively correlated to the richness of fungal species with
large-size fruitbodies (p<0.001). Due to the higher biomass, there were significantly more fungal
species of the III height group at the bottom of the mountain (F (4.13) =5.63; p=0.01).
The dierence between the aphyllophoroid communities occurring in the treeless tundra and
in the boreal zone can be summarized as follows. In the poorest level, the tundra, litter-inhabiting
clavarioids with small-size basidiomata (I height group), are highly represented (48% of the total
species), while other ecological and morphological groups of fungi do not exceed 7% of the total species.
In contrast, in the richest boreal level II, the ecological and morphological groups of aphyllophoroids
are more evenly distributed: wood-inhabiting corticioids and poroids (31% and 25%, respectively),
and litter-inhabiting clavarioids with middle-size basidiomata (II height groups) (19%). Saprobes are
dominating at all altitudes, while, as expected, the richness of mutualistic symbionts or parasites is
generally low in this subarctic study site.
4. Discussion
This study proved the hypothesis that aphyllophoroid fungal species richness is generally
decreasing with altitude, as is also reported from other parts of the Urals [
9
]. However, altitude is
not always related to the number of fungal species, as this also depends on the scale and structure
of the investigated area. In an earlier study carried out in an adjacent mountain of the Polar Urals,
we examined forest areas (20
×
20 m) with crown densities of 70–80%, and a CWD volume of about
100 t/ha, and compared them to several areas in the middle and lower parts of the slope, where open
meadows and wetlands were predominating, and CWD was 20 t/ha. Here, species richness was
significantly lower in lowlands compared with the upper part of the forest belt [
10
]. Similar results
have been shown in other studies [
45
]. Thus, aphyllophoroid fungal species richness is also related to
the structure of the forest, and to the amount of CWD.
Moreover, the other hypotheses we tested were largely confirmed. As hypothesized, fungal
species richness negatively correlates with altitude. The highest species richness was detected in
old-growth forests with a maximum crown density. A direct relationship between plant richness
and aphyllophoroid richness was not found. However, the study confirmed close correlations for
individual ecological groups, e.g., for tree species richness and wood-destroying fungi, or for geophytes
and clavarioid fungi. We also proved that both the richness of wood-decaying fungi, and the richness
of fungi-forming large fruitbodies, correlates to wood volume.
4.1. Why Is Plant Diversity Highest at the Slopes of the Mountains?
The richness of aphyllophoroid fungi was highest at lower altitudinal levels, and was gradually
decreasing from the slopes to the tundra. At first glance it appears strange that species diversity is
lower in the river valley than at the slopes. However, this can be explained by the typical structure
J. Fungi 2020,6, 353 18 of 22
of this pristine river valley, as the ground is largely covered with mosses and horsetail. Over the
past 15 years, its swampiness has increased due to an increase in precipitation, increase permafrost
thawing depth and increasing amounts of water running down the slopes into the valley. This explains
why optimal conditions for the aphyllophoroid communities are rather found on the middle slope
of the mountain. Here, the conditions are optimal due to an ideal SW exposure, drainage and no
stagnation of cold valley air, and a maximal plant richness (especially of trees, shrubs, grasses and
forbs). On the slopes, soil permafrost has been thawing fastest over the last 35 years, thus resulting in
high soil microbial activities [
9
]. This is reflected by the maximum number of aphyllophoroid species
growing on soil in these areas (humus saprobic and ectomycorrhizal species like Ramaria, Hydnum,
Thelephora spp.), and by the recent “invasion” of “southern forest” species (Polyporus umbellatus (Pers.)
Fr., Osteina obducta (Berk.) Donk, Coltricia perennis (L.) Murrill).
4.2. Is Fungal Diversity Positively Correlated to Plant Diversity?
Richness of tree species appears to be a key factor for aphyllophoroid fungal species richness.
The number of tree species is strongly related to the richness of poroid fungi, to the richness of plant
parasitic fungi and to richness of corticoid fungi. This is probably all because of the strong dependence
of these fungi on plant biomass. Due to the higher biomass, there are significantly more fungi with
large fruitbodies at the bottom slopes of the mountain. A similar trend was shown for clavarioid
fungi along the entire Ural latitudinal-zonal transect [
46
]: the proportion of clavarioid species of
the III height group increases to a maximum in the direction from the tundra to hemiboreal forests,
while clavarioid species of the I height group decreases to a minimum. As shown on the Slantsevaya
mountain, negatively geotropic fungi, like stipitate Hydnum, Thelephora, Cantharellus, Polyporus, etc.,
are also following this trend.
