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Citation: Shiryaev, A.G.; Zmitrovich,
I.V.; Bulgakov, T.S.; Shiryaeva, O.S.;
Dorofeyeva, L.M. Global Warming
Favors the Development of a Rich
and Heterogeneous Mycobiota on
Alien Vines in a Boreal City under
Continental Climate. Forests 2022,13,
323. https://doi.org/10.3390/
f13020323
Academic Editors:
Nadezhda Tchebakova and Sergey
V. Verkhovets
Received: 25 January 2022
Accepted: 11 February 2022
Published: 16 February 2022
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4.0/).
Article
Global Warming Favors the Development of a Rich and
Heterogeneous Mycobiota on Alien Vines in a Boreal City
under Continental Climate
Anton G. Shiryaev 1, * , Ivan V. Zmitrovich 2, Timur S. Bulgakov 3, Olga S. Shiryaeva 1
and Lyudmila M. Dorofeyeva 4
1Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences,
620144 Ekaterinburg, Russia; olga.s.shiryaeva@gmail.com
2V.L. Komarov Botanical Institute, Russian Academy of Sciences, 197376 St. Petersburg, Russia;
iv_zmitrovich@mail.ru
3
Federal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, 354002 Sochi, Russia;
fungi-on-don@yandex.ru
4Institute Botanic Garden, Ural Branch of the Russian Academy of Sciences, 620144 Ekaterinburg, Russia;
dorofeyeva.lm@gmail.com
*Correspondence: anton.g.shiryaev@gmail.com
Abstract:
The species richness and composition of macro- and microfungi on vine species in the
parks of Ekaterinburg City (the Ural macroregion, Russia) located in the southern boreal vegetation
subzone in a continental climate was studied. The average annual air temperature has increased
by 3.1
◦
C since the beginning of the 20th century; therefore, the conditions for the growth of vines
have improved. These conditions include warmer winters and, consequently, less frost damage to
perennial plants. Due to the warmer climate, the area of vines grown in the city has increased five
times over half a century, and the yield of grapes has grown 3.7 times. The alien East Asian vines
are the most dominate vine species cultivated, while European, North American, and native plant
species, including archaeophytes, together only represent a handful of the species cultivated. At the
same time, 65% of the area of woody vines in the city is covered by a North American species, namely
Parthenocissus quinquefolia. An increase in the number of vine species, their biomass, and covered
areas contributes to an increase in the number of fungal species growing on these vine species. In total,
81 species of phytopathogenic and 87 species of saprobic macro- and microfungi have been recorded
during the century-long history of mycological research in Ekaterinburg City. Mycobiota of vines in
Ekaterinburg City is biogeographically heterogeneous and 1.1–3.2 times richer in comparison with
ones of the regions located on the northern limit of natural ranges of the vines. Recorded macrofungi
(Basidiomycota) are predominantly present on native boreal species; however, some exotic tropical
and subtropical East Asian fungal species (that have not ever been recorded on other substrates in
the natural forests of the Urals and Siberia) are found here too. Recorded microfungi are highly
specialized vine-associated species (mainly Ascomycota) that are widespread within the natural
ranges of the vines and absent in the boreal zone of Eurasia: there are 63 vine-associated species
(15 macro- and 48 microfungi) in Ekaterinburg that are not found in the Urals on other substrates.
Many of these species have been recorded for the first time in this study, so we consider that they
invaded Ekaterinburg City in the last 20 years, likely due to the warming climate observed over
the last decades in the region. There are 19 and 32 species of phytopathogenic fungi collected in
the families Cucurbitaceae and Vitaceae, respectively. During the past 40 years, the recorded fungal
species richness has increased by 16% on Cucurbitaceae, as well as 37% on grapes. In this study, the
distribution of vine-associated fungi, including phytopathogenic fungal species, from the nearest
regions of ancient vine culture (Southern European Russia and the Caucasus, Central Asia, the south
of the Russian Far East) to the boreal regions of the Urals were investigated. The increase in the
range of these phytopathogenic fungal species can lead to significant economic losses to the regional
agricultural sector.
Forests 2022,13, 323. https://doi.org/10.3390/f13020323 https://www.mdpi.com/journal/forests
Forests 2022,13, 323 2 of 22
Keywords:
climate change; disturbance; urban ecology; alien plants; biological resources; northern
viticulture; plant pathogens; biogeography; fungal diversity; vitis; liana
1. Introduction
Vines (lianas) play an important role in modern cities, acting as the main elements of
vertical urban landscapes, and help cultivate an optimal microclimatic environment [
1
,
2
].
Due to global warming, vines are becoming more commonly used in the cities of North
Eurasia that exhibit ultra-continental climates, such as the macroregions of Ural and Siberia
in Russia [3].
Vines are a very common plant life form in the tropical and subtropical regions of
Earth, where a high amount of vegetation and biodiversity can be found as well as an
overproduction of biomass and a deep differentiation of ecological niches. However, in
continental regions of the Eurasian boreal zone, vines (especially woody vines) are rare
and are largely considered as one of the most exotic plant life forms in Ural and Siberia [
4
].
There are only two native vine species in the Ural region: hop (Humulus lupulus L.) and
Siberian clematis (Atragene sibirica L.). Other vine species, especially woody vines, are alien
species growing exclusively as cultivated plants [
4
]. Thus, exotic vines grown in Ural and
Siberia are not well adapted to the cold climates of these regions and are highly susceptible
to frost damage, and often cannot restore died perennial parts (twigs and branches) after a
very cold winter [1].
The alien vines currently grown in Ekaterinburg, one of the largest cities in the Urals
(Northern Asia), largely comprises East Asian and European subtropical vine species [
1
,
4
].
The role of economically important edible vines of the families Vitaceae Juss. ex Bercht. & J.
Presl and Cucurbitaceae Juss. is increasing in Ekaterinburg due to the gradual warming
climate over the last few decades. The frontier of northern viticulture is shifting further to
the north in Ural and Siberia, and a yield of cucurbitaceous crops and grapes is increasing
in the regions too [
1
,
2
,
5
]. As a consequence of the climate warming, vine culture (primarily
viticulture) is expanding further north in Ural and Siberia, and yields of cucurbitaceous
crops and grapes are increasing in these macroregions [1,2,5].
The cultivation of vines in Ekaterinburg dates to the 18–19th centuries, when the city
was developed as an administrative center for the mining industry in the Ural macrore-
gion [
6
–
9
]. Top managers of local factories and mines of the city were inspired by the estates
they often watched in Saint Petersburg and Moscow and tried to design their own local
estates and gardens in a similar “European manner”. This often resulted in the introduction
and cultivation of many exotic ornamental plants (including some vines) in their local
gardens. For example, the most popular vine—common grape vine (Vitis vinifera L.)—was
introduced in Ural cities from the Southern European Russia (mainly from West Caucasus
and Crimea). Several manors in the center of Ekaterinburg City had at least a 50-year
history of vine cultivation by the beginning of the 20th century. However, the center of
Ekaterinburg underwent an urban change in the 1940–1950s, with many old houses and
estates being demolished and replaced by high-rise blocks, resulting in the destruction of
those cultivated vines and vineyards.
Most popular edible herbal vines and cucurbitaceous crops, first of all the ridge cu-
cumber (Cucumis sativus L.) and field pumpkin (Cucurbita pepo L.), were already being
grown in open fields and in greenhouses across Ekaterinburg by the 18th century [
6
]. Other
common herbaceous vines, such as climbing nightshade (Solanum dulcamara L.) and field
bindweed (Convolvulus arvensis L.), were originally accidentally introduced into Ekaterin-
burg as weeds at the end of the 19th century [
6
]. Later, hedge false bindweed (Calystegia
sepium (L.) R. Br.) and ground virgins bower (Clematis recta L.) were introduced too, and
now they are the most common alien herbaceous vines in the modern Ekaterinburg [
6
]. In
addition, the oldest thickets of native vines (hops and Siberian clematis) were preserved
in old cemeteries, which have been around since the 19th century. For example, large
Forests 2022,13, 323 3 of 22
thickets of hops are present at the Ivanovskoye cemetery, which has existed since 1810, and
centennial thickets of hops and the Siberian clematis are preserved at the Mikhailovskoye
cemetery, founded in 1865 [8].
Many alien woody vine species grow in Ekaterinburg along the walls of various
buildings and in parks. The most common of these vines include European common
grape (Vitis vinifera) and European ivy (Hedera helix L.), North American Virginia creeper,
or five-leaved ivy (Parthenocissus quinquefolia (L.) Michx.), and several East Asian plant
species: Amur grape (Vitis amurensis L.), Chinese magnolia-vine (Schisandra chinensis (Turcz.)
Baill.), Variegated-leaf hardy kiwi (Actinidia kolomikta (Rupr. et Maxim.) Maxim.), Yellow
honeysuckle (Lonicera prolifera (Kirchn.) Rehder), Chinese bittersweet (Celastrus orbiculatus
Thunb.), Regel’s Threewingnut (Tripterygium regelii Sprague et Takeda), and climbing
hydrangea (Hydrangea petiolaris Siebold et Zucc.). The common grape and European ivy
are often grown indoors.
Approximately 200–300 km south of Ekaterinburg, the grapes have been grown in
large quantities for wine production in the last 50–80 years [
1
,
5
,
9
]. Due to warming climate
in recent decades, some local farmers of Ekaterinburg and Sverdlovsk province have
also started to produce wine [
5
]. At the same time, many vine-associated saprobic and
phytopathogenic fungi were found on grapes in the city and its suburbs for the first time in
the 2000–2010s [8,10].
We will test the hypothesis that alien vine species, cultivated far from their natural
range, carry much less pathogenic fungi than they do inside their natural range.
The purpose of this study is to determine what fungal species are present on vines
cultivated in Ekaterinburg City, and to determine the potential risk phytopathogenic fungi
pose to the economically important groups of vines such as fruits and vegetable crops. Some
related problems should be resolved: to study the dynamics of the climate in Ekaterinburg
during the 20th to 21st centuries; to assess the species diversity and dynamics of vine
productivity in Ekaterinburg over the last 40 years; to make a list of phytopathogenic fungi
infecting Cucurbitaceae and Vitaceae plants and their dynamics over the last 40 years; to
analyze the covered areas of studied plant species; and to investigate whether the “core
species” of saprobic and phytopathogenic fungi is preserved on the vines outside their
natural and traditional cultural ranges.
2. Materials and Methods
2.1. Climate of Ekaterinburg City
Ekaterinburg City (former Sverdlovsk City, capital of Sverdlovsk province) is situated
in the south boreal subzone (56.825
◦
N; 60.565
◦
E; 280 m a.s.l.) in the Ural macroregion on
the border of Europe and Asia (Figure 1). The city area covers 468 km
2
, and the population
is about 1.5 million people. The average annual temperature over the last ten years has
varied in the range of 3.1–5.3
◦
C [
11
,
12
]. The local climate is considered continental, with
sharp variability in weather conditions and clearly defined seasons. The average monthly
temperature in July is 19.4
◦
C, the absolute daily maximum is 39.6
◦
C. The average monthly
temperature in January is −14.3 ◦C, and the absolute daily minimum is −46.7 ◦C.
