Comparative Analysis of Foliar Diseases of Some Native and Non-Native Tree Species in Belarus and Siberia

Abstract

Urban green spaces are known to be subjected to additional anthropogenic stress. Using native plants in monoculture, i.e., planting trees of the same species, may favour disease outbreaks and plant death. Non-native plants to be used in large cities for creating sustainable plantations are being searched for worldwide. Meanwhile, it is necessary to control plant pathogens in the variable conditions of the region and natural habitat. In Siberian cities, non-native European trees are used, and non-native Siberian plants are introduced in Belarus. This article reports long-term observations of foliar fungal pathogens attacking 21 woody plants (19 European, 2 Siberian) in Siberian and Belarusian cities. In both regions, 48 leaf fungal pathogens were detected, with powdery mildew fungi predominating in Belarus and leaf spotting fungi prevailing in Siberia. In both research regions, the greatest number of fungal species was found on Syringa vulgaris L. In Siberia, many pathogens were found on the non-native European plant Berberis vulgaris (9 species) and native plant Caragana arborescens Lam. (8 species). We have not detected the pathogens on European plants: Acer campestre L., Acer platanoides L., Euonymus europaeus L., Lonicera caprifolium L. in urban green areas in Siberia, while we have identified one to four foliar fungal pathogens on these plants in Belarus. To sum up: more pathogens were found on native plants in Siberia and Belarus; some leaf pathogen species ( Sawadaea tulasnei (Fuckel) Homma , Erysiphe alphitoides (Griffon & Maubl.) U. Braun & S. Takam. , Cladosporium syringae (Oudem.) Montem. , Erysiphe syringae Schwein. , Erysiphe palczewskii (Jacz.) U. Braun & S. Takam.) followed their host plants ( Acer tataricum L. , Syringa vulgaris L. , Caragana arborescens Lam.) when introduced into new areas; and some local pathogens were also observed to spread to the non-native plants of closely related species.

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ISSN 1995-4255, Contemporary Problems of Ecology, 2023, Vol. 16, No. 2, pp. 217–229. © The Author(s), 2023. This article is an open access publication.
Comparative Analysis of Foliar Diseases of Some Native
and Non-Native Tree Species in Belarus and Siberia
M. A. Tomoshevicha, *, D. Belomesyatsevab, **, E. V. Banaeva, I. G. Vorob’evaa, and T. Shabashovab
a Laboratory of Dendrology, Central Siberian Botanical Garden, Siberian Branch, Russian Academy of Sciences,
Novosibirsk, 630090 Russia
b Laboratory of Mycology, V.F. Kuprevich Institute of Experimental Botany, Minsk, 220072 Republic of Belarus
*e-mail: arysa9@mail.ru
**e-mail: dasha_belom@yahoo.com
Received November 28, 2022; revised December 8, 2022; accepted December 17, 2022
Abstract—Urban green spaces are known to be subjected to additional anthropogenic stress. Using native
plants in monoculture, i.e., planting trees of the same species, may favour disease outbreaks and plant death.
Non-native plants to be used in large cities for creating sustainable plantations are being searched for world-
wide. Meanwhile, it is necessary to control plant pathogens in the variable conditions of the region and nat-
ural habitat. In Siberian cities, non-native European trees are used, and non-native Siberian plants are intro-
duced in Belarus. This article reports long-term observations of foliar fungal pathogens attacking 21 woody
plants (19 European, 2 Siberian) in Siberian and Belarusian cities. In both regions, 48 leaf fungal pathogens
were detected, with powdery mildew fungi predominating in Belarus and leaf spotting fungi prevailing in
Siberia. In both research regions, the greatest number of fungal species was found on Syringa vulgaris L. In
Siberia, many pathogens were found on the non-native European plant Berberis vulgaris (9 species) and
native plant Caragana arborescens Lam. (8 species). We have not detected the pathogens on European plants:
Acer campestre L., Acer platanoides L., Euonymus europaeus L., Lonicera caprifolium L. in urban green areas
in Siberia, while we have identified one to four foliar fungal pathogens on these plants in Belarus. To sum up:
more pathogens were found on native plants in Siberia and Belarus; some leaf pathogen species (Sawadaea
tulasnei (Fuckel) Homma, Erysiphe alphitoides (Griffon & Maubl.) U. Braun & S. Takam., Cladosporium
syringae (Oudem.) Montem., Erysiphe syringae Schwein., Erysiphe palczewskii (Jacz.) U. Braun & S. Takam.)
followed their host plants (Acer tataricum L., Syringa vulgaris L., Caragana arborescens Lam.) when intro-
duced into new areas; and some local pathogens were also observed to spread to the non-native plants of
closely related species.
