Pathogenic Mycobiota on Trees in Novosibirsk Plantations. Tomoshevich, M. A.

Abstract

Pathogenic Mycobiota on Trees in Novosibirsk Plantations

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Pathogenic Mycobiota on Trees in Novosibirsk Plantations
M. A. Tomoshevich
Central Siberian Botanical Garden, Siberian Branch of the Russian Academy of Sciences,
ul. Zolotodolinskaya 101, Novosibirsk, 630090 Russia
E-mail: tomoshevich@csbg.nsc.ru
Abstract—In 2003–2008 the author inventoried fungal infections of trees in various landscaped areas of
Novosibirsk. As a result, 77 fungal species has been distinguished and their seasonal development has been
revealed. Dominant pathogenic genera and species have been determined. The intensity of fungal growth on
urban trees and shrubs depends on the time the disease appears, the aggressiveness of the causative agent, and
specific microclimate of the landscaped area.
DOI: 10.1134/S1995425509040122
Key words: causative agents, pathogenic micromycetes, trees, urbanized environment, seasonal succession,
infection-resistant plants
Ecological factors and specific anthropogenic im-
pacts that depress plants in urbanized environment are
quite specific. Of the biotic factors, pathogens, in par-
ticular fungi, have the most adverse effect on urban
plantations. They inhibit photosynthesis in trees; as a
result, leaves turn yellow and fall, productivity and lon-
gevity decrease, plant appearance deteriorates, and
some plants die.
Inventorying pathogens in a specific environment is
of top priority, as this suggests well-grounded practical
protective measures. Results of such studies are useful
for landscape architects, foresters, and specialists in-
volved in plant introduction and establishment.
In Novosibirsk, tree diseases were studied by Noz-
drenko [1–3]. In addition to diseases of trees, the works
deal with those of flowering plants. The author isolated
pathogens of the genera Phoma,Cytospora,Gloeo-
sporium,Tubercularia,Macrosporium,Cladosporium,
and Fusarium that cause dying of shoots and branches.
Although fungal biota of Novosibirsk has been stud-
ied since the 1960s, we still lack data on fungal patho-
gens that parasitize trees in urban landscapes. The
diversity of pathogens that cause leaf diseases has re-
cently been noted to increase. The work therefore is
aimed at studying phytopathogenic biota that affects
Novosibirsk trees and shrubs. The tasks were as fol-
lows: (1) to reveal fungal species composition and the
most harmful causative agents; (2) to determine the de-
velopment period and disease symptoms; (3) to reveal
plants resistant to mycromycete pathogens.
MATERIALS AND METHODS
The study involved field and laboratory examina-
tion of plants, detection of symptoms, observation of
disease dynamics, collection of infected specimens, re-
cording of infection-resistant plants, and isolation and
identification of pathogens. The study was conducted
during the vegetative seasons of 2003–2008, every ten
days from May through October. Nine hundred infected
specimens were collected. Fungal species were deter-
mined using the identification guides [4–14].
Nomenclature is given after Index Fungorum
(http://www.speciesfungorum.org/Names/Names.asp),
CABI databases. At present, imperfect fungi (Deutero-
mycota) are placed in the order Ascomycota.
The work reports results of phytopathological stud-
ies conducted in 8 miniparks, 9 parks, 6 boulevards and
on trees and shrubs planted along the main roads, in-
cluding those in residential areas of Kalininskii, Dzer-
zhinskii, Zael’tsovskii, Leninskii, Kirovskii, Tsentral’-
nyi, and Sovetskii districts, and the towns of Krasno-
obsk and Pashino.
RESULTS AND DISCUSSION
Examination of urban trees and shrubs revealed a
variety of causative agents. The most diverse group of
pathogens was that of fungi, followed by viral and non-
parasitic ones. A total of 77 micromycetes that affect
mainly plant leaves were discovered.