Forests 2022,13, 323 4 of 22
Forests2022,13,xFORPEERREVIEW4of23
Figure1.MapofRussiawithEkaterinburgCitylocation.
TheclimateinRussiaiswarmingtwiceasfastastheglobalone,andthisclimatic
trendcanisrecordedinEkaterinburgCitytoo[12,13].Thelocalclimatewasrelatively
coldfromthe1900stothe1970s:theaverageannualtemperaturesvariedintherangeof
−0.7–−3.3°С(Figure2A).Untilthe1970s,regularlong‐termfrosts(withtemperaturesbe‐
low−35–−40°С)wererecordedinthecity,withtheabsoluterecordedminimum−46.7
°С.Asteadyclimatewarminghasstartedsincethelate1970s:frostperiodshavebecome
shorter,themiddle‐winterfrostshaveeased,andduringthelatter40years,nowadays
temperatureinthecityrarelydropsbelow−30°С.Overthelasthalf‐century,thecoldest
year(withthecoldestwinter)was1969(−0.7°С),whilethewarmestyearwas2020(5.3
°С)[12].Thus,theclimaticregimeof2020becamesimilartothecitiesofCentralRussia
attheendofthe20thcentury[12].Over100years,theaveragewintertemperaturein‐
creasedby3.1°С,andtheaveragesummertemperature—by0.2°С[12,13].
ThefrequencyoflastspringfrostsinApril–Juneisalsoimportantforthermophile
plants.Untilthe1970s,regularfrostsdownto−5°Сandsnowfall0.5mdeepwererec‐
ordedinMay–Juneevery4–6years(FigureS1).However,suchlatefrostswerenotob‐
servedinthecityinthe2010s(wereregisteredonlyonceinthelast20years),although
shortsnowfallsoutsidethecityarestillpossible.AverageannualprecipitationinEkate‐
rinburgwas483mm/yearinthe1920s,andithasincreasedto537mm/yearinthe2010s
(Figure2B).Thus,theaverageannualprecipitationhasslightlyincreasedoverthepast
century,withanaveragerateof5.4mm/10years.
2.2.SystematicReviewofYieldDynamicsandAssessmentofVinesCoveredAreas
ThemodelplantwasAmurgrape,thecultivar“Amurbreakthrough”(alsoknown
as“Potapenko‐7”),whichhasgrownheresince1961.Thefollowingmethodwasusedto
estimatetheannualyielddynamics:10modelbushesfor8yearswereobservedand
studied(1966,1972,1979,1986,1993,2001,2012,2020).Thelengthofeachmodelplant
wasaboutsixmeterslongwiththesamecrownshape(E.V.Sinitsyn,pers.data).This
grapecultivarwaschosenforcultivationduetoitshighfrostresistance,highyields,and
highsugarcontentintheberries(23%).
Figure 1. Map of Russia with Ekaterinburg City location.
The climate in Russia is warming twice as fast as the global one, and this climatic
trend can is recorded in Ekaterinburg City too [
12
,
13
]. The local climate was relatively
cold from the 1900s to the 1970s: the average annual temperatures varied in the range
of
−
0.7–
−
3.3
◦
C (Figure 2A). Until the 1970s, regular long-term frosts (with tempera-
tures below −35–−40 ◦C) were recorded in the city, with the absolute recorded minimum
−46.7 ◦C
. A steady climate warming has started since the late 1970s: frost periods have
become shorter, the middle-winter frosts have eased, and during the latter 40 years, nowa-
days temperature in the city rarely drops below
−
30
◦
C. Over the last half-century, the
coldest year (with the coldest winter) was 1969 (
−
0.7
◦
C), while the warmest year was
2020 (5.3 ◦C) [12]. Thus, the climatic regime of 2020 became similar to the cities of Central
Russia at the end of the 20th century [
12
]. Over 100 years, the average winter temperature
increased by 3.1 ◦C, and the average summer temperature—by 0.2 ◦C [12,13].
Forests2022,13,xFORPEERREVIEW5of23
Figure2.The120‐years‐longdynamicsofaverageannualtemperature(A)andaverageannual
precipitation(B)inEkaterinburgCity.Forannualtemperaturedataseparatedbytwoperiods:
blue—1900–1978years,andred—1979–2020years.
Inaddition,wecarriedoutanapproximateassessmentofthecoveredareadynam‐
icsofthemostcommonwoodyvinesinthelastfivedecades(1920,1950,1970,1990,
2010).Theactualcoveredareasofvineswereestimatedduringthecollectionoffungiin
2018–2019.ThearchiverecordsandphotographsoftheEkaterinburgHistoricalMuseum
andarchiverecordsof(1)ironworksfoundedinthe18–19thcenturies,(2)cemeteries
foundedinthe19thcentury,(3)educationalinstitutionsbuiltintheearlyandthemiddle
ofthe20thcentury,(4)arboretathatwereplantedin1930–1940,aswellaspublishedsci‐
entificdata,canapproximatelyestimatetheareaofvariousvinesinEkaterinburgin
1921–2020.
2.3.FungalSampling
Inthepresentresearchwork,westudiedfungigrowingonstems,roots,leaves,and
fruitsoftheoutdoorvinescollectedinEkaterinburgCityanditssuburbsbytheauthors
aswellasfungalspecimenscollectedbyearlierresearchersinthethreemainperiods
(thenamesofthecollectorsaregiven):(I)1913–1950:N.А.Naumov,Z.А.Demidova,
F.А.Solovyov,S.I.Vanin,andА.S.Kazanskiy;(II)1951–1990:Z.А.Demidova,N.Т.Ste‐
panova‐Kartavenko,L.K.Kazantseva,А.V.Sirko,L.М.Mezentseva,andЕ.А.Shurova;
(III)1991–2021:А.G.Shiryaev,N.V.Ushakova,K.А.Fefelov,Е.V.Bryndina,О.S.Shiry‐
aeva,andL.М.Dorofeyeva[8,10,14,15].Thepresentresearchworkdoesnotincludefun‐
galspeciesfoundingreenhousesonly,aswellasmacrofungithatformfruitingbodies
onthesoilsurfaceonly.
Aphyllophoroidfungi,whichpredominatesonsomewoodyvines(upto80–100%
ofallspecies),canbeconsideredasthebest‐studiedgroupamongallrecordedmacro‐
fungionvines,whereasagaricoid,gasteroid,andheterobasidiomycetousfungiarerep‐
resentedbyasmallernumbersofspeciesandmaybeconsideredasstillinsufficiently
knowngroups[8].Thefungiwererecordedin25vinespeciesinthelast100years,but
thepresentresearchonlyincludesthe17mostfungal‐richplantspecies(onwhichmore
thanfivefungalspeciesarerecorded):Actinidiakolomikta,Atragenesibirica,Calystegiase‐
pium,Celastrusorbiculatus,Clematisrecta,Convolvulusarvensis,Dioscoreacaucasica,Hedera
helix,Humuluslupulus,Hydrangeapetiolaris,Loniceraprolifera,Menispermumdauricum,Par‐
thenocissusqiunquefolia,Schisandrachinensis,Tripterygiumregelii,Vitisamurensis,andV.
vinifera(FigureS2).
А В
Figure 2. The
120-years-long dynamics of average annual temperature (
A
) and average annual
precipitation (
B
) in Ekaterinburg City. For annual temperature data separated by two periods:
blue—1900–1978 years, and red—1979–2020 years.
The frequency of last spring frosts in April–June is also important for thermophile
plants. Until the 1970s, regular frosts down to
−
5
◦
C and snowfall 0.5 m deep were recorded
Forests 2022,13, 323 5 of 22
in May–June every 4–6 years (Figure S1). However, such late frosts were not observed
in the city in the 2010s (were registered only once in the last 20 years), although short
snowfalls outside the city are still possible. Average annual precipitation in Ekaterinburg
was 483 mm/year in the 1920s, and it has increased to 537 mm/year in the 2010s (Figure 2B).
Thus, the average annual precipitation has slightly increased over the past century, with an
average rate of 5.4 mm/10 years.
2.2. Systematic Review of Yield Dynamics and Assessment of Vines Covered Areas
The model plant was Amur grape, the cultivar “Amur breakthrough” (also known
as “Potapenko-7”), which has grown here since 1961. The following method was used
to estimate the annual yield dynamics: 10 model bushes for 8 years were observed and
studied (1966, 1972, 1979, 1986, 1993, 2001, 2012, 2020). The length of each model plant was
about six meters long with the same crown shape (E.V. Sinitsyn, pers. data). This grape
cultivar was chosen for cultivation due to its high frost resistance, high yields, and high
sugar content in the berries (23%).
In addition, we carried out an approximate assessment of the covered area dynamics
of the most common woody vines in the last five decades (1920, 1950, 1970, 1990, 2010). The
actual covered areas of vines were estimated during the collection of fungi in 2018–2019.
The archive records and photographs of the Ekaterinburg Historical Museum and archive
records of (1) ironworks founded in the 18–19th centuries, (2) cemeteries founded in the
19th century, (3) educational institutions built in the early and the middle of the 20th
century, (4) arboreta that were planted in 1930–1940, as well as published scientific data,
can approximately estimate the area of various vines in Ekaterinburg in 1921–2020.
2.3. Fungal Sampling
In the present research work, we studied fungi growing on stems, roots, leaves, and
fruits of the outdoor vines collected in Ekaterinburg City and its suburbs by the authors
as well as fungal specimens collected by earlier researchers in the three main periods
(the names of the collectors are given): (I) 1913–1950: N.A. Naumov, Z.A. Demidova, F.A.
Solovyov, S.I. Vanin, and A.S. Kazanskiy; (II) 1951–1990: Z.A. Demidova, N.T. Stepanova-
Kartavenko, L.K. Kazantseva, A.V. Sirko, L.M. Mezentseva, and E.A. Shurova; (III) 1991–
2021: A.G. Shiryaev, N.V. Ushakova, K.A. Fefelov, E.V. Bryndina, O.S. Shiryaeva, and L.M.
Dorofeyeva [
8
,
10
,
14
,
15
]. The present research work does not include fungal species found
in greenhouses only, as well as macrofungi that form fruiting bodies on the soil
surface only.
Aphyllophoroid fungi, which predominates on some woody vines (up to 80–100% of
all species), can be considered as the best-studied group among all recorded macrofungi on
vines, whereas agaricoid, gasteroid, and heterobasidiomycetous fungi are represented by a
smaller numbers of species and may be considered as still insufficiently known groups [
8
].
The fungi were recorded in 25 vine species in the last 100 years, but the present research
only includes the 17 most fungal-rich plant species (on which more than five fungal species
are recorded): Actinidia kolomikta,Atragene sibirica,Calystegia sepium,Celastrus orbicula-
tus,Clematis recta,Convolvulus arvensis,Dioscorea caucasica,Hedera helix,Humulus lupulus,
Hydrangea petiolaris,Lonicera prolifera,Menispermum dauricum,Parthenocissus quinquefolia,
Schisandra chinensis,Tripterygium regelii,Vitis amurensis, and V. vinifera (Figure S2).