Keywords: fungi, plant-host, alien species, native species, geographic distribution, damage, frequency
DOI: 10.1134/S1995425523020166
Woody plants are of particular importance for
urban green spaces since they form the structure of
gardens and parks, create a long-term shape of land-
scape objects, have a significant artistic impact, and
considerably affect the microclimate and sanitary
conditions of urban areas. The state of woody plants in
urbanized areas largely determines the quality of the
environment, the aesthetics of the urban landscape,
and the physical and psycho-emotional health of
urban residents. However, species sustainability and
the extent of the impact of urban environmental fac-
tors on vegetation are known to influence the physio-
logical state of plants, their ornamental features, lon-
gevity in gardens and parks (Sucharzewska, 2010;
Timofeeva, 2014; Kumar, 2018; Desprez-Loustau et al.,
2019; Faticov et al., 2020). The range of plants used in
urban green areas tends to include native woody plants.
More than 50% of native plants in plantings contribute
to the development of more pathogens (Tomoshevich,
2019). Using plant monocultures favour disease out-
breaks and the consequent mortality of trees in urban
green areas (Heiniger and Rigling, 1994; Brasier and
Buck, 2001; Brasier and Kirk, 2010; Buiteveld et al.,
2015; Jurisoo et al., 2019; Selikhovkin et al., 2020).
Non-native trees are planted in urban greeneries in
both Europe and Asia. The global practice of intro-
ducing non-native species, varieties, and forms of trees
and shrubs in the landscaping of large cities has shown
the need for multi-species plantations (various species
of native and non-native woody plants) that are more
resistant to pathogenic complexes (Koropachinskii
et al., 2011). Non-native plants have been reported to
be more resistant, at least at the first stages of intro-
duction, due to differences in phases of ontogenesis
of plants and local harmful species, the absence of
syngenetic pathogens at the new site, and some other
factors (Tomoshevich, 2009; Tomoshevich and
Banaev, 2013).

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TOMOSHEVICH et al.
However, research indicates the possibility for new
variants of pathogen complexes to emerge and their
infectious potential to increase ex situ (Lebeda et al.,
2008; Takamatsu et al., 2016; Jakuschkin et al., 2016;
Yin et al., 2020).
Studies conducted in Siberian cities found that
among non-native species, the highest resistance was
in plants of Far Eastern and North American origin
(Tomoshevich, 2019; Tomoshevich and Banaev, 2013).
European non-native plants in Siberia proved to have
variable resistance to leaf pathogens. It is unclear
whether the plant resistance to pathogens is due to the
specific characteristics of the plant species or to the
climate impact. In this regard, it is worth investigating
and comparing the species composition of pathogens,
taking into account their damage, on European plants
in their homeland (Europe) and in the new climatic
conditions, in Siberia. In European conditions, urban
green areas of Belarusian cities feature the key factor
for comparing the species composition of leaf patho-
gens, i.e., the similar principles in urban planting and
the maximum contrasting climatic conditions. Of par-
ticular interest are European plants Quercus robur L.
and Syringa vulgaris L., widely introduced into urban
green spaces in Siberian cities in recent years, and
Siberian plants Caragana arborescens Lam. and Rham-
nus cathartica L., becoming increasingly common in
Belarusian cities.
At the first stages, it is essential to identify the species
composition of leaf pathogens of woody plants, the
damage caused, and the frequency of occurrence. It is
known that some pathogens that follow their host plant
may fail to adapt to local climatic conditions or manifest
themselves in some years under specific weather condi-
tions and cause damage (Tomoshevich, 2019).
In this article, we summarize observations of leaf
pathogens that attack European and Siberian woody
plant species in urban green spaces in Siberia and
Belarus (Europe), taking into account that European
woody plants are non-native to Siberia and Siberian
woody plants are non-native to Belarus (Europe). We
also discuss how the species composition of pathogens
on European non-native plants in Siberian cities will
differ compared to the same plants in urban planta-
tions in Belarus, where European plants are native.
Moreover, we consider how non-native plants without
close relatives in the local flora are affected by leaf
pathogens and discuss the potential for new pathogens
to be found that may pose a threat to native and non-
native woody plants, both in Siberian and in Belaru-
sian (European) conditions.
MATERIALS AND METHODS
Collecting Samples in Urban Green Areas
In 5 Siberian cities, 19 European plants were used
in urban plantations, while only two Siberian woody
plants were found in urban green spaces in Belarus; all
these species were taken as model plants for research
(Table 1).
Phytopathological surveys of 21 species of woody
plants (19 European and 2 Siberian) were conducted
annually in Siberian cities (Novosibirsk, Krasnoyarsk,
Barnaul, Tomsk, Kemerovo) and Belarusian cities
(Baranovichi, Braslav, Brest, Vitebsk, Gomel, Grodno,
Dzerzhinsk, Minsk, Orsha, Polotsk, Soligorsk) (Fig. 1).
Inspection and sampling was continuously con-
ducted for 19 years (2000–2018) throughout the
summer periods in all cities. The following categories
of urban green spaces were considered: parks,
squares, gardens, highways, boulevards, territories
adjacent to the house, intra-quarter territories, street
plantings, etc. Trees and shrubs in all urban green
areas (more than 100 plantation objects), including
arboreta, were studied. In different parks, one woody
plant species was found to be represented by a differ-
ent number of specimens (from 3 to 50). At each
plantation object, all plants of the same species were
examined from four cardinal directions, large trees
up to 2 m from the ground. The leaves with symptoms
of the disease were incorporated into the herbarium.