The most fungi-ridden were plants of the genera
Rosa and Populus, each genus parasitized by 10 fungal
species, Berberis by 9, Caragana by 8, Tilia and Cra-
taegus by 7 each, and Betula by 6 species; plants of
other genera were infected by 4 species or less.
Some trees were infected by two or more species of
fungi, for example, Erysiphe adunca (Wallr.) Fr., Alter-
naria alternata (Fr.) Keissl., Cladosporium herbarium
(Pers.) Link., Fusicladium martianoffianum Th.,
Gloeosporium populi-nigrae (Allesh.) Karak., and
Mycosphaerella populi (Auersw.) J. Schröt were found
on leaves of Populus nigra L.
ISSN 1995-4255, Contemporary Problems of Ecology, 2009, Vol. 2, No. 4, pp. . © Pleiades Publishing, Ltd., 2009.
Original Russian Text © M.A. Tomoshevich, 2009, published in Sibirskii Ekologicheskii Zhurnal, 2009, Vol. 16, No. 4, pp. 615–621.
1

In the species composition of pathogenic micromy-
cetes, the phylum Basidiomycota is represented by 10
species (13.6% of the total number of species) of the or-
ders Uredinales and Polyporales. The most abundantly
represented are the genera Phragmidium (3 species)
and Melamspora (2 species) (Table 1).
Autoecious fungi begin to grow in May and persist
throughout the vegetative season. Heteroecious rust
fungi are mainly represented by species that pass
through the uredo- and theliostage, with the exception
of Puccinia graminis. First uredopustules appear in
July and August (Table 1). Rust fungi grow more ac-
tively in wet habitats, such as river floodplains and
riversides.
Many Rosa species are highly susceptible to infec-
tion of Phragmidium fusiforme and P. tuberculatum.
The ecidial stage of Phragmidium fusiforme is capable
of infecting all above-ground parts of the plants. The
mass appearance of uredo- and theliopustules shortens
the vegetation period because leaves wither and growth
decreases.
Most species identified are of the order Ascomy-
cota: 67 species, or 86.6% of the total number of species
isolated.
The phylum Erysiphales includes 17 pathogen spe-
cies (Table 2). The genus Erysiphe includes 10 species,
Podosphaera,3,Phyllactinia, 2, and Microsphaera and
Sawadaea, 1 species each.
Powdery mildew fungi are ranked among the most
harmful pathogens that affect plants over a long period.
Some pathogens affect plants as early as middle June
and persist till late vegetation period (Table 2). Most
mildew fungi begin to grow in middle July. In 2007,
first mildew symptoms occurred as early as late May.
That year, conditions were particularly favorable for
powdery mildew growth, such as early spring, rainless
period, followed by high humidity and air temperature
of 18–20°C in middle May.
In the city, conidia develop on young shoots and
leaves of Rosa canina,Acer negundo,Spireae, and
Crataegus. On these species the pathogen often skips
ascigerous stage.
The entire spectrum of the order Ascomycota is
dominated by pathogens that cause spots (74%).
Sixty-one percent of them have pycnidia and stromatic
conidia (Table 3).
Pycnidial micromycetes in the urban plantations are
represented by 16 species, with the most common
Phyllosticta (6 species) and Ascochyta (4 species).
Fungi of the order Phyllosticta have been noted to
grow most intensively when conditions are favorable
for parasite’s invasion and growth, i.e. when host plants
are weakened abiotically or damaged by entomo-
phages.
Stromatic-conidial fungi constitute a large part of
the isolated pathogens, with the genera Gloeosporium
(3 species), Cylindrosporium (2 species), and Cory-
neum (2 species) represented most abundantly. These
fungi have mucous conidia dispersed by water or ani-
mals, primarily by insects, to which they may adhere.
“Semiopen” conidia ensure rapid dispersal of these
pathogens when they appear late (in middle August).
The disease develops rapidly: first symptoms of Phaci-
dium betulinum Mouton appear on birch leaves in mid-
dle August, and in early September the invasion may be
as high as 60–70%.