Species richness of saprobial fungi is not related to the amount of mortmass. There are several
hypotheses which might explain this. We assume contrasting trends in dierent altitudinal levels to be
the main reason for this paradox: in the lower part of the slope with CWD and FWD as predominating
mortmass, this relationship is clearly positive; however, higher up the slope, where litter, grass,
lichens and mosses predominate mortmass, this relationship is negative. Further research is needed to
prove this hypothesis.
4.3. The subarctic as a Model for Biotic Factors Influencing Aphyllophoroid Fungal Communities
The tree species dominating in the studied subarctic region is Siberian larch, and the main
undergrowth is mountain green alder [
2
]. Decomposition rates of Larix wood are important ecological
factors for ecosystem development and changes in subarctic regions [
47
]. The study area almost
represents the western border of the “Siberian” range of these two tree species. West of the Urals,
the green alder bushes disappear from the undergrowth, and also Siberian larch sharply reduces its
coenotic role; its westernmost locations are in the White Sea region. A modeling-based prediction of
future changes in similar areas is extremely interesting and could also be economically important.
In the upper part of the closed forest, the basis of the biomass is formed by larch (and green
alder), but as soon as spruce and large birch appear, the number of wood-destroying fungal species
increases and reaches a maximum in areas with the highest species richness of trees and bushes and
with the maximal CWD and FWD. Thanks to the appearance of spruce, CWD increased by only 7.6 t/ha
(6.6% of the total woody biomass formed by three tree species, see Table S4), but this was enough
for a significant increase in the species richness of wood-destroying fungi. Thus, the number of tree
species turned out to be an important predictor for the species richness of poroid fungi growing on
rotting logs, as well as for their share of the total number of species. In Siberian subarctic forests,
fungal species richness generally strongly depends on the forest type (conifers vs. deciduous trees),
and on the presence of single tree species [
48
,
49
]. The identity of tree species can even be the main factor
shaping the composition of wood-decaying fungi [
11
]. The overall amount and diversity of deadwood
(including the role of dierent tree species) is a major factor shaping the diversity of wood-decaying
J. Fungi 2020,6, 353 19 of 22
fungi [
50
56
]. In addition, the size of the wood explains the diversity of fungi belonging to dierent
morphological or functional groups: as is convincingly shown in this study, species richness of poroid
fungi significantly depends on log size.
Despite the small size of the studied area, striking similarities were found with results from similar
large-scale studies [
10
]. On the 3000 km long Ural latitudinal transect, the maximum proportion of
poroid fungi (of the total number of aphyllophoroid species) corresponds to southern and hemiboreal
forests with the maximum crown density, stand age and species diversity of tree and shrub species,
while in open tundra regions their proportion is minimal. The maximum proportion of clavarioid
fungi was found in the “treeless” tundra regions, and it slowly decreases from the forest tundra to
hemiboreal regions. The proportion of corticoid fungi was maximal in the forest-tundra and was
slowly decreasing towards the hemiboreal forests. This confirms that the extensive data obtained in
this study in a small area are correct, and that conclusions are also valid for larger scales. This study
revealed and confirmed important factors shaping the mycobiota in subarctic regions, and is thus
forming a solid base for future large-scale studies and simulations.
5. Conclusions
Aphyllophoroid fungi represent all three main ecological groups of macromycetes, allowing them
to develop on the maximum possible spectrum of substrates available. In this regard, they can be
considered as a simple ecological model describing the principle fungal distribution in a simply
arranged, high-latitude forest ecosystem, at the polar limit of the taiga.
Strikingly, we discovered a ratio of 1:3–3.5 between the aphyllophoroid fungal species richness
of the tundra and the adjacent river-valley. The middle part of the slope appears to have optimal
conditions for these fungi, as the maximum species richness occurred here. However, fungal species
richness was not related to the species richness of plants or to mortmass in these habitats. The poorest
aphyllophoroid communities were related to the richest lichen communities in terms of lichens species
richness and biomass, as well as to evergreen ericoids and Sphagnum bogs.
The range of morphological and ecological groups of aphyllophoroid fungi occurring in the
tundra diers significantly from those occurring in forest. This shows that fungal communities are
highly influenced by various biotic factors such as substrate availability and substrate type. Most of
the detected fungi were wood saprobes, but also litter saprobial species were quite species-rich,
while humus saprobes, parasites and ectomycorrhizal aphyllophoroid fungi were comparatively rare.