When examining woody plants, we made the records
of disease damage. The plant damage area was evalu-
ated according to a special scale: 1 point, 1–10%
damage; 2 points, 11–25%; 3 points, 26–50%; and
4 points, >50% (Dudka et al., 1982).
Given the heterogeneous occurrence of woody
plants in different categories of urban green spaces in
Belarus and Siberia, we provide a general profile of the
occurrence of plants in the study area in Table 1.
Microscopy and Identification
of Pathogens
Sections of fruit bodies were made with a blade and
examined under an Olympus SZ51 binocular micro-
scope. Preparations of dry samples for further micros-
copy were prepared in a mixture of glycerol and alco-
hol, in a 3% KOH solution, and in distilled water.
Erythrosine was used to increase the contrast of a
number of preparations. Pathogens were identified
using Zeiss Discovery V4, Olympus CX31, and Nikon
Eclipse E200 microscopes. More than 1500 samples
were examined during the study. When possible, the
nomenclature corresponds to Index Fungorum, 2021
(www.indexfungorum.org). Siberian samples of foliar
fungal pathogen species that were collected in this
study are stored in the Central Siberian Botanical
Garden of the Siberian Branch of the Russian Acad-
emy of Sciences (Herbarium of the Laboratory of
Dendrology, NSC Collection). Belarusian samples
are stored at V.F. Kuprevich Institute of Experimental
Botany of the National Academy of Science of Belarus
(Herbarium of the MSC-F mycology laboratory).

CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 16 No. 2 2023
COMPARATIVE ANALYSIS OF FOLIAR DISEASES 219
Table 1. Frequency of woody plant occurrence in urban green areas of Siberia and Belarus
1 Widely spread, 81–100%; frequent, 41–80%; rare, 11–40%; very rare, 1–10%.
Woody plant species Plant occurrence in urban green areas1
Siberia Belarus
Acer campestre L. Very rare
non-native plant
Rare
Acer platanoides L. Very rare
non-native plant
Widely spread
native plant
Acer tataricum L. Frequent
non-native plant
Frequent
native plant
Alnus glutinosa (L.) Gaertn. Very rare
non-native plant
Frequent
native plant
Alnus incana (L.) Moench Very rare
non-native plant
Frequent
native plant
Berberis vulgaris L. Widely spread
non-native plant
Frequent
native plant
Chamaecytisus austriacus (L.) Link Very rare
non-native plant
Rare
Chamaecytisus ruthenicus
(Fisch. x Woloszcz.) Klaskova
Rare
non-native plant
Frequent
Crataegus nigra Waldst. & Kit. Very rare
non-native plant
Rare
Euonymus europaeus L. Very rare
non-native plant
Frequent
native plant
Lonicera caprifolium L. Very rare
non-native plant
Frequent
Lonicera nigra L. Very rare
non-native plant
Rare
Quercus robur L. Widely spread
non-native plant
Frequent
native plant
Rosa glauca Pourr. Rare
non-native plant
Rare
Salix acutifolia Willd. Very rare
non-native plant
Frequent
native plant
Salix daphnoides Vill. Very rare
non-native plant
Rare
Syringa josikaea J. Jacq. ex Rchb. Widely spread
non-native plant
Very rare
Syringa vulgaris L. Widely spread
non-native plant
Widely spread
Viburnum lantana L. Rare
non-native plant
Rare
Caragana arborescens Lam. Widely spread
native plant
Frequent
non-native plant
Rhamnus cathartica L. Widely spread
native plant
Frequent
non-native plant
Interpretation and Analysis of Results
The following parameters were applied to assess
the damage and occurrence of each pathogen on
European and Siberian species of woody plants in
green areas of Siberia and Belarus cities: A: pathogen
is detected irregularly, i.e., not every year or not in
every place where the plant is found; B: detected
annually and in all places where the plant grows.
A Mann–Whitney U-test was used to compare the
series of data on the number of pathogens on leaves
of woody plants.

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TOMOSHEVICH et al.
Fig. 1. Map of the locations in Belarus and Siberia (Russia) where the samples of infection on trees and shrubs were collected,
and boundaries of neighboring countries.
Norw.
Sweden
Finland
Pol.
Belarus
Belarus
Moscow
Ukr.
G.
Az.
Russia
Kazakhstan
Novosibirsk
Toms k
Kemerovo
Barnaul
Krasnoyarsk
Vladivostok
Grodno
Brest
Baranovichi
Minsk
Braslav
Polotsk
Vitebsk
Dzerzhinsk
Soligorsk
Orsha
Gomel
RESULTS
Foliar fungal pathogens were found on 21 (19 Euro-
pean and 2 Siberian species) woody plant species
inspected (Table 2). A total of 48 fungal species were
detected, with 18 causing leaf spot; 17 species being
powdery mildews, 7 species—saprotrophic fungal,
5 species—rusts, and one—fungal species, Taph r ina
acerina A.G. Eliasson, which caused leaf deformation.