We subdivided all studied vine species into three groups by their natural ranges to
analyze the species richness of the associated fungi: (1) four European species (Clematis
recta,Dioscorea caucasica,Hedera helix, and Vitis vinifera); (2) four Eurasian species, including
two common native species (Atragene sibirica and Humulus lupulus), and archaeophytes
that have been present in the city since its foundation (Calystegia sepium and Convolvulus
arvensis); (3) nine “geographically distant” species from East Asia (Actinidia kolomikta,Celas-
trus orbiculatus,Hydrangea petiolaris,Lonicera prolifera,Menispermum dauricum,Schisandra
chinensis, and Tripterygium regelii) and North America (Parthenocissus quinquefolia). East
Asian and North American woody vines were analyzed together because North American
vines are represented by a single species (Parthenocissus quinquefolia).
Forests 2022,13, 323 6 of 22
The fungal diversity was studied in the eleven perennial woody vine species: Atragene
sibirica,Actinidia kolomikta,Celastrus orbiculatus,Hedera helix,Hydrangea petiolaris,Lonicera
prolifera,Parthenocissus quinquefolia,Schisandra chinensis, and Tripterygium regelii, and in the
six annual herbaceous vine species: Calystegia sepium,Clematis recta,Convolvulus arvensis,
Dioscorea caucasica,Humulus lupulus, and Menispermum dauricum. Most attention was paid
to phytopathogenic macro- and microfungi affecting crops of the two most economically
important plant families, Cucurbitaceae and Vitaceae.
Living plants and their dead parts were examined for fruit bodies of macrofungi
and/or plant disease signs caused by phytopathogenic fungi (leaf spots or mildews on
leaves, shoot dieback or blight, trunk rot, fruit rot, and so on) and/or the presence of fungal
generative structures (conidiomata and conidia, ascomata and ascospores, sporangia and
sporangiospores, and others). Affected plant parts with phytopathogenic microfungi were
collected and dried according to the traditional methods [
15
] and placed in paper envelopes.
Fruiting bodies of macrofungi were collected on living and dead parts of plants according to
the standard methods [
8
] and placed in paper bags. All specimens were labeled to provide
complete information about the host plant, locality, date of collection, and collector [
16
,
17
].
Most of the fungal specimens were collected in summer and early autumn seasons (mainly
in July, August, and September). The identification of ascomycetous microfungi was made
by T.S. Bulgakov, the identification of basidiomycetous macrofungi—by A.G. Shiryaev, I.V.
Zmitrovich, and O.S. Shiryaeva.
More than 1180 fungal specimens were examined during the present research. The
collected fungal species were identified using light microscopes LEICA 2000 and Axio
Imager A1. The collected specimens are deposited in Institute of Plant and Animal Ecology
Herbarium (SVER) and V.L. Komarov Botanical Institute Herbarium (LE F). The fungal
species nomenclature is given according to the open database Index Fungorum [18].
2.4. Data Analysis
The main static parameters (mean, SE, SD), box–whisker plots (using middle point—
median, whisker value—min–max, and box value—percentiles (25–75%)), and 95% con-
fidence intervals were calculated in Statistica 8.0. A Mann–Whitney U-test was used to
compare the data series on the number of phytopathogens on stems and leaves of woody
vines. The cluster analysis was performed using Statistica 8.0, using a matrix of Ward’s
method and 1-Pearson correlation coefficient.
3. Results
3.1. Dynamics of Grape Yield and Woody Vines Areas in Ekaterinburg City
The mean yield range of Amur grape (cultivar “Amur breakthrough”, or “Potapenko-
7”) in Ekaterinburg suburbs was 4.7–6.4 kg per model bush during the 1960–1970s. Later,
it increased to 13.1 kg in 1993, to 15.5 kg in 2001, to 20.6 kg in 2012, and to 23.9 kg
in 2020. In 2020, there was a maximal harvest per one plant—28 kg (Figure 3). Thus,
the mean yield was stably low during the 1960–1970s, and it had started to increase
since 1979
(F (5.52) = 61.703
,p= 0.00001). Consequently, the harvest of cultivar “Amur
breakthrough” has grown significantly (p< 0.001) for 41 years (from 1979 to 2020): the
average yield per plant increased 3.7 times, and the maximum yield per plant increased
2.8 times (from 10 to 28 kg).
The covered area of woody vines in the city was consistently low from the 1920s to
the 1950s, varying slightly in the range from 38 to 65 m
2
(Figure 4). In the 1960s, due to
the introduction of many East Asian alien species, the covered area of vines began to grow,
reaching 516 m
2
in the 1970s, mainly due to the Vitaceae plants, whose area was 365 m
2
(Table S1). In the 2010s, the total covered area of vines increased to 2587 m
2
, while the area
of Vitaceae was 1958 m
2
. The main growth in the covered area (among all woody vine
species) was recorded for the Virginia creeper (Parthenocissus quinquefolia). This species
was introduced in Ekaterinburg in the late 1950s only and was absent in the city in the
1920–1940s. However, the covered area of five-leaved ivy had reached 280 m
2
in the 1970s
Forests 2022,13, 323 7 of 22
already, and in the 2010s it increased up to 1685 m
2
, i.e., it currently comprises 65% of the
total area of all woody vines in the city. Thus, nowadays, Parthenocissus quinquefolia is the
most common vine species in the city. Among Vitis species, the largest area in the 2010s was
covered by Vitis amurensis (195 m
2
). The area covered by the plants of the Vitaceae family
has grown 78 times over a 100-year period—from 25 to 1958 m
2
, and the covered area
percentage of Vitaceae plants among all woody vines has also grown steadily, increasing
from 62% in 1920 to 76% in 2010 (Table S1).
Forests2022,13,xFORPEERREVIEW7of23
1979(F(5.52)=61.703,p=0.00001).Consequently,theharvestofcultivar“Amurbreak‐
through”hasgrownsignificantly(p<0.001)for41years(from1979to2020):theaverage
yieldperplantincreased3.7times,andthemaximumyieldperplantincreased2.8times
(from10to28kg).
Figure3.Box–whiskerplotsofthe55‐year‐longyielddynamicfortheonemodelbushofAmur
grape(cultivar“Amurbreakthrough”,or“Potapenko‐7”).
Thecoveredareaofwoodyvinesinthecitywasconsistentlylowfromthe1920sto
the1950s,varyingslightlyintherangefrom38to65m2(Figure4).Inthe1960s,dueto
theintroductionofmanyEastAsianalienspecies,thecoveredareaofvinesbeganto
grow,reaching516m2inthe1970s,mainlyduetotheVitaceaeplants,whoseareawas
365m2(TableS1).Inthe2010s,thetotalcoveredareaofvinesincreasedto2587m2,while
theareaofVitaceaewas1958m2.Themaingrowthinthecoveredarea(amongall
woodyvinespecies)wasrecordedfortheVirginiacreeper(Parthenocissusquinquefolia).
ThisspecieswasintroducedinEkaterinburginthelate1950sonlyandwasabsentinthe
cityinthe1920–1940s.However,thecoveredareaoffive‐leavedivyhadreached280m2
inthe1970salready,andinthe2010sitincreasedupto1685m2,i.e.,itcurrentlycom‐
prises65%ofthetotalareaofallwoodyvinesinthecity.Thus,nowadays,Parthenocissus
quinquefoliaisthemostcommonvinespeciesinthecity.AmongVitisspecies,thelargest
areainthe2010swascoveredbyVitisamurensis(195m2).Theareacoveredbytheplants
oftheVitaceaefamilyhasgrown78timesovera100‐yearperiod—from25to1958m2,
andthecoveredareapercentageofVitaceaeplantsamongallwoodyvineshasalso
grownsteadily,increasingfrom62%in1920to76%in2010(TableS1).
Figure 3.
Box–whisker plots of the 55-year-long yield dynamic for the one model bush of Amur grape
(cultivar “Amur breakthrough”, or “Potapenko-7”).
Forests2022,13,xFORPEERREVIEW8of23
Figure4.Schematicvisualizationofthe100‐year‐longdynamicofcoveredareasforallwoody
vinesandforVitaceaefamilyonlyinEkaterinburgCity.Datacorrespondtothe1920s,1950s,
1970s,1990s,and2010s.
3.2.SystematicReviewoftheFungalSpeciesRichnessRevealedduringtheLast100Years
Thenumberofidentifiedmacrofungalspeciesonallvinesincreasedfrom4to15
fromthe1920stothe1940s(Figure5A).Duringtheseyears,commongrape(Vitisvinif‐
era)wasthemostcommonwoodyvineinEkaterinburgCity,whilethemostcommon
herbaceousvinewascommonhop(Humuluslupulus).Commongrapeplantations(pri‐
vatevineyards)weredestroyedinthe1950s,sotherewerenofungalspecimenscollect‐
edfromgrapesbytheendofthatdecade,andalllocalvineswererepresentedonlyby
hopsandSiberianclematiscoveringsmallareasinsuburbs.Becauseanylargewoody
vineswereabsentinEkaterinburginthe1950s,onlycorticioidandclavarioidvine‐
associatedfungiwerefoundatthattime.Inthelate1950sandearly1960s,EastAsian
frost‐resistantvinespecieswereintroducedinthecity.Beginningwiththe1970s,these
vinespecies—Actinidiakolomikta,Schisandrachinensis,andVitisamurensis—hadgrown
intensively,anddeadwoodypartsinfestingbyporoidfungi(includingphytopathogenic
ones)appeared.Thepeakofregionalfungalresearchfellinthesameperiod—the1970s,
whichcanbeconsideredasthemost“fruitful”periodforthelocalmycologyinthe20th
centuryingeneral,when60specieswerefirstfound.Asaresult,thenumberofknown
vine‐associatedmacrofungalspeciesinEkaterinburgincreasedfrom36to67(Figure
5A),i.e.,doubled,comparedtothepreviousdecade.Thisperiodofactivemycological
researchinthe1970sgavewaytoadeclineinscientificactivityinthe1980s.
Thenextperiodofactiveresearchinthe1990swasassociatedwiththeactivitiesof
theauthors,whichhavecontinuedinthe2000s.Thesecondpeakinthecollectionof
macrofungifellinthe2010s.Asaresult,thetotalnumberofrecordedfungalspeciesin‐
creasedandreached95species.Thus,thereweretwomainpeaks(periods)ofactivesci‐
entificresearchonvine‐associatedfungi:the1970sandthe2010s,whichareseparated
by40years.
Figure 4.
Schematic visualization of the 100-year-long dynamic of covered areas for all woody vines
and for Vitaceae family only in Ekaterinburg City. Data correspond to the 1920s, 1950s, 1970s, 1990s,
and 2010s.