In Novosibirsk there has been a recent increase in
spreading of plant diseases caused by fungi of the or-
ders Cercospora,Leptoxyphium,Cladosporium, and
Fusicladium. The pathogens begin to develop in late
June and persist throughout the vegetation period, July
being the most favorable for growth. Since the conidia
are open, the fungi are highly sensitive to environmen-
CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 2 No. 4 2009
2 TOMOSHEVICH
Table 1. Mycromycetes Basidiomycota and their host plants
Nos. Micromycete: genus and species Host plant: genus and species Development
period
1Melampsoridium betulinum (Pers.)
Kleb.
Betula pubescens Ehrh., B. microphylla
Bunge
Jul–Oct
2Melampsora epitea Th&&
um. Salix sp., Salix capria L. Jul–Sep
3M. laricis-populinà Kleb. Populus balsamifera L., P. suaveolens
Fisch.
Jul–Oct
4Cronartium ribicola J. C. Fisch. Ribes aureum Pursh Jul–Oct
5Phragmidium fusiforme J. Schröt. Rosa sp., R. acicularis L. May–Sep
6P. rosae-rugosae Kasai. Rosa sp. May–Sep
7P. tuberculatum J. M&&
ull. Rosa sp., R. davurica L., R. acicularis May–Sep
8Puccinia graminis Pers. Berberis vulgaris L. May–Jun
9Uromyces cytisi J. Schr&&
ot. Caraganà arborescens Lam. Jul–Oct
10 Chondrostereum purpureum (Pers.)
Pouzar
Malus baccata (L.) Borkh. May–Sep

tal factors: the development of the pathogens slows
down in too hot and dry weather. On the other hand,
open conidia damage plant significantly when weather
conditions are favorable for pathogen growth.
A rather harmful form of Micromycete Leptoxy-
phium fumago (Woron.) R. C. Srivast. develops annu-
ally on leaves and shoots of many trees and shrubs, e.g.
Rosa canina,Spiraea,Berberis vulgaris,Tilia par-
vifolia,Quercus robur, and others. As early as July
(sometimes in June) when plants are well into vegeta-
tion, a soot-like deposits cover plant leaves. This not
only affects the plant appearance, but also reduces as-
similation area and, consequently, weakens the plant.
Cercospora rosicola affects riverside Rosa canina
plantations; the pathogen deteriorates the appearance of
the shrubs with numerous small brown-purple spots
that drop out in a while.
Many of isolated fungi are dangerous causative
agents.
Phyllactinia guttata and Phacidium betulinum de-
velop to a dangerous degree on leaves of the European
white birch.
Powdery mildew (Erysiphe adunca), rust (Melam-
psora larici-populina), and spots caused by the
micromycetes Gloeosporium populi-nigrae and Myco-
sphaerella populi were found on Populus nigra.
Whether a single or complex fungal infection, they
cause trees to shed leaves in late August or early Sep-
tember.
The powdery mildew caused by Erysiphe
alphitoide, an annual disease of young leaves and an-
nual shoots, was found on Quercus robur.
Erysiphe palczewskii,Uromyces cytisi, and Asco-
chyta borjomi develop abundantly on leaves of Cara-
gana arborescens. On many plants powdery mildew on
leaf upsides co-occurs with rust on leaf undersides.
Less widespread diseases include the powdery mil-
dew caused by Erysiphe trifolii on Cytisus, spots
caused by Cladosporium syringae on Syringa and Spi-
raea (Phyllosticta spiraenta f. spiraenia-bumaldae).
There were solitary occurrences of rust on leaves of
Rosa canina (caused by Phragmidium rosae-rugosae
Kasai) and Berberis vulgaris (Puccinia graminis);
CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 2 No. 4 2009
PATHOGENIC MYCOBIOTA ON TREES IN NOVOSIBIRSK PLANTATIONS 3
Table 2. Mycromycetes Erysiphales and their host plants
Nos. Micromycete: genus and species Host plant: genus and species Development
period
1Erysiphe alphitoides (Griffon &
Maubl.) U. Braun & S. Takam.