At the same, in green plantings of Siberian cities,
no pathogens were found on five European woody
plants: Acer campestre, A. platanoides, Euonymus euro-
paeus, Lonicera caprifolium, L. nigra. In cities and
parks of Belarus, from one to four pathogens were reg-
istered on these species (Fig. 2). Syringa vulgaris was
found to be the most affected species in both regions
of the study. In Siberia, Berberis vulgaris (European
woody plants) were infected by nine pathogens, and
Caragana arborescens (native Siberian woody plants)
by eight pathogens. While, in Belarus, Berberis vulgaris
were infected by six pathogens and Caragana arbo-
rescens by two pathogens.
Significant differences have been revealed in the
number of pathogens on native and non-native
plants. Non-native plants showed a lower number of
pathogens, averaging 1.89 ± 0.57, whereas native
plants showed 2.31 ± 0.43 (Mann–Whitney test
Z=2.01, p = 0.04).
In Siberian cities, the fungal-caused leaf spot, scab,
and similar diseases are dominant (52%), while in
Belarusian cities, powdery mildews were found to pre-
vail (48%) (Fig. 3).
In Belarus, 35 pathogens were registered, with
15 not reported in Siberian cities (Table 2). In Siberia,
a total of 29 species of fungi were detected, with 13 of
them found only in Siberian cities. Twenty species of
micromycetes were found on woody plants in both
study regions, with 43% of them being powdery mil-
dew fungi distributed on species: Acer tataricum, Ber-
beris vulgaris, Chamaecytisus austriacus, Chamaecyti-
sus ruthenicus, Quercus robur, Salix acutifolia, Salix
daphnoides, Syringa josikaea, Syringa vulgaris, Cara-
gana arborescens (Table 2). Four pathogens (Erysiphe
lonicerae, Erysiphe penicillata, Podosphaera pannosa,
Sawadaea bicornis) were also found in both study
regions, but they do not occur on European woody
plants in Siberia.
DISCUSSION
Leaf Pathogens Affecting Non-Native and Native Plants
We found that both in Siberia and Belarus, a greater
number of pathogens were found on native plants. Sibe-
rian woody plant species in green spaces of Belarusian
cities were found to be attacked by 1–2 pathogens,
whereas in Siberia, 4–9 pathogens were registered on
them. In Siberia, European woody plants were also
infected with fewer fungal species (more often,
1‒2 fungus species) than in Belarusian cities. The
most significant differences were identified for Acer
platanoides that was not affected in Siberia but was
infested by four pathogens in Belarus and for Cara-
gana arborescens that was in contrast affected in Sibe-
ria by eight pathogens and in Belarus by two patho-

CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 16 No. 2 2023
COMPARATIVE ANALYSIS OF FOLIAR DISEASES 221
Table 2. Foliar fungal pathogens found on European and Siberian woody plant
Pathogen species recorded on woody plants Urban green areas with presence of pathogens
Siberia Belarus
Acer campestre
Sawadaea bicornis (Wallr.) Homma –†Minsk
Acer platanoides
Rhytisma acerinum (Pers.) Fr. – Widespread
Sawadaea bicornis (Wallr.) Homma – Widespread
Sawadaea tulasnei (Fuckel) Homma – Widespread
Tap hrin a aceri n a A.G. Eliasson – Minsk
Acer tataricum
Sawadaea bicornis (Wallr.) Homma – Minsk
Sawadaea tulasnei (Fuckel) Homma Widespread Minsk‡
Alnus glutinosa
Cladosporium cladosporioides (Fresen.) G.A. de Vries – Soligorsk
Erysiphe penicillata (Wallr.) Link – Widespread
Melampsoridium hiratsukanum S. Ito ex Hirats. – Minsk
Mycopappus alni (Dearn. & Barthol.) Redhead & G.P. White Novosibirsk –
Phyllactinia alni Y.N. Yu & S.J. Han – Minsk
Alnus incana
Erysiphe penicillata (Wallr.) Link – Widespread
Melampsoridium hiratsukanum S. Ito ex Hirats. – Minsk
Mycopappus alni (Dearn. & Barthol.) Redhead & G.P. White Novosibirsk –
Phyllactinia alni Y.N. Yu & S.J. Han – Orsha‡
Berberis vulgaris
Alternaria alternata (Fr.) Keissl. Widespread Minsk
Cladosporium herbarum (Pers.) Link Novosibirsk Minsk
Erysiphe berberidis DC. Widespread Widespread
Kabatiella berberidis (Cooke) C.G. Shaw & Arx = [Gloeosporium ber-
beridis Cooke]
Novosibirsk, Krasnoyarsk –
Fumago vagans Pers. = [Leptoxyphium fumago (Woron.) R.C. Srivast.] Novosibirsk, Kras-
noyarsk, Kemerovo
–
Phyllosticta westendorpii Thum. Novosibirsk –
Puccinia graminis Pers.Widespread Widespread
Sphaerulina berberidis (Niessl) Quaedvl., Verkley & Crous = [Septoria
berberidis Niessl]
Novosibirsk Minsk
Ascochyta berberidina Sacc Novosibirsk Minsk, Brest
Chamaecytisus austriacus
Erysiphe trifoliorum (Wallr.) U. Braun Novosibirsk Minsk
Pleiochaeta setosa (Kirchn.) S. Hughes Novosibirsk –
Chamaecytisus ruthenicus
Erysiphe trifoliorum (Wallr.) U. Braun Widespread Gomel, Dzerzhinsk
Fumago vagans Pers. = [Leptoxyphium fumago (Woron.) R.C. Srivast.] Novosibirsk –
Ascochyta borjomi Bondartsev Novosibirsk –
Phyllosticta caraganae P. Syd . No v o s i b i r sk –
Pleiochaeta setosa (Kirchn.) S. Hughes Novosibirsk –
Crataegus nigra
Coryneum foliicola Fuckel Krasnoyar sk –
Euonymus europaeus
Erysiphe euonymi DC.–Vitebsk‡
Lonicera caprifolium
Erysiphe lonicerae DC. – Minsk
Lonicera nigra
Erysiphe lonicerae DC. – Minsk
Quercus robur
Alternaria alternata (Fr.) Keissl. Widespread Minsk
Cladosporium macrocarpum Preuss. Novosibirsk Minsk, Brest Gomel
Dendrostoma leiphaemia (Fr.) Senan. & K.D. Hyde = [Gloeosporium
quercinum Westend.]