At the arctic limit of forest distribution, the species richness of aphyllophoroid fungal communities
is determined by the amount of available dead wood, and with the growth of this resource, the proportion
(and absolute species richness) of poroid fungi increases. At the same time, the proportion of clavarioid
fungal species is higher in the tundra and decreases with an increase in the density of the forest crowns.
The higher the litter mortmass, the higher the proportion of clavarioid fungi and their species richness
in the aphyllophoroid communities becomes. The proportion of corticoid fungal species reaches a
maximum in crooked forests, and was negatively correlated to the biomass of woody plants. However,
the correlation of the species richness of aphyllophoroid fungi with the floristic richness and total
mortmass could not be established. This is an interesting result for aphyllophoroid macromycetes,
as their species richness and diversity were, up to now, traditionally associated with the availability of
substrate resources only.
Supplementary Materials:
The following are available online at http://www.mdpi.com/2309-608X/6/4/353/s1,
Figure S1. Location of five plots inside the altitudinal level. Table S1. Presence–absence of data for 157
aphyllophoroid fungal species found along the altitudinal transect “Slantsevaya mountain” in the Polar Urals
(from the Sob’ River valley, slopes of the Slantsevaya mountain to mountain shrub tundra) during the year 2020,
and characteristics of the species (ecological strategy, fruitbody type, height group). Table S2. Projective cover
(%) for dierent functional groups and life forms of vascular plants. Table S3. Distribution of biomass (t/ha) for
functional groups and life forms of vegetation along the altitudinal transect. Table S4. Mean and standard errors
of the main dendrometric parameters (for larch and spruce) within trial plots. Table S5. Characteristics of tree
stands (macrophanerophytes) at the first altitudinal level (Sob’ river valley). Data are given for the three most
common tree species.
J. Fungi 2020,6, 353 20 of 22
Author Contributions:
A.G.S. conceived and coordinated the overall project. A.G.S., U.P., S.Y.S., N.M.D. and
A.A.G. designed the sampling experiment. V.V.E. worked with satellite data. A.G.S., D.A.K., S.Y.S., N.M.D.,
A.A.G., O.S.S. and V.V.E. analyzed the data. A.G.S., U.P., S.Y.S, O.S.S., N.M.D. and A.A.G. wrote the manuscript.
All authors have read and agreed to the published version of the manuscript.
Funding:
The research was carried out with the financial support of the Russian Foundation for Basic Research
(project 18-05-00398 A) and FWF Micinsnow P-31038.
Acknowledgments:
We would like to thank the anonymous reviewers for their comments on an earlier version of
the manuscript. We very much appreciate the support provided by the administration of the Arctic Research
Station of the Institute of Plant and Animal Ecology UrB RAS (Labytnangi) for their miscellaneous assistance during
this research. We are deeply grateful to S.G. Shiyatov (Ekaterinburg), V.S. Mazepa (Ekaterinburg), P.A. Moiseev
(Ekaterinburg) and P.O. Drobyshev (Moscow) for providing personal information, as well as for assistance in data
processing and discussion of the results. We thank, for field work assistance, A.I. Ischenko (Chelyabinsk) and A.F.
Zubkov (Kharp).
Conflicts of Interest: The authors declare no conflict of interest.
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... Over the past century, in the Polar Urals, the average annual air temperature increased by 2 • C and the average annual precipitation increased by 88 mm, as a result of which the growing season has increased by 7 days. As a result of the above bioclimatic parameters, the upper border of the forest has risen by 40-60 m [15,16] (Figures S1 and S2: Table S1), and the biomass of woody plants has increased tenfold [15,17]. New, typically forest species of mosses and vascular plants have appeared [18][19][20][21]; borealization of the fauna is taking place [22]. ...
... The studies were carried out on the southwestern slope of Slantsevaya Mountain (N 66 • 54 ; E 65 • 44 ), located on the eastern macroslope of the Polar Urals [16], in the Yamal-Nenetsk Autonomous District (Figure 1). At its foot, in the valley of the Sob River (70 to 90 m a. s. l.), there are forest thickets representing northern boreal vegetation with a predominance of Larix sibirica Lebed., Picea obovata Lebed. ...
... Until now, there have been metal signs on the trees with the designation of the plot numbers, which helped us to identify the altitude level at which the studies were carried out in the 1960-1970s. There is an extensive list of publications [10][11][12][13][14][15][16], as well as a large amount of collection material. In 1996, participants in the Fifth International Symposium on Arcto-Alpine mycology worked here [23]. ...
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