Quercus robur L. Jul–Sep
2Er. adunca (Wallr.) Fr. Salix sp., S. capria L., S. viminàlis L.,
S. cinerea L., S. pentandra L., Populus
nigra L., P. balsamifera L.
Jul–Sep
3Er. clandestinà Biv. Crataegus sp., C. sanguinea Pall. Jun–Sep
4Er. lonicerae DC. Lonicera tatarica L., L. xylosteum L. Jul–Sep
5Er. ornàta (U. Braun) U. Braun et
S. Takamatsu
Betula pubescens Aug–Sep
6Er. palczewskii (Jacz.) U. Braun et
S. Takamatsu
Caraganà arborescens Jun–Sep
7Er. syringae Schwein. Syringae vulgaris L., S. josikaea Jacq. Jul–Sep
8Er. trifolii Grev. Chamaecytisus ruthenicus (Fisch.
ex Woloszcz.) Klaskova
Aug–Sep
9Er. viburni Duby Viburnum opulus L. Aug–Sep
10 Er. vanbruntianà (W. R. Gerard)
U. Braun et S. Takamatsu
Sambucus rasemosa L. Jun–Sep
11 Microsphaera berberidis (DC.) Lev. Berberis vulgaris L. Jul–Sep
12 Phyllactinia guttata (Wallr.: Fr.) Lev. Betula pendula Roth., B. pubescens
Ehrh.
Aug–Oct
13 Ph. mali (Duby.) U. Braun Malus baccata (L.) Borkh. Aug–Sep
14 Podosphaera tridactyla (Wallr.) de
Bary
Padus avium Mill. Jul–Sep
15 P. clandestine (Wallr.) Lev. var.
clandestine
Spiraea media Franz Schmidt Jun–Sep
16 P. pannosa (Wallr.: Fr.) de Bary Rosa rugosa Thunb., R. acicularis
Lindl.
Jul–Sep
17 Sawadaea tulasnei (Fuckel) Homma Acer negundo L., A. ginnàla Maxim. Jul–Sep

CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 2 No. 4 2009
4 TOMOSHEVICH
Table 3. Spot-forming pathogens and their host plants
Nos. Micromycete: genus and species Host plant: genus and species Development
period
1Alternària alternàta (Fr.) Keissl. Berberis vulgaris,Caraganà
arborescens,Populus alba L., Quercus
robur,Tilia cordata Mill.
Jul–Sep
2Apiognomonia errabunda (Roberge ex
Desm.) H&&
ohn.
Tilia cordata Aug–Sep
3Ascochyta berberidianà Sacc. Berberis vulgaris Aug–Sep
4As. borjomi Bondartsev Caraganà arborescens Jul–Sep
5As. caraganàe (Vestergr.) Melnik Chamaecytisus ruthenicus Aug–Sep
6As. crataegi Fuckel Crataegus sanguinea,Crataegus sp. Jun–Sep
7Asteromella mali (Briard) Boerema Malus baccata Jul–Sep
8Blumeriella jaapii (Rehm) Arx Prunus virginianà L. Aug–Sep
9Cercospora opuli H&&
ohn. Viburnum opulus Jul–Sep
10 C. rosicola Pass. Rosa majalis Herrm. Jun–Sep
11 Cladosporium herbarum (Pers.) Link. Amelanchier spicata (Lam.) C. Koch.,
Berberis vulgaris,Caraganà
arborescens,Populus alba,
P. balsamifera,Rosa majalis,Rosa sp.,
Tilia cordata,Syringae vulgaris
Jul–Sep
12 Cl. humile Davis Acer ginnàla Sep
13 Cl. macrocarpum Preuss. Quercus robur Aug–Sep
14 Cl. syringae (Oudem.) Montem. Syringae vulgaris Aug–Sep
15 Cl. variabile (Cooke) G. A. de Vries Rosa sp. Aug–Sep
16 Coryneum foliicola Fusk. Crataegus sanguinea Jul–Sep
17 C. sorbi Peck Sorbus aucuparia L. Jul–Sep
18 Cylindrosporium betulae Davis. Betula pendula Sep
19 C. salicinum (Peck) Dearn. Salix alba L. Aug–Sep
20 Diplocarpon rosae F. A. Wolf Rosa majalis Aug–Sep
21 Fusicladium martianoffianum (Th&&
um.)