–Brest
Erysiphe alphitoides (Griffon & Maubl.) U. Braun & S. Takam. Widespread Widespread

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CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 16 No. 2 2023
TOMOSHEVICH et al.
gens. This fact was confirmed by other researchers
who found fewer plant pathogens on non-native plants
than on native plants (Mitchell and Power, 2003;
Kleunen and Fischer, 2009).
Analysis of the Species Composition of Pathogens Found
on European Plants in Siberia and Belarus (Europe)
At the same, in green plantings of Siberian cities,
no pathogens were found on five European woody
plants: Acer campestre, A. platanoides, Euonymus euro-
paeus, Lonicera caprifolium, L. nigra. In cities and
parks of Belarus, from one to four pathogens were reg-
istered on these species (Table 2). Pathogens were not
found only on one species Crataegus nigra in urban
green areas in Belarus.
More surprisingly, four European woody plants
(non-native) in green plantings in Siberia had
4‒9 pathogens: Berberis vulgaris, Chamaecytisus
ruthenicus, Quercus robur, Syringa vulgaris (Table 2). It
† Pathogen not found; ‡ species identified by I.S. Girilovich (2018).
Fumago vagans Pers. = [Leptoxyphium fumago (Woron.) R.C. Srivast.] Widespread –
Septoria quercina Desm.–Brest
Rosa glauca
Botrytis cinerea Pers. – Minsk
Passalora rosae (Fuckel) U. Braun Krasnoyarsk –
Phragmidium mucronatum (Pers.) Schltdl. – Minsk
Podosphaera pannosa (Wallr.) de Bary – Minsk
Salix acutifolia
Erysiphe adunca (Wallr.) Fr. Novosibirsk Minsk
Salix daphnoides
Erysiphe adunca (Wallr.) Fr. Novosibirsk Minsk
Syringa josikaea
Erysiphe syringae Schwein. Widespread Minsk
Erysiphe syringae-japonicae (U. Braun) U. Braun & S. Takam.–Minsk‡
Cladosporium syringae (Oudem.) Montem. Novosibirsk –
Syringa vulgaris
Ascochyta syringae (Westend.) Bres. Novosibirsk Minsk
Capnodium citri Berk. & Desm. – Minsk
Cladosporium herbarum (Pers.) Link Novosibirsk Minsk
Cladosporium syringae (Oudem.) Montem. Novosibirsk –
Erysiphe syringae Schwein. Widespread Widespread
Fumago vagans Pers. = [Leptoxyphium fumago (Woron.) R.C. Srivast.] Krasnoyarsk, Tomsk
Novosibirsk
Brest
Septoria syringae Westend. Novosibirsk
Krasnoyarsk, Barnaul
Brest
Viburnum lantana
Cladosporium herbarum (Pers.) Link Novosibirsk –
Erysiphe hedwigii (Lév.) U. Braun & S. Takam. – Minsk, Brest, Grodno‡
Caragana arborescens
Erysiphe palczewskii (Jacz.) U. Braun & S. Takam. Widespread Minsk, Brest
Erysiphe robiniae Grev.–Minsk‡
Alternaria alternata (Fr.) Keissl. Novosibirsk –
Ascochyta borjomi Bondartsev Novosibirsk, Krasnoyarsk –
Cladosporium herbarum (Pers.) Link Novosibirsk –
Mycosphaerella jaczewskii Potebnia [=Septoria caraganae (Jacz.) Died.] Novosibirsk –
Fumago vagans Pers. = [Leptoxyphium fumago (Woron.) R.C. Srivast.] Widespread –
Phyllosticta caraganae P. Syd . No vosibirsk –
Uromyces cytisi J. Schröt. Novosibirsk, Kras-
noyarsk, Tomsk
–
Rhamnus cathartica
Erysiphe friesii (Lév.) U. Braun & S. Takam. – Baranovichi, Gomel‡
Phyllosticta cathartici Sacc. Novosibirsk –
Puccinia coronata Corda Novosibirsk –
Pathogen species recorded on woody plants Urban green areas with presence of pathogens
Siberia Belarus
Table 2. (Contd.)

CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 16 No. 2 2023
COMPARATIVE ANALYSIS OF FOLIAR DISEASES 223
may be due to the wide distribution of these woody
plants in plantations in Siberia (Table 1). Two of them—
Berberis vulgaris, Chamaecytisus ruthenicus—were
attacked by a greater number of leaf pathogens than in
green plantings in Belarus (Fig. 2).
Ascochyta borjomi and Phyllosticta caraganae, fungi
widespread on the Siberian native woody plant Cara-
gana arborescens, were found on Chamaecytisus ruthe-
nicus (non-native woody plant).
Of particular interest is the species Pleiochaeta
setosa, causing leaf spot and root rot on various herba-
ceous lupin species (Lupinus sp.). Pleiochaeta setosa, a
dangerous pathogen infesting lupin worldwide (Pau-
litz, 1992; Yang and Sweetingham, 2002; Garibaldi
et al., 2012; Gur and Om, 2015; Luckett et al., 2009),
was also registered in Belarus (Mikobiota Belorussko-
Valdajskogo poozer’ya, 2013). Nevertheless, the patho-
gen was found in Siberian greenspaces on the woody
plant Chamaecytisus ruthenicus in the medium degree
of damage (Fig. 4). Earlier, Pleiochaeta setosa was
detected on woody plants of the legume family: on
Genista tinctoria in Oregon (USA) (Sahakian, 1996) and
Chamaecytisus supinus (L.) Link. in Poland (Mułenko
et al., 2008).
Analysis of the Species Composition of Pathogens Found
on Siberian Plants in Siberia and Belarus (Europe)
In green spaces of Belarusian cities, Siberian spe-
cies of woody plants Caragana arborescens and Rham-
Fig. 2. Number of foliar pathogen species found on different plant species in urban green areas in Siberia and Belarus.
5
4
3
2
9
10
8
7
6
1
0
Acer campestre
Siberia Belarus Total
Acer platanoides
Acer tataricum
Alnus glutinosa
Alnus incana
Berberis vulgaris
Chamaecytisus austriacus
Chamaecytisus ruthenicus
Crataegus nigra
Euonymus europaeus
Lonicera caprifolium
Lonicera nigra
Quercus robur
Rosa glauca
Salix acutifolia
Syringa josikaea
Salix daphnoides
Syringa vulgaris
Viburnum lantana
Caragana arborescens
Rhamnus cathartica
Fig. 3. Diagram of foliar fungal pathogens discovered in urban green areas: (a) Belarus; (b) Siberia.
(a) (b)
3%
20%
20%
48%
9%
Powdery mildews
14%
24%
52%
10%
Rust Leaf spot, scab and similar diseases Saprotrophic fungal Leaf deformation

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CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 16 No. 2 2023
TOMOSHEVICH et al.
nus cathartica were attacked mainly by powdery mil-
dew fungi: Erysiphe palczewskii, Erysiphe robiniae,
Erysiphe friesii. In Siberia, they were also found to
have rust and leaf spots (Table 2).
In the 1960s and 1970s, the leaf pathogen Erysiphe
palczewskii was endemic to the Far East (Koval’ and
Nelen, 1970; Nelen, 1963, 1972). Extensive use of the
Siberian species Caragana arborescens as an ornamen-
tal plant in the landscaping of cities in the Far East
allowed Е. palczewskii to displace Trichocladia cara-
gana. At the beginning of the 1980s, the occurrence of
the fungus in the European part of the former USSR
and the epiphytotic character of the disease develop-
ment were reported (Gelyuta, 1981; Gelyuta and Gor-
Fig. 4. Pathogen Pleiochaeta setosa: (a) fungal spore; (b) disease symptoms on leaves Chamaecytisus ruthenicus.
(а) (b)
Fig. 5. Symptoms of leaf spot infection (Passalora rosae) on plant-hosts: (a) Rosa spinosissima; (b) Rosa majalis; (c) Rosa glauca;
(d) fungal spore.
(а) (b)
(c) (d)

CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 16 No. 2 2023
COMPARATIVE ANALYSIS OF FOLIAR DISEASES 225
lenko, 1984). Recently, many researchers have been
observing this fungus further advancing from the East
to the West (Huhtinen et al., 2001; Vajna, 2006;
Lebeda et al., 2008; Mieslerová et al., 2020). Most
likely, Erysiphe palczewskii entered Belar usian cities
together with the Siberian plant Caragana arborescens.