3.2. Systematic Review of the Fungal Species Richness Revealed during the Last 100 Years
The number of identified macrofungal species on all vines increased from 4 to 15 from
the 1920s to the 1940s (Figure 5A). During these years, common grape (Vitis vinifera) was
the most common woody vine in Ekaterinburg City, while the most common herbaceous
vine was common hop (Humulus lupulus). Common grape plantations (private vineyards)
Forests 2022,13, 323 8 of 22
were destroyed in the 1950s, so there were no fungal specimens collected from grapes by
the end of that decade, and all local vines were represented only by hops and Siberian
clematis covering small areas in suburbs. Because any large woody vines were absent in
Ekaterinburg in the 1950s, only corticioid and clavarioid vine-associated fungi were found
at that time. In the late 1950s and early 1960s, East Asian frost-resistant vine species were
introduced in the city. Beginning with the 1970s, these vine species—Actinidia kolomikta,
Schisandra chinensis, and Vitis amurensis—had grown intensively, and dead woody parts
infesting by poroid fungi (including phytopathogenic ones) appeared. The peak of regional
fungal research fell in the same period—the 1970s, which can be considered as the most
“fruitful” period for the local mycology in the 20th century in general, when 60 species
were first found. As a result, the number of known vine-associated macrofungal species in
Ekaterinburg increased from 36 to 67 (Figure 5A), i.e., doubled, compared to the previous
decade. This period of active mycological research in the 1970s gave way to a decline in
scientific activity in the 1980s.
Forests2022,13,xFORPEERREVIEW9of23
Figure5.Dynamicsandaccumulationcurveofspeciesrichnessformacrofungi(A)andaphyllo‐
phoroidfungisingle(B)onvinesinEkaterinburgforthetenlastdecades(sincethe1920stothe
2010s).
Intotal,110specieshavebeenfoundandidentifiedduring100yearsofstudying
themacrofungidiversityonvinesinEkaterinburg(TableS2).Theycanbesubdivided
intothefollowingecologicalgroups:87saprobic,5symbiotic,and18phytopathogenic
species.Inaddition,63speciesofmicrofungiwerecollectedonlivingleaves,shoots,and
twigs(TableS3).Thedynamicsofthespeciesrichnessofaphyllophoroidfungiaresimi‐
lartothosefortheentiremacrofungigroup(Figure5B)andaredeterminedmainlyby
aphyllophoroidfungicollectedandidentifiedonwoodyvinesinthe1920sandallsub‐
sequentdecades.Thecollectingofmacrofungialsopeakedinthe1970sand2010s,when
53and75specieswererecorded,respectively.
Anaverageof24.7aphyllophoroidfungispecieswererecordedontheEastAsian
andNorthAmericanvinespecies(TableS2).Theaveragespeciesrichnessoffungi
amongthe17mostfungal‐richvinespeciesisstatisticallysignificantlyhigherforEast
AsianandNorthAmericanvinespecies(24.7fungalspecies),whosenaturalhabitatsare
thefurthestfromEkaterinburg,thanforgeographicallycloserEuropeanandnative
NorthernEurasianvinespecies,whoseaveragespeciesrichnessare9.7and8.9fungal
species,respectively(Figure6A).
Theaveragespeciesrichnessofmacrofungionwoodyvinespeciesis3.3times
higherthanthatforherbaceousvinespecies(25.2vs.7.7species)(Figure6B).Thus,
woodyvineshavestatisticallysignificantlyhigherfungaldiversitythanherbaceous
ones:F(1.14)=16.047,p=0.0013.Inaddition,theseconclusionsareconfirmedbythefact
that95%confidenceintervalsforthespeciesrichnessofthecomparedgroupsdonot
overlap.
Thecomparisonofthelistsofmacrofungifoundandidentifiedoverthelast100
yearsindicatesthatthevinespecieshaveunitedintotwobasicclusters:woodyandher‐
baceousvinespecies(Figure7).Thefirstsubclusterincludeswoodyvinespeciesofthe
Vitaceaefamily(Vitisamurensis,V.vinifera,andParthenocissusquinquefolia),andthesec‐
ondsubclusterincludesthewoodyvinespeciesofotherplantfamiliesandgenera:Acti‐
nidia,Hedera,Lonicera,Schisandra,etc.Theherbaceousvinespeciescanbegroupedinto
twosubclusterstoo:(1)thealienvinespecies(e.g.,Clematisrecta,Dioscoreacaucasica,and
Menispermumdauricum),includingtheweeds(CalystegiasepiumandConvolvulusarven‐
sis);(2)thenativevinespecies(AtragenesibiricaandHumuluslupulus).
A B
Figure 5.
Dynamics and accumulation curve of species richness for macrofungi (
A
) and aphyl-
lophoroid fungi single (
B
) on vines in Ekaterinburg for the ten last decades (since the 1920s
to the 2010s).
The next period of active research in the 1990s was associated with the activities of
the authors, which have continued in the 2000s. The second peak in the collection of
macrofungi fell in the 2010s. As a result, the total number of recorded fungal species
increased and reached 95 species. Thus, there were two main peaks (periods) of active
scientific research on vine-associated fungi: the 1970s and the 2010s, which are separated
by 40 years.
In total, 110 species have been found and identified during 100 years of studying the
macrofungi diversity on vines in Ekaterinburg (Table S2). They can be subdivided into
the following ecological groups: 87 saprobic, 5 symbiotic, and 18 phytopathogenic species.
In addition, 63 species of microfungi were collected on living leaves, shoots, and twigs
(Table S3).
The dynamics of the species richness of aphyllophoroid fungi are similar to those
for the entire macrofungi group (Figure 5B) and are determined mainly by aphyllophoroid
fungi collected and identified on woody vines in the 1920s and all subsequent decades. The
collecting of macrofungi also peaked in the 1970s and 2010s, when 53 and 75 species were
recorded, respectively.
An average of 24.7 aphyllophoroid fungi species were recorded on the East Asian
and North American vine species (Table S2). The average species richness of fungi among
the 17 most fungal-rich vine species is statistically significantly higher for East Asian and
Forests 2022,13, 323 9 of 22
North American vine species (24.7 fungal species), whose natural habitats are the furthest
from Ekaterinburg, than for geographically closer European and native Northern Eurasian
vine species, whose average species richness are 9.7 and 8.9 fungal species, respectively
(Figure 6A).
Forests2022,13,xFORPEERREVIEW10of23
Figure6.ComparisonofspeciesrichnessformacrofungiinEkaterinburgCityondifferentgeo‐
graphicalgroupsofvines(A)andstructuraltypes(B).Meansand95%confidenceintervalsare
given.Geographicalrange:EA+NA—EastAsianandNorthAmericanvines,EU—European,
NAT—native(Eurasian),incl.archaeophytes;Structuraltype:Woody—woodyvines,Herba‐
ceous—herbaceousvines.
Theaphyllophoroidfungihavethewidestpossiblerangeofvinessubstratesamong
recordedmacrofungi.Forexample,Typhulamicanswasrecordedonthelargestnumber
ofvinespecies(16hostplantspecies),aswellassomeothermacrofungi:T.setipes(14
hostplantspecies),Xylodonsambuci(13),Typhulacrassipes(13),T.culmigena(12),T.juncea
(10),Pteruliciumgracile(11),Bjerkanderaadusta(9),Irpexlacteus(9),Peniophoracinerea(9),
Cylindrobasidiumevolvens(8),Schizophyllumcommune(7).Theagaricoid,gasteroid,and
heterobasidiomycetousfungiwererecordedononeortwovinespeciesonly.Allthese
speciesarecommonnativespeciesattheUralsandSiberia.
Figure7.Correlationofmacrofungispeciescompositionforthe17mostfungal‐richvinespeciesin
EkaterinburgCity.
Figure 6.
Comparison of species richness for macrofungi in Ekaterinburg City on different geo-
graphical groups of vines (
A
) and structural types (
B
). Means and 95% confidence intervals are
given. Geographical range: EA + NA—East Asian and North American vines, EU—European,
NAT—native (Eurasian), incl. archaeophytes; Structural type: Woody—woody vines, Herbaceous—
herbaceous vines.
The average species richness of macrofungi on woody vine species is 3.3 times
higher than that for herbaceous vine species (25.2 vs. 7.7 species) (Figure 6B). Thus,
woody vines have statistically significantly higher fungal diversity than herbaceous ones:
F (1.14) = 16.047
,p= 0.0013. In addition, these conclusions are confirmed by the fact that
95% confidence intervals for the species richness of the compared groups do not overlap.
The comparison of the lists of macrofungi found and identified over the last 100 years
indicates that the vine species have united into two basic clusters: woody and herbaceous
vine species (Figure 7). The first subcluster includes woody vine species of the Vitaceae
family (Vitis amurensis,V. vinifera, and Parthenocissus quinquefolia), and the second subcluster
includes the woody vine species of other plant families and genera: Actinidia,Hedera,
Lonicera,Schisandra, etc. The herbaceous vine species can be grouped into two subclusters
too: (1) the alien vine species (e.g., Clematis recta,Dioscorea caucasica, and Menispermum
dauricum), including the weeds (Calystegia sepium and Convolvulus arvensis); (2) the native
vine species (Atragene sibirica and Humulus lupulus).
The aphyllophoroid fungi have the widest possible range of vines substrates among
recorded macrofungi. For example, Typhula micans was recorded on the largest num-
ber of vine species (16 host plant species), as well as some other macrofungi: T. setipes
(14 host
plant species), Xylodon sambuci (13), Typhula crassipes (13), T. culmigena (12), T. juncea
(10), Pterulicium gracile (11), Bjerkandera adusta (9), Irpex lacteus (9), Peniophora cinerea (9),
Cylindrobasidium evolvens (8), Schizophyllum commune (7). The agaricoid, gasteroid, and
heterobasidiomycetous fungi were recorded on one or two vine species only. All these
species are common native species at the Urals and Siberia.
Forests 2022,13, 323 10 of 22
Forests2022,13,xFORPEERREVIEW10of23
Figure6.ComparisonofspeciesrichnessformacrofungiinEkaterinburgCityondifferentgeo‐
graphicalgroupsofvines(A)andstructuraltypes(B).Meansand95%confidenceintervalsare
given.Geographicalrange:EA+NA—EastAsianandNorthAmericanvines,EU—European,
NAT—native(Eurasian),incl.archaeophytes;Structuraltype:Woody—woodyvines,Herba‐
ceous—herbaceousvines.
Theaphyllophoroidfungihavethewidestpossiblerangeofvinessubstratesamong
recordedmacrofungi.Forexample,Typhulamicanswasrecordedonthelargestnumber
ofvinespecies(16hostplantspecies),aswellassomeothermacrofungi:T.setipes(14
hostplantspecies),Xylodonsambuci(13),Typhulacrassipes(13),T.culmigena(12),T.juncea
(10),Pteruliciumgracile(11),Bjerkanderaadusta(9),Irpexlacteus(9),Peniophoracinerea(9),
Cylindrobasidiumevolvens(8),Schizophyllumcommune(7).Theagaricoid,gasteroid,and
heterobasidiomycetousfungiwererecordedononeortwovinespeciesonly.Allthese
speciesarecommonnativespeciesattheUralsandSiberia.
Figure7.Correlationofmacrofungispeciescompositionforthe17mostfungal‐richvinespeciesin
EkaterinburgCity.
Figure 7.
Correlation of macrofungi species composition for the 17 most fungal-rich vine species in
Ekaterinburg City.