K. Schub. et U. Braun
Populus balsamifera Aug–Sep
22 F. orbiculatum (Desm.) Th&&
um. Sorbus aucuparia Aug–Sep
23 Entomosporium thumenii (Cooke) Sacc. Crataegus chlorosarca Maxim. Aug–Sep
24 Gloeosporium crataeginum Sacc. Crataegus chlorosarca Aug–Sep
25 Gl. populi-nigrae Gonz. Frag. Populus balsamifera,P. alba Aug–Sep
26 Gl. tremulae (Lib.) Pass. Populus tremula L. Jul–Sep
27 Leptoxyphium fumago (Woron.)
R. C. Srivast.
Amelanchier spicata,Betula pendula,
Berberis vulgaris,Caraganà
arborescens,Chamaecytisus ruthenicus,
Crataegus chlorosarca,Populus tremula,
Rosa majalis,Rosa sp., Spiraea
salisifolia L., Tilia cordata,Quercus
robur
Jun–Sep
28 Marssonina betulae (Lib.) Magnus Betula pendula Sep
29 Monostichella salicis (Westend.) Arx Salix fragilis L. Aug–Sep
30 Mycosphaerella cerasella Aderh. Amygdalus nànà L. Jun–Sep
31 M. microsora Syd. Tilia cordata Jun–Sep
32 M. populi (Auersw.) J. Schrt. Populus alba, P. balsamifera Jul–Sep
33 Oidium spp. Acer ginnàla Maxim., Caraganà
arborescens, Rosa majalis, Rosa sp.
Jun–Oct

spots on leaves of Rosa canina (caused by Clado-
sporium variabile), Amygdalus (Mycosphaerella cera-
sella), Viburnum lantana (Cercospora opuli), Rosa
canina (Diplocarpon rosae), Berberis vulgaris (Asco-
phyta berberidina), and Sambucus (Phoma exigua).
The study shows that the following plants used in
urban landscapes are the most resistant to the isolated
pathogens: Viburnum lantana,Frascinus pennsylva-
nica,Padus maackii,Euonymus europaeus,Juglans
mandshurica,Elaeagnus argentia,Elaeagnus angusti-
folia,Sorbaria sorbifolia,Rhododendron dahuricum,
Dasiphora fruticosa,Forsythia, and Philadelphus.
The results show that pathogen species composition
depends on plant species diversity of urban plantations
and plant condition. Not all diseases occur in a danger-
ous form and their distribution does not indicate the
scale of damage they cause. Most likely, the scale of
damage depends on the time of disease onset, aggres-
siveness of the causative agent, and specific microcli-
mate in which a tree or shrub exists.
Different pathogenic mycobiota forms in different
urban landscapes. As a result, trees and shrubs in
streets, miniparks, and parks even in the same district
are affected by entirely different pathogen species, with
intensity of pathogen development varying still more
remarkably. Therefore, further monitoring of phyto-
pathogens is required to reveal disease dynamics and
suggest appropriate protective measures.
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PATHOGENIC MYCOBIOTA ON TREES IN NOVOSIBIRSK PLANTATIONS 5
Table 3. (Contd.)
Nos. Micromycete: genus and species Host plant: genus and species Development
period
34 Pollaccia radiosa (Lib.) E. Bald. & Cif. Populus alba Aug–Sep
35 Phacidium betulinum Mouton Betula pendula Aug–Sep
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38 Phyllosticta aucupariae Th&&
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