Leaf Pathogens of Non-native Plants
with no Close Relatives in the Local Flora
Some pathogens have been found to affect both
native and closely related European woody plants in
Siberia. For example, Coryneum foliicola is widely
found in Siberia on a native plant Crategus sanguinea
Pall. and has been found on Crataegus nigra (Euro-
pean woody plant). Similarly, Passalora rosae actively
attacks native species Rosa acicularis Lindl., R. majalis
Herrn, R. spinosissima L. and has been found on Euro-
pean species Rosa glauca (Fig. 5). These pathogens
have a vast distribution area but were not registered on
native European woody plants in Belarusian cities.
Meanwhile, some species of leaf pathogens (Sawa-
daea tulasnei, Erysiphe alphitoides, Cladosporium syrin-
gae, Erysiphe syringae) were possibly brought to Sibe-
ria with their plant hosts (Acer tataricum, Quercus
robur, Syringa vulgaris (Fig. 6)), since there are no
closely related species in this Region.
Also, non-native European plants Acer campestre,
A. platanoides, Euonymus europaeus, Alnus glutinosa,
A. incana have no closely related representatives in
Siberia, but they have not brought pathogens from the
European region. The fungus Mycopappus alni was
registered on Alnus glutinosa and A. incana plants in
Novosibirsk, while it remains to be determined how it
appeared in Siberia. M. alni was first found in Canada
and the United States on Alnus rubra and A. sinuata in
the late 1980s (Redhead and White, 1985). Later,
M. alni was detected in the Far East on leaves of Alnus
hirsuta, as well as on hawthorn and chokeberry leaves
in Korea and Turkey (Braun et al., 2000; Lee et al.,
2013; Park et al., 2013). We detected this fungus for the
first time in Russia in 2005 in the arboretum of the
Siberian Branch of the Russian Academy of Sciences
Fig. 6. Symptoms of powdery mildew infection on plant-hosts: (a) Acer tataricum in Kemerovo; (b) Acer tataricum in Novosibirsk;
(c) chasmothecia Sawadaea tulasnei; symptoms of powdery mildew infection on plant-hosts: (d) Quercus robur in Novosibirsk;
(e) Quercus robur in Krasnoyarsk; (f) chasmothecia Erysiphe alphitoides; (g) symptoms of powdery mildew infection on Syringa
vulgaris in Barnaul; (h) chasmothecia Erysiphe syringae.
(а) (b) (c)
(d) (e)
(g) (h)
(f)

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CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 16 No. 2 2023
TOMOSHEVICH et al.
on Alnus glutinosa and A. incana (Tomoshevich, 2008).
The fungus is not found every year, but under favor-
able weather conditions, it causes serious damage (leaf
damage up to 80–100%), resulting in curling and fall-
ing of leaves on lower branches by mid-August. Ear-
lier, we noted that the fungus Mycopappus alni was
likely to appear in Europe (Tomoshevich et al., 2013).
Pathogen Impact on Woody Plants
in Siberia and Belarus
It should be noted that in green areas of Belarus,
pathogens, excluding Ascochyta syringae and Clado-
sporium macrocarpum, are found every year and at all
locations (Flora of Belarus, 2015). However, in Sibe-
ria, only seven pathogens (Erysiphe adunca, Erysiphe
alphitoides, Erysiphe berberidis, Erysiphe palczewskii,
Erysiphe syringae, Sawadaea tulasnei, Septoria syrin-
gae) are found every year and at all locations where the
plants grow (values A and B, Table 3).
In Belarus (Europe), seven pathogens (Erysiphe
adunca, Erysiphe alphitoides, Erysiphe berberidis, Ery-
siphe palczewskii, Erysiphe syringae, Sawadaea tulas-
nei, Puccinia graminis) cause 26–50% or more dam-
age, whereas in Siberia, only three pathogens (Septoria
syringae, Sawadaea tulasnei, Erysiphe trifoliorum) are
more aggressive (values 3–4, Table 3). This fact proves
Table 3. Fungus–host plant associations found in Siberia and Belarus and pathogen impact
1 Relative levels of damage by pathogen (i.e. the percentage of damaged surface of leaf or other tissues): 1: 1–10%; 2: 11–25%; 3: 26–50%;
4: >50% of leaf/plant surface. Two numbers in the s ame row represent different situations in different cities. Frequency of attack:
A: found irregularly, i.e. not every year or not at every location where the plant occurs; B: found every year and at all locations where the
plant occurs.