In contrast, we found some thermophilous fungi on a large number of woody vine
species, also nonnative species for the region—they are not recorded in the wild nature at a
distance of 2000–5000 km from Ekaterinburg City. For example, Hydnophlebia chrysorhiza
are species known only in the south of the Far East of Russia (the nearest finds). This
species was also recorded in East Asia (Japan, South Korea), the Himalayas (India), tropical
Africa (Cameroon), the eastern United States, southeastern Canada, and South America
(Brazil, Venezuela); moreover, this fungus is a candidate for inclusion in the international
Red Book (http://iucn.ekoo.se/iucn/species_view/332100/) (accessed on 20 Novem-
ber 2021). The nearest recorded locations for the Tomentella olivascens are in deciduous
forests of Europe (France, the Carpathians in Ukraine, the Caucasus in Russia), East
Asia (the Kuril Islands and Primorsky province of Russia), and North America (USA).
Radulomyces rickii was also collected for the first time in the Ural macroregion; this fun-
gus is known in deciduous and tropical regions of East Asia (Japan), Africa (Ethiopia),
Europe (Great Britain, France, the Netherlands, Italy, southern Scandinavia, western Rus-
sia), North America (USA), Australia, and New Zealand. There are collections of this
species in Siberia (Tomsk Region) in 1931 (https://www.gbif.org/occurrence/3043183453)
(accessed on 20 November 2021). Steccherinum bourdotii was collected for the first time
in Ekaterinburg. This species is known from mixed coniferous–deciduous forests in
the tropics; it was found in Asia (India), Europe (from southern Scandinavia to the
Iberian Peninsula, western Russia), Africa (Uganda), and North America (USA). There
is a single find in Siberia (https://www.gbif.org/occurrence/2309708470) (accessed on
20 November 2021). In addition, we found Crustomyces expallens, which is common
in deciduous forests of Manchuria (China), Europe (Great Britain and from southern
Scandinavia to the Alps), North America, and the European part of Russia; its nearest
record is in the Altai Mountains (https://www.gbif.org/species/2550290) (accessed on
20 November 2021). Gloeohypochnicium analogum is the next first-time-collected species
in the Urals; it was found in East Asia (China and Primorsky province of Russia), Africa
(Malawi), New Zealand, North America (USA, Canada), Europe (from the south of Scan-
dinavia to the Mediterranean) (https://www.gbif.org/species/2544664) (accessed on 20
November 2021). For Lilaceophlebia cf. ochraceofulva, the center of the natural range lies
in deciduous forests of Europe (from southern Scandinavia to the Mediterranean) and
North America (USA, Canada) (https://www.gbif.org/species/2545063) (accessed on 20
November 2021). The record of the cosmopolitan poroid fungus Cerioporus scutellatus
(https://www.gbif.org/species/2547190) (accessed on 20 November 2021) on hardy kiwi
Forests 2022,13, 323 11 of 22
is extremely interesting because this species is treated as arcto-alpine, associated with dead-
wood of Alnus fruticosa and A. viridis in Europe, Ural, and Siberia. We have two specimens
of this species collected in hardy kiwi at 5000–6000 km distance from Ekaterinburg, in East
Asia (Jilin province in China and Sakhalin province in Russia) (H. Kotiranta, pers. comm.
and A. Shiryaev, unpubl. data). The full list of first-found species is much longer and
includes many other macro- and microfungal species: Elsinoe ampelina,Erysiphe necator,
Eutypa scabrosa,Mycoacia uda,Phaeomoniella chlamydospora,Ramularia schisandrae,Taeniolina
scripta, etc.
3.3. Fungal Groups’ Tendencies during the Last 40 Years
The distribution of fungal species richness in the three main biogeographic groups of
macrofungi recorded in the 1970s and 2010s is similar (p< 0.01) to that for the entire study
period (Figure 6A). However, the result for the 2010s show that the vine-associated fungal
species richness in vine species originated from the most distant regions (East Asia and
North America) is 3.5 times higher than in European and native vine Northern Eurasian
species (16.4 species vs. 5.0 and 4.7) (Figure 8). East Asian and North American vines have
also higher fungal diversity than European and native Northern Eurasian ones in the 1970s
(the average numbers of species were 7.7 vs. 1.7 and 3.3). However, the average number of
fungal species recorded on East Asian and North American vines has increased from 7.7 to
16.4 (U = 7, z =
−
2.57, p= 0.009) in the last 40 years, while the fungal diversity for European
and native (Eurasian) vines did not change significantly (p= 0.58 and 0.66, respectively),
remaining stably low. Among the native vine species, the most fungal-rich is hops, on
which seven and five fungal species, respectively, were identified in two compared periods.
Forests2022,13,xFORPEERREVIEW12of23
Americanvineshasincreasedfrom7.7to16.4(U=7,z=−2.57,p=0.009)inthelast40
years,whilethefungaldiversityforEuropeanandnative(Eurasian)vinesdidnot
changesignificantly(p=0.58and0.66,respectively),remainingstablylow.Amongthe
nativevinespecies,themostfungal‐richishops,onwhichsevenandfivefungalspecies,
respectively,wereidentifiedintwocomparedperiods.
Figure8.Box–whiskergraphof40‐year‐longdynamicsofaphyllophoroidfungispeciesrichnessat
threegeographicalrangegroupsofvinespecies.EA+NA—East‐AsianandNorthAmericanvine
species;EU—European;NAT—native.
Thenumberofaphyllophoroidfungionwoodyvinespecieshassignificantlyin‐
creasedinthelast40years(F(1.25)=11.05,p=0.002):theaveragespeciesrichnesshas
doubled,from6.6to13.7species(Figure9).Ontheotherhand,thenumberoffungal
speciesonherbaceousvinespeciesdoesnotdiffersignificantlybetween40yearsago
andnow(F(1.13)=1.41,p=0.256),sotheaveragespeciesrichnesshaschangedinsignifi‐
cantly,from3.3to4.6species.
Figure9.Box–whiskergraphof40‐year‐longdynamicsofaphyllophoroidfungispeciesrichness
onwoodyandherbaceousvinespecies.
Figure 8.
Box–whisker graph of 40-year-long dynamics of aphyllophoroid fungi species richness at
three geographical range groups of vine species. EA + NA—East-Asian and North American vine
species; EU—European; NAT—native.
The number of aphyllophoroid fungi on woody vine species has significantly increased
in the last 40 years (F (1.25) = 11.05, p= 0.002): the average species richness has doubled,
from 6.6 to 13.7 species (Figure 9). On the other hand, the number of fungal species
on herbaceous vine species does not differ significantly between 40 years ago and now
(F (1.13) = 1.41
,p= 0.256), so the average species richness has changed insignificantly, from
3.3 to 4.6 species.
Forests 2022,13, 323 12 of 22
Forests2022,13,xFORPEERREVIEW12of23
Americanvineshasincreasedfrom7.7to16.4(U=7,z=−2.57,p=0.009)inthelast40
years,whilethefungaldiversityforEuropeanandnative(Eurasian)vinesdidnot
changesignificantly(p=0.58and0.66,respectively),remainingstablylow.Amongthe
nativevinespecies,themostfungal‐richishops,onwhichsevenandfivefungalspecies,
respectively,wereidentifiedintwocomparedperiods.
Figure8.Box–whiskergraphof40‐year‐longdynamicsofaphyllophoroidfungispeciesrichnessat
threegeographicalrangegroupsofvinespecies.EA+NA—East‐AsianandNorthAmericanvine
species;EU—European;NAT—native.
Thenumberofaphyllophoroidfungionwoodyvinespecieshassignificantlyin‐
creasedinthelast40years(F(1.25)=11.05,p=0.002):theaveragespeciesrichnesshas
doubled,from6.6to13.7species(Figure9).Ontheotherhand,thenumberoffungal
speciesonherbaceousvinespeciesdoesnotdiffersignificantlybetween40yearsago
andnow(F(1.13)=1.41,p=0.256),sotheaveragespeciesrichnesshaschangedinsignifi‐
cantly,from3.3to4.6species.
Figure9.Box–whiskergraphof40‐year‐longdynamicsofaphyllophoroidfungispeciesrichness
onwoodyandherbaceousvinespecies.
Figure 9.
Box–whisker graph of 40-year-long dynamics of aphyllophoroid fungi species richness on
woody and herbaceous vine species.
For 40 years, the largest number of fungal species was found on woody vine species
that cover the largest areas in the city (1970s: r = 0.84, p= 0.0002 vs. 2010s: r = 0.64,
p= 0.003
) (Figure 10A). During the 2010s, the largest number of macrofungi was known
on Parthenocissus quinquefolia—26 species were found over an area of 1685 m
2
(Table S1),
19 species
—on Actinidia kolomikta were recorded from an area of 210 m
2
, and 16 species—on
Vitis amurensis from an area of 195 m2. For comparison, only 22 macrofungal species were
recorded in the 1970s on Parthenocissus quinquefolia from an area of 280 m
2
, 14 species—on
Actinidia kolomikta from an area of 45 m
2
, 13 species—on Schisandra chinensis from an area
of 40 m2, and 13 species—on Vitis amurensis from an area of 70 m2(Figure 10B).
Forests2022,13,xFORPEERREVIEW13of23
For40years,thelargestnumberoffungalspecieswasfoundonwoodyvinespecies
thatcoverthelargestareasinthecity(1970s:r=0.84,p=0.0002vs.2010s:r=0.64,p=
0.003)(Figure10A).Duringthe2010s,thelargestnumberofmacrofungiwasknownon
Parthenocissusquinquefolia—26specieswerefoundoveranareaof1685m2(TableS1),19
species—onActinidiakolomiktawererecordedfromanareaof210m2,and16species—on
Vitisamurensisfromanareaof195m2.Forcomparison,only22macrofungalspecies
wererecordedinthe1970sonParthenocissusquinquefoliafromanareaof280m2,14spe‐
cies—onActinidiakolomiktafromanareaof45m2,13species—onSchisandrachinensis
fromanareaof40m2,and13species—onVitisamurensisfromanareaof70m2(Figure
10B).
Figure10.Thecorrelationsbetweenthemacrofungalspeciesrichnessateachwoodyvinespecies
andthecoveredarea(A)in1970s(n=14),and(B)in2010s(n=17).
Themorphologicalstructureoftherecordedmacrofungihasbeentransformedin
thelast40years(Figure11A).Inthe1970s,EastAsianandNorthAmericanvinespecies
hadyoungandthinbranchesandtwigs,onwhichmainlysaprobicporoidandagaricoid
macrofungiformedtheirbasidiomas.Thebio‐andmortalmasses,aswellastheareaof
thevines,haveincreasedsignificantlyinthe2010s.Thenumberofporoid(from11to20
species)andcorticioid(from33to43species)macrofungiincreasedmostsignificantly,
whilethenumberofclavarioidspeciesremainedalmostthesame(Figure11A).Conse‐
quently,theproportionofrecordedporoidsincreased.Thespeciesrichnessofsaprobic
fungalspecieshasalmostdoubledafter40years,whilethenumberofphytopathogenic
fungihasincreasedbyathirdonly(Figure11B).