Pathogen species Plant species
Period of pathogen
development Plant tissues infeсted Damage/frequency1
Belarus Siberia Belarus Siberia Belarus Siberia
Alternaria alternata Berberis vulgaris Jul–Aug Jul–Aug Leaves, shoots Leaves 2/B 2/А
Quercus robur Jul–Sept Jul–Sept Leaves, young
shoots
Leaves 1-2/B 2/А
Ascochyta syringae Syringa vulgaris Jul–Sept Aug–Sept Leaves Leaves 2/А 1/A
Cladosporium herba-
rum
Berberis vulgaris Jul–Aug Jul–Aug Leaves, shoots Leaves 1/B 1/А
Syringa vulgaris Jul–Sept Jul–Sept Leaves, young
shoots
Leaves 1/B 1/А
Cladosporium mac-
rocarpum
Quercus robur Jul–Sept Aug–Sept Leaves, young
shoots
Leaves 1/А 1/A
Erysiphe adunca Salix acutifolia Jun–Sept Aug –Sept Leaves Leaves 2-3/B 2-3/B
Salix daphnoides Jun–Sept Aug –Sept Leaves Leaves 2/B 2/B
Erysiphe alphitoides Quercus robur Jun–Sept Jun–Sept Leaves Leaves,
young shoots
4/B 3-4/B
Erysiphe berberidis Berberis vulgaris Jun–Sept Jul–Sept Leaves Leaves,
young shoots
4/ B 4/B
Erysiphe palczewskii Caragana arbo-
rescens
Jun–Sept Jun–Sept Leaves Leaves,
young shoots
3/B 4/B
Erysiphe syringae Syringa josikaea. Jul–Aug Jul–Sept Leaves Leaves 4/B 2/А
Syringa vulgaris Jul–Aug Jul–Sept Leaves Leaves 3-4/B 3-4/B
Erysiphe trifoliorum Chamaecytisus
austriacus
Jun–Sept Aug–Sept Leaves Leaves 2/B 2/А
Chamaecytisus
ruthenicus
Jun–Sept Aug–Sept Leaves Leaves 2/B 3/А
Puccinia graminis Berberis vulgaris Jun–Aug May–Jun Leaves Leaves 2-3/B 2/А
Sawadaea tulasnei Acer tataricum Jun–Oct Jul–Sept Leaves Leaves,
young shoots
3/B 3-4/B
Septoria syringae Syringa vulgaris Jul–Sept Jun–Aug Leaves Leaves 1-2/B 3-4/B
Sphaerulina ber-
beridis
Berberis vulgaris Jul–Sept Jul–Sept Leaves Leaves 2/ B 1/A

CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 16 No. 2 2023
COMPARATIVE ANALYSIS OF FOLIAR DISEASES 227
native species to be affected to a greater extent in the
region of origin.
Leaf pathogens Alternaria alternata, Cladosporium
herbarum, Erysiphe alphitoides, Erysiphe palczewskii,
Sphaerulina berberidis were found to develop during in
the same months in Siberia and Belarus (Table 3).
However, most fungi occur in green areas of Siberia a
month later or have a longer period of development
than in the Belarusian cities. The exception is Puccinia
graminis recorded in Siberia in May–June. The later
occurrence of leaf pathogens in Siberia is related to the
delayed phenophases of European woody plants. For
example, in the European part of Russia, the first oak
shoots open in mid-April (Shimanyuk, 1964). In Sibe-
ria, the opening of buds and the growth of Quercus
robur shoots were recorded more than a month later
(late May-early June) (Vstovskaya and Koropachins-
kiy, 2005).
CONCLUSIONS
The research has shown that using native and non-
native woody plants in parks and gardens enables cre-
ating more sustainable green spaces. However, contin-
uous monitoring of European woody plants in Siberia
and Siberian plants in Belarus should be carried out
since the transmission of local pathogens to intro-
duced plants and increased aggressiveness of patho-
gens that were brought to the region by their host
plants are observed. It is particularly the case for pow-
dery mildew fungi since these biotrophic pathogens
can persist in twigs and seeds, such as oak acorns.
When adapting to environmental conditions, the
non-native woody plants change their development
rhythm and decrease the resistance, affecting the
degree of pathogenic fungi development. For exam-
ple, in the sharply continental conditions of Siberia,
the delayed appearance of disease symptoms is
observed due to the shift in the phenophases of plants,
but the aggressiveness of pathogens increases com-
pared to the regions of Belarus.
The new findings on the development of Mycopap-
pus alni and Pleiochaeta setosa for Siberia suggest that
they are likely to appear on woody plants in Europe
and have a possible invasive status.
The first findings of pathogen analysis on non-
native and native plants in Siberia and Belarus
(Europe) show that using non-native plants in urban
plantations can cause new associations between plants
and pathogens and even more severe plant lesions.
Future molecular studies are needed to understand the
distribution of the fungus more accurately, especially
in urban areas. In controversial cases, pathogen iden-
tification and replenishment of GenBank with parallel
analyses of samples of Siberian and European fungus
samples will be required.
FUNDING
This research was funded by the National Academy of
Sciences of Belarus, State program of scientific research
“Nature management and ecology” Projects no. 20190899,
20190898 and was funded by the Ministry of Science and
Higher Education of the Russian Federation program of
scientific research “Theoretical and applied aspects of
studying gene pools of natural plant populations and con-
servation of plant diversity “outside the typical environ-
ment” (ex situ)” (АААА-А21-121011290027-6). In prepar-
ing the publication, materials of the bioresource scientific
collection of the CSBG SB RAS “Collections of living
plants indoors and outdoors” USU_440534 (Novosibirsk,
Russia) were used.
CONFLICTS OF INTEREST
The authors declare no conflict of interest.
OPEN ACCESS
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