3.4.PhytopathogenicFungionEdibleVines
TheediblevinespeciesofCucurbitaceaeandVitaceaeplantfamiliescoverthelarg‐
estareasamongplantationsoftheeconomicallysignificantgroupsofvinesinEkaterin‐
burgCity(Table1).Theyhavethelongesthistoryofcultivationinthecity:forexample,
thepumpkin(Cucurbitaspp.)hasbeencultivatedheresincethebeginningofthe18th
centuryandthegrapes(Vitisspp.)—sincethemiddleofthe19thcentury.Thecovered
areaofVitaceaeplantsinEkaterinburghasincreasedfivetimes(Figure4;TableS1),and
thecoveredareaofCucurbitaceaeplants—aboutthreetimes,sincethe1970s(A.L.Ma‐
nilova,pers.data).
Figure 10.
The correlations between the macrofungal species richness at each woody vine species
and the covered area (A) in 1970s (n= 14), and (B) in 2010s (n= 17).
The morphological structure of the recorded macrofungi has been transformed in
the last 40 years (Figure 11A). In the 1970s, East Asian and North American vine species
had young and thin branches and twigs, on which mainly saprobic poroid and agaricoid
Forests 2022,13, 323 13 of 22
macrofungi formed their basidiomas. The bio- and mortal masses, as well as the area of the
vines, have increased significantly in the 2010s. The number of poroid (from 11 to
20 species
)
and corticioid (from 33 to 43 species) macrofungi increased most significantly, while the
number of clavarioid species remained almost the same (Figure 11A). Consequently, the
proportion of recorded poroids increased. The species richness of saprobic fungal species
has almost doubled after 40 years, while the number of phytopathogenic fungi has increased
by a third only (Figure 11B).
Forests2022,13,xFORPEERREVIEW14of23
Figure11.40‐year‐longdynamicsofmorphologicalformandecologicalstrategygroupsofaphyl‐
lophoroidfungionthevinespecies.1—numberofspecies,2—percentage(%);A—morphological
form,B—ecologicalstrategy.Morphologicalforms:Cor—corticioid,Por—poroid,Cla—clavarioid;
ecologicalstrategies:Sw—saprobesonwood,Sl—saprobesonlitter,P—phytopathogens,M—
mycorrhizalfungi.
Intotal,81speciesofphytopathogenicfungiwererecordedonlivingvinesduring
thelast100years(TableS3),including49speciesfoundonthehostplantsofCucurbita‐
ceaeandVitaceaefamilies(Table1).Amongthem,32specieswerefoundinVitaceae,in‐
cluding13speciesofmacrofungi(Armillariaborealis,Fomitoporiapunctata,Stereumhirsu‐
tum,andothers)and19speciesofmicrofungi(Erysiphenecator,Phyllostictaampelicida,
Pseudocercosporavitis,andothers)(Table1).Inaddition,19speciesofphytopathogenic
fungiwererecordedinCucurbitaceaeplants,includingfourspeciesofmacrofungi
(Ceratobasidiumcornigerum,Typhulamicans,andT.culmigena)and15speciesofmicrofun‐
gi(Cladosporiumcucumerinum,Golovinomycestabaci,Septoriacucurbitacearum,andothers).
Inthe1910–1970s,16speciesofphytopathogenicfungiwerealreadyknowninCu‐
curbitaceaeplants(84%ofallspeciesknownin2010s),whilethephytopathogenicfungi
inVitaceaeplantswererepresentedby20species(63%)(Figure12).Thenumberofrec‐
ordedmacrofungiinCucurbitaceaecropshasincreasedby25%inthelast40years,
whilethenumberofrecordedmicrofungihasincreasedby20%inthesameperiod.
Somephytopathogenicfungi—Colletotrichumorbiculare,Septoriacucurbitacearum,andTy‐
phulaculmigena—werecollectedforthefirsttimeinEkaterinburgin2010s.Thenumber
ofmacrofungirecordedinVitaceaeplantshasincreasedby38%inthelast40years,
whilethenumberofmicrofungihasincreasedby33%.Comparedtothe1970s,species
suchasArmillariaborealis,Fomitiporiapunctata,Phaeomoniellachlamydospora,andsome
othershavebeenfoundforthefirsttime.
Figure 11.
40-year-long dynamics of morphological form and ecological strategy groups of
aphyllophoroid fungi on the vine species.
1
—number of species,
2
—percentage (%);
A
—
morphological form,
B
—ecological strategy. Morphological forms: Cor—corticioid, Por—
poroid, Cla—clavarioid; ecological strategies: Sw—saprobes on wood, Sl—saprobes on litter, P—
phytopathogens, M—mycorrhizal fungi.
3.4. Phytopathogenic Fungi on Edible Vines
The edible vine species of Cucurbitaceae and Vitaceae plant families cover the largest
areas among plantations of the economically significant groups of vines in Ekaterinburg
City (Table 1). They have the longest history of cultivation in the city: for example, the
pumpkin (Cucurbita spp.) has been cultivated here since the beginning of the 18th century
and the grapes (Vitis spp.)—since the middle of the 19th century. The covered area of
Vitaceae plants in Ekaterinburg has increased five times (Figure 4; Table S1), and the
covered area of Cucurbitaceae plants—about three times, since the 1970s (A.L. Manilova,
pers. data).
Forests 2022,13, 323 14 of 22
Table 1.
The species list of phytopathogenic fungi recorded in Cucurbitaceae and Vitaceae plants in
Ekaterinburg City.
Cucurbitaceae Vitaceae
Macrofungi
Ceratobasidium cornigerum Armillaria borealis
Rhizoctonia solani Athelia rolfsii
Typhula micans Ceratobasidium cornigerum
Typhula culmigena Fomitiporia punctata
Ganoderma applanatum
Irpex lacteus
Inonotus hispidus
Phanerochaete velutina
Phellinopsis conchata
Pholiota limonella
Pleurotus pulmonarius
Schizophyllum commune
Stereum hirsutum
Microfungi
Alternaria alternata Alternaria alternata
Alternaria cucumerina Aureobasidium pullulans
Botrytis cinerea Botrytis cinerea
Cladosporium cucumerinum Colletotrichum parthenocissicola
Colletotrichum orbiculare Colletotrichum quinquefoliae
Fusarium oxysporum Coniella diplodiella
Golovinomyces tabaci Diplodia seriata
Podosphaera xanthi Elsinoe ampelina
Pseudoperonospora cubensis Erysiphe necator
Pythium aphanidermatum Eutypa scabrosa
Septoria cucurbitacearum Fusarium oxysporum
Sclerotinia sclerotiorum Globisporangium debaryanum
Stagonosporopsis cucurbitacearum Nectria cinnabarina
Verticillium alboatrum Phaeomoniella chlamydospora
Verticillium dahliae Phyllosticta ampelicida
Plasmopara viticola
Pseudocercospora vitis
Ramularia vitis
Verticillium glaucum
Note:
in bold
—the fungal species were not known on these substrates in the 1970s but were collected in the 2010s.
Fumago vagans s. l. was excluded from the list as an unclear and not plant parasitic species. This fungus was
recorded on the plants of the both families in the 1970s and 2010s.
In total, 81 species of phytopathogenic fungi were recorded on living vines during the
last 100 years (Table S3), including 49 species found on the host plants of Cucurbitaceae
and Vitaceae families (Table 1). Among them, 32 species were found in Vitaceae, including
13 species
of macrofungi (Armillaria borealis,Fomitoporia punctata,Stereum hirsutum, and
others) and 19 species of microfungi (Erysiphe necator,Phyllosticta ampelicida,Pseudocercospora
Forests 2022,13, 323 15 of 22
vitis, and others) (Table 1). In addition, 19 species of phytopathogenic fungi were recorded
in Cucurbitaceae plants, including four species of macrofungi (Ceratobasidium cornigerum,
Typhula micans, and T. culmigena) and 15 species of microfungi (Cladosporium cucumerinum,
Golovinomyces tabaci,Septoria cucurbitacearum, and others).
In the 1910–1970s, 16 species of phytopathogenic fungi were already known in Cucur-
bitaceae plants (84% of all species known in 2010s), while the phytopathogenic fungi in
Vitaceae plants were represented by 20 species (63%) (Figure 12). The number of recorded
macrofungi in Cucurbitaceae crops has increased by 25% in the last 40 years, while the num-
ber of recorded microfungi has increased by 20% in the same period. Some phytopathogenic
fungi—Colletotrichum orbiculare,Septoria cucurbitacearum, and Typhula culmigena—were col-
lected for the first time in Ekaterinburg in 2010s. The number of macrofungi recorded in
Vitaceae plants has increased by 38% in the last 40 years, while the number of microfungi
has increased by 33%. Compared to the 1970s, species such as Armillaria borealis,Fomitiporia
punctata,Phaeomoniella chlamydospora, and some others have been found for the first time.
Forests 2022, 13, x FOR PEER REVIEW 16 of 23
Figure 12. 40-year-long dynamic of phytopathogenic fungi richness on Cucurbitaceae and Vita-
ceae plant families.
4. Discussion
The climate of Ekaterinburg in the 1920–1940s was too cold for the development of
many vine species in the 1920–1940s: the average annual temperatures varied in the
range of −0.6…−2.9 °С, and winters were extremely severe: frosts reached up to −40 °С
and lasted more than one month. Only few woody vine species (Vitis vinifera and its hy-
brids) were grown in small numbers in such climatic conditions—mainly as ornamental
plants, as they were regularly damaged by frost and produced low yields. Almost all
grapes and old vineyards were destroyed in the 1950s due to the city center develop-
ment.
Botanical and natural resource research in the 1940–1950s in the Russian Far East
made it possible to find and introduce many East Asian vine species that are much more
frost-resistant than the South European ones [2]. Based on Vitis amurensis, some new
frost-resistant cultivars were bred in those years [5], and soon they gained popularity in
Russia. The extensive introduction of such grape cultivars began in the boreal regions of
Russian Far East, Siberia, and Ural in the late 1950s [3], including Ekaterinburg in the
late 1950s and early 1960s. At the same time, from the early 1960s, East Asian and North
American woody vines were introduced in wide culture in boreal cities of Russia: Acti-
nidia kolomikta, Schizandra chinensis, Hydrangea petiolaris, Parthenocissus quinquefolia, and
many others. Thus, despite the closer location of European vineyards to Ekaterinburg,
the current species diversity of exotic (mainly East Asian) vines in the city is 2.5 times
higher compared with the species diversity of native and European ones due to the low
number of the latter in the flora of the Urals and Siberia, as well as better winter hardi-
ness of the East Asian species introduced from the Russian Far East [3,5,19–21].
The average annual temperature in the city has increased from 2.3 °С in the 1970s to
4.7 °С in the 2010s; at the same time, the average monthly temperature in January has in-
creased from −18.3 to −14.5 °С, and the average duration of frosts below −30 °С has de-
creased from 22 to 11 days per year during the same 40-year period [11]. Consequently,
the city climate has become more favorable for the alien vine species, which now are less
frostbitten in cold winters and therefore can reach larger sizes and older age. The species
diversity of cultivated vines has also increased: the number of vine species in the open
field has increased 2.4 times in the last 40 years. The average grape yield has grown 3.7
times, and the covered area of woody vines has grown five times. The growth in produc-
tivity and area of grapes strongly positively correlates with the average annual tempera-
ture (p = 0.0001). The warming climate causes the increasing of the diversity of woody
vine species as well as the covered area, and these processes lead to an increase in bio-
Figure 12.
40-year-long dynamic of phytopathogenic fungi richness on Cucurbitaceae and Vitaceae
plant families.
4. Discussion
The climate of Ekaterinburg in the 1920–1940s was too cold for the development of
many vine species in the 1920–1940s: the average annual temperatures varied in the range
of
−
0.6
. . . −
2.9
◦
C, and winters were extremely severe: frosts reached up to
−
40
◦
C and
lasted more than one month. Only few woody vine species (Vitis vinifera and its hybrids)
were grown in small numbers in such climatic conditions—mainly as ornamental plants, as
they were regularly damaged by frost and produced low yields. Almost all grapes and old
vineyards were destroyed in the 1950s due to the city center development.
Botanical and natural resource research in the 1940–1950s in the Russian Far East
made it possible to find and introduce many East Asian vine species that are much more
frost-resistant than the South European ones [
2
]. Based on Vitis amurensis, some new
frost-resistant cultivars were bred in those years [
5
], and soon they gained popularity in
Russia. The extensive introduction of such grape cultivars began in the boreal regions of
the Russian Far East, Siberia, and Ural in the late 1950s [
3
], including Ekaterinburg in the
late 1950s and early 1960s. At the same time, from the early 1960s, East Asian and North
American woody vines were introduced in wide culture in boreal cities of Russia: Actinidia
kolomikta,Schizandra chinensis,Hydrangea petiolaris,Parthenocissus quinquefolia, and many
others. Thus, despite the closer location of European vineyards to Ekaterinburg, the current
species diversity of exotic (mainly East Asian) vines in the city is 2.5 times higher compared
with the species diversity of native and European ones due to the low number of the latter
in the flora of the Urals and Siberia, as well as better winter hardiness of the East Asian
species introduced from the Russian Far East [3,5,19–21].
Forests 2022,13, 323 16 of 22
The average annual temperature in the city has increased from 2.3
◦
C in the 1970s
to 4.7
◦
C in the 2010s; at the same time, the average monthly temperature in January has
increased from
−
18.3 to
−
14.5
◦
C, and the average duration of frosts below
−
30
◦
C has
decreased from 22 to 11 days per year during the same 40-year period [11]. Consequently,
the city climate has become more favorable for the alien vine species, which now are less
frostbitten in cold winters and therefore can reach larger sizes and older age. The species
diversity of cultivated vines has also increased: the number of vine species in the open field
has increased 2.4 times in the last 40 years. The average grape yield has grown 3.7 times,
and the covered area of woody vines has grown five times. The growth in productivity
and area of grapes strongly positively correlates with the average annual temperature
(p= 0.0001)
. The warming climate causes the increasing of the diversity of woody vine
species as well as the covered area, and these processes lead to an increase in biomass
of vines (which is the main substrate for phytopathogenic fungi) and accumulation of
wood debris (which is the main substrate for wood-destroying fungi). Therefore, climate
warming is the main reason for the local increase in the diversity of fungi associated with
the vine species [22,23].
4.1. General Results of 100-Year-Long Monitoring
In modern time, 110 species of macrofungi were recorded on vines in Ekaterinburg
City. This seems to be a significant number for a considerably small area of 468 km
2
located
2000–5000 km from the northern frontier of distribution of woody vines in Europe and
Central and East Asia. For example, regional and local lists of fungi known on vines
include not more than 20–30 species in the lands of ancient viticulture, such as Primorsky
and Sakhalin provinces (Russia), Manchuria (Northern China), Uzbekistan, southeastern
Kazakhstan, Caucasus, Crimea, and some Mediterranean countries [24–33].
Such relatively high fungal diversity in vines in Ekaterinburg City can be explained
by a critical study of the substrate, i.e., high selective effort, as well as by a high species
diversity of introduced vine species cultivated together in a relatively small area. The
local climate is unfavorable for the vine species, which grow in conditions that are far
beyond their ecological optimum and, therefore, they have weakened vitality. As is well
known, stressed and depressed plants become more susceptible to weak and opportunistic
pathogens, especially native macrofungal species. This can explain the high number
(18 species) of phytopathogenic macrofungi recorded on the studied vines.
The review of 100-year-long research works shows that the average species num-
ber of macrofungi recorded on the most “geographically distant” East Asian and North
American vine species is 3.3–3.5 times higher than on the European and the native ones
(Figures 6and 8)
. This fact allows us to compare the data on the East Asian vines of Ekater-
inburg with any similar data, for example, with ones for Primorsky province (the Russian
Far East), where only 34 macrofungal species on all vine species were recorded [
33
–
35
]. As
we can see, the number of macrofungal species in Ekaterinburg is three times higher than
in Primorsky province, despite the fact that the latter area is three orders of magnitude
larger than the first one (165,900 vs. 468 km
2
). The total number of phytopathogenic
macrofungi in Ekaterinburg City is 18 species, whereas only 14 species were recorded in
Primorsky province. Moreover, 81 species of phytopathogenic macro- and microfungi were
found on all vine species in Ekaterinburg, whereas only 79 species are recorded in vines
in the much larger Primorsky province [
33
–
37
]. However, this result mostly indicates the
incompleteness of current data on the mycobiota of Primorsky province.
The comparison of fungal species richness of vine species indicates that, for example,
38 species of macrofungi were collected on the East Asian Actinidia kolomikta in Ekaterin-
burg [
8
], and only 17 species were recorded on the same plant in Primorsky province [
37
].
The number of known phytopathogenic microfungi on the same plant in Ekaterinburg is
six, whereas in Primorsky province—five species [
33
–
37
]. Vitis amurensis demonstrates a
similar pattern: 36 species of macrofungi, including eight pathogenic ones, were collected
Forests 2022,13, 323 17 of 22
on this plant species in Ekaterinburg, and only 17 species (including seven phytopathogenic
ones) are known in Primorsky province [37].
The mycobiota of vine species in Ekaterinburg City is not only unexpectedly rich but
also is biogeographically heterogeneous (Section 3.3), including both boreal and cosmopoli-
tan species, as well as many tropical and subtropical East Asian and European species. At
least 15 species of macrofungi and 48 species of microfungi have been found exclusively on
alien vines in Ekaterinburg City and Sverdlovsk province.
The overwhelming majority of the East Asian and North American vines were initially
introduced in Ekaterinburg in the form of seeds that were germinated and grown in
seedlings in greenhouses. Therefore, we can suppose that alien phytopathogenic microfungi
have been introduced via infested seeds. Quite likely, the fungi first spread on host plants in
greenhouses, and then in outdoor plantings in Ekaterinburg City and Sverdlovsk province.
The spreading of highly specialized phytopathogenic microfungi with windborne spores
over thousands of kilometers seems less likely, excluding rust and smut fungi [
38
,
39
], but
these taxa were not recorded on the vines in Ekaterinburg City.
On the other hand, the main pathway for the spreading of wood-inhabiting macro-
fungi is wind-mediated spore dispersion [
38
], and for this reason, many macrofungi have
very wide or cosmopolitan ranges. Such species prevail among the vine-associated macro-
fungi in our research, especially common tropical and subtropical East Asian and European
saprobic macrofungi: Crustomyces expallens,Gloeohypochnicium analogum,Hydnophlebia
chrysorhiza,Lilaceophlebia cf. ochraceofulva,Mycoacia uda,Steccherinum bourdotii, and To-
mentella olivascens. Obviously, these species have entered Ekaterinburg in the 2010s, most
likely as a consequence of global warming, which has accelerated the growth of vines and
thereby led to the sufficient accumulation of live and mortal biomass—the substrates for
saprobic and phytopathogenic fungi. Thus, the alien vine species retained only a weak
biogeographical specificity for macrofungi. However, microfungi show a different pattern:
highly host-plant-specialized fungal taxa predominate.
4.2. Dynamics of the Model Groups during the Last 40 Years
The number of macrofungal species known on woody vines in Ekaterinburg has
increased by 37% in the last 40 years: from 60 species in the 1970s to 95 species in the 2010s.
At the same time, the number of known fungal species on herbaceous vines has increased
much less (p= 0.256), and the average species richness has changed insignificantly, from
3.3 to 4.6 species (Figure 8). Contrariwise, the average number of known species on woody
vines has increased significantly (by 52%), from 6.6 to 13.7 species, while the covered area
of woody vine species in the city has increased five times in the 40 years, and the covered
area of herbaceous vine species—about three times.
Apparently, such a high revealed fungal diversity is not only the result of our high
selective effort, but also the consequence of the increase in the biomass of host plants—woody
vines—due to climate warming. The “overgrowing” of woody vines (such as grapes) also
leads to the accumulation of a large amount of mortal mass, especially considering that
sanitary pruning of dry twigs and branches in some unkempt gardens and vineyards has
not been performed since the 1990s. Therefore, many overgrown woody vines (grapes,
hardy kiwi, and magnolia vine) have been in the unkempt state for over 20 years. We found
the largest number of fungi on lignified debris in abandoned vine thickets. Only a few
species of fungi were found in stands where dead plant parts were regularly pruned and
removed. For example, 10 phytopathogenic and 27 saprobic fungal species were found
on an Amur grape vine in an abandoned garden (A.G. Shiryaev, E.V. Sinitsyn, pers. data),
while only five phytopathogenic and eight saprobic fungal species have been recorded on a
similar Amur grape vine in a same area in a neighboring garden. In the latter-mentioned
garden, the trellis was being annually cleaned—all dead parts of grapevine were being
annually pruned and removed during the last 20 years (the recorded yields are presented
on Figure 4).
Forests 2022,13, 323 18 of 22
The morphological structure of macrofungal communities has been transformed in
the last 40 years too. The majority of East Asian and North American woody vine species
were introduced in the city in the early 1960s, so in those years they had only young and
thin branches and twigs, on which only saprobic species with small basidiomata (mainly
corticioid and clavarioid) could grow. Their mortal mass (branches and twigs thickness)
had much increased by the end of the 1970s, when the vines were 15–18 years old. In this
regard, the poroid and agaricoid macrofungi with larger basidiomata, including perennial
phytopathogenic poroid species, began to grow on them. The morphological structure of
macrofungal community changed in the 2010s (40 years later) as a result of increasing of
the areas covered by vines, their age, and the bio- and mortal mass. The number of poroid
and corticioid macrofungi has increased more than others, while the number of clavarioid
species remained almost the same. Consequently, the proportion of poroids increased,
while the proportion of corticioids decreased. The number of recorded saprobes on wood
and litter also increased: the species richness of these two groups almost doubled, while
the number of phytopathogenic fungi increased by a third only. These results indicate that
the data were received correctly in the 1970s, and this fact makes it possible to compare
them with the data for the 2010s. Moreover, not only has the number of aphyllophoroid
phytopathogens increased after 40 years, but agaricoid fungi causing trunk rots of woody
vines have also appeared [8].
4.3. Pathogenic Fungi on Alien Edible Vines
The frontier of viticulture is shifting to the north as the climate in the Urals and Siberia
warms [
5
]. At the beginning of the 20th century, the grapes were grown as edible plants
only in the south of the Ural macroregion (for example, in Orenburg city, 51–53
◦
N, 500 km
south of Ekaterinburg). However, the zone of home viticulture has expanded 250 km to the
north in the middle of the 20th century (to the latitude of Ufa City, 54
◦
N), and has reached
Ekaterinburg (56◦N) in the early 21st century [5].
For 150 years of grape cultivation in Ekaterinburg, 32 species of phytopathogenic
fungi were recorded on the Vitaceae plants (Parthenocissus and Vitis species), including
13 macrofungal species (Table 1). Some of them, for example, Fomitiporia punctata,In-
onotus hispidus,Phellinopsis conchata,Pleurotus pulmonarius,Stereum hirsutum,Armillaria,
and Pholiota species, are common plant pathogens within the natural and cultural ranges
of grapes [
40
]. However, 19 species of recorded phytopathogenic microfungi (Coniella
diplodiella,Erysiphe necator,Phyllosticta ampelicida,Pseudocercospora vitis, and others) are
widespread common species within the natural and cultural ranges of grapes, but these
fungi were never found in natural boreal plant communities in Ural and Siberia. The
number of known phytopathogenic fungal species in Vitaceae plants has increased by a
third in the last 40 years, while the covered area of Vitaceae plants has increased in five
times (Table S1). Therefore, the current ratio of phytopathogenic micro- and macrofungi is
60 to 40%. Moreover, all phytopathogenic macrofungi found in Vitaceae plants are native
species growing on native deciduous trees, but all phytopathogenic microfungi are alien
species and mainly highly specialized plant parasites of Vitaceae plants—common within
their modern ranges but never recorded on native plants in the Ural macroregion.
More than 400 species of fungi associated with Vitaceae plants are known in the world,
of which at least 70 species are recorded in Europe as plant pathogens [
40
,
41
]. Dozens
of species of phytopathogenic fungi growing on the twigs and leaves of Vitaceae plants
are also known in the geographically close regions of long-term viticulture—mountain
foothills of Central Asia, Southern European Russia, and South Caucasus [
42
]. For example,
29 microfungal species (97%) and only one macrofungal species (3%) are known now as
grape pathogens in the arid subtropical climate of Uzbekistan, in the desert zone of Central
Asia ([
43
,
44
]; Y. Gafforov, pers. comm.). Similarly, 50 species of fungi are known on grapes
in the semiarid temperate climate of Rostov province (Southern European Russia, steppe
zone of Eastern Europe) ([
45
]; T. Bulgakov, pers. comm.), including 45 microfungal species
(90%) and only five macrofungal species (10%). Thus, we can state that the percentage and
Forests 2022,13, 323 19 of 22
the significance of phytopathogenic macrofungi on grapes increases (from 3 to 40%) from
dry subtropics (Central Asia) to the semihumid boreal zone (the Urals and Siberia) parallel
to a decrease in the average annual temperature and an increase in precipitation from south
to the north.
Higher relative air humidity (rains in the warm seasons and snowfalls in winters) in
Ekaterinburg City is the main climatic factor that could explain the greater number and
proportion of macrofungal species in Ekaterinburg in comparison with other mentioned
regions of ancient grape culture. In the boreal zone, the macrofungi often grow on root
collars near wet soil surface, or on trunk at low height above the ground (at the level of
snow in a winter season), or in frost cracks in the middle part of the vine trunk. Thus,
analyzing the species richness and morphological spectrum of phytopathogenic micro-
and macrofungi for the three compared regions with a relatively close level of knowledge
of phytopathogenic grape fungi, we obtained an interesting result that requires further
research and interpretation.
The other economically important vine species in Ekaterinburg are plants of Cucur-
bitaceae family (mainly pumpkins and cucumbers), which have been cultivated here for
300 years. The species composition of cultivated Cucurbitaceae formed a long time ago
and does not change in modern time; therefore, the species composition of associated
phytopathogenic fungi stabilized many decades ago and remains the same nowadays.
Therefore, 84% of all recorded fungal phytopathogens in Cucurbitaceae plants were already
known in Ekaterinburg 40 years ago (for example, Cladosporium cucumerinum,Golovinomyces
tabaci,Podosphaera xanthii, and others). However, Rhizoctonia solani was not recorded in
Sverdlovsk province as pathogen of these plants until the late 1950s, but by then it had
started to affect Cucurbitaceae plants regularly. Some species, such as Typhula culmigena,
Septoria cucurbitacearum, and Verticillium alboatrum, were not previously recorded in Ekater-
inburg either. We should note the recent appearance of Colletotrichum orbiculare causing
the anthracnose of cucumbers and pumpkins, which has become a common species now
wherever the host plants cultivate. As in the case of Vitaceae, highly specialized phy-
topathogenic microfungi of Cucurbitaceae are mostly alien species for the region, but all
recorded macrofungi are native species.
The list of known phytopathogenic fungi on annual Cucurbitaceae plants has increased
by only 16% in the last 40 years, but the list of fungal pathogens in Vitaceae plants has
increased much more (by 37%) during the same period, and many new wood-inhabiting
macrofungi affecting old grape twigs, branches, and trunk were first found in Ekaterinburg
in the 2010s. We assume that this is the result of aging of grape plants and the accumulation
of mortal plant mass, mainly wood. Thus, the recorded 32 species of phytopathogenic
fungi in Vitaceae plants and 19 ones in Cucurbitaceae plants are relatively large numbers
for an area of 468 km
2
, located far beyond the natural ranges of the host plants. Such results
can be explained by the high level of selective effort as well as the pessimal conditions for
the growth of the vines. Such a large number of recorded wound phytopathogens can be
considered as evidence of a weakened state of vines, which have regularly been damaged
by frost in cold winters. We must also take into account the long history of the host plants’
cultivation in the region, which should inevitably lead to an increase in trophic connections
between native fungi and alien plants as substrates for fungi.
The species composition of phytopathogenic fungi recorded on both plant families in
Ekaterinburg is more constant and similar to the one in their natural and cultural ranges
than the species composition of saprobic fungi. We attribute this to the closer and more
specific trophic connection between phytopathogenic fungi and their host plants (especially
for obligate plant parasites); more so, a similar pattern is shown for other regions of the
planet [46,47].
5. Conclusions
Based on the results of this study, specific morphological features of the vines (i.e.,
special adaptations that help to maintain orthotropic growth of shoots) do not significantly
Forests 2022,13, 323 20 of 22
affect their colonization by fungi. The main factor predetermining the presence and growth
of wood-destroying fungi is a specific substrate—lignified tissues and organs of host
plants (trunks, branches, and twigs of woody vines)—while the presence of living plant
parenchyma is the main factor predetermining the presence and growth of phytopathogenic
microfungi that infect nonlignified tissues and organs of host plants.
The macrofungal species recorded on woody vine species in Ekaterinburg include
both native and widespread (often cosmopolitan) taxa, although some nonnative (alien)
species are also present (mostly East Asian subtropical and tropical species). Contrar-
ily, the recorded microfungal species are mainly highly host-specialized phytopathogens
(growing mainly on leaves and other nonlignified plant parts), and they mostly can be
considered as alien species strictly associated with genera and families of host plants in
their natural ranges.
The number of phytopathogenic fungal species recorded on herbaceous vines (includ-
ing Cucurbitaceae) has not increased significantly over the past 40 years. This fact can
be explained by the long history of their cultivation in Ekaterinburg, starting from the
18th–19th centuries: the mycobiota of the herbaceous vines had time to form and stabilize
over this time, in contrast with the mycobiota of woody vines.
The situation is quite different with woody vines: the warming climate contributes
to an increase in their species diversity, covered area and age, thickness of trunks and
branches, and also leads to an increase in the mass of wood and lignified debris, which
are the main substrates for vine-associated macrofungi. Due to these factors, the num-
ber of recorded phytopathogenic macrofungal species has grown by a third in the last
40 years
. Previously absent macrofungi with large basidiomata (perennial poroids) have
now appeared, although saprobic macrofungi with small annual basidiomata (corticioids)
are still predominant.
The total number of vine-associated macrofungal species is 1.1–3.2 times higher in
Ekaterinburg compared to the regions located along the northern border of the natural
ranges of many considered woody vine species, while the species diversity and composition
of recorded phytopathogenic fungi are similar to the species diversity and composition
typical for well-studied regions—the nearest regions of ancient culture of the studied
vine species (the Mediterranean, the south of the European Russia and the Caucasus,
Central Asia, the south of the Russian Far East and Northern China). Consequently,
the results of this study demonstrate that the tested hypothesis that poor fungal species
diversity on alien vine species (cultivated far away from their natural ranges) has not been
confirmed, or it needs to be corrected. However, the main reason for this may be poor
knowledge of the mycobiota of the vine species in some European and Central and East
Asian regions near the northern border of the natural and traditional cultural ranges of
the woody vine species. Nevertheless, we can state that the current expansion of many
vine-associated fungal species (including phytopathogenic ones) occurs simultaneously
with the expansion of vine culture zone to the north in the Ural macroregion, caused by
the current climate warming. This process will undoubtedly lead to significant economic
losses for the regional agriculture.
Supplementary Materials:
The following supporting information can be downloaded at: https://
www.mdpi.com/article/10.3390/f13020323/s1, Figure S1. June snowfall in Ekaterinburg city in 1973
and 1967. Figure S2. 17 most fungal-rich vines in Ekaterinburg city (on which more than
5 species
of fungi are recorded). Table S1. 100-years long covered area (m
2
) dynamic of woody vines in
Ekaterinburg city. Table S2. The checklist of macrofungi collected on vines in Ekaterinburg (incl.
subdivision in morphological and ecological groups) with a small addition. Table S3. The checklist of
pathogenic micro- and macrofungi collected on live vines in Ekaterinburg.
Author Contributions:
A.G.S.: Conceptualization, methodology, investigation, formal analysis,
data curation, writing—original draft, writing—review and editing, project administration, funding
acquisition. I.V.Z.: Methodology, formal analysis, writing—review and editing. T.S.B.: Methodology,
formal analysis, investigation, conceptualization, writing—review and editing. O.S.S.: Formal
Forests 2022,13, 323 21 of 22
analysis, investigation, visualization, writing—review and editing. L.M.D.: Investigation, writing—
review and editing. All authors have read and agreed to the published version of the manuscript.
Funding:
The research was carried out with the financial support of Russian Science Foundation
(project No. 22-26-00228).
Data Availability Statement:
The data presented in this study are available on request from the
corresponding author. The data are not publicly available due to privacy.
Acknowledgments:
We would like to thank the anonymous reviewers for their comments on an
earlier version of the manuscript. We are deeply grateful to the staff of the Botanical Garden UB RAS
O.A. Kiseleva and E.N. Minogina. We very much appreciate N.G. Erokhin for valuable advice on
the history of Ekaterinburg City, as well as the staff of the Ekaterinburg History Museum. We are
deeply grateful to E.V. Sinitsyn for providing personal data on grape yield. We thank Yu. Gafforov for
personal data on the list of fungal species collected on grapes in Uzbekistan. The authors are grateful
to K. Lynn and M. Bradshaw for their help in improving English text. We are deeply appreciative of
the constructive comments from the editor and anonymous reviewers.
Conflicts of Interest:
The authors declare that they have no known competing financial interests or
personal relationships that could have appeared to influence the work reported in this paper.
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