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Asian Jr. of Microbiol. Biotech. Env. Sc. Vol. 18, No. (2) : 2016 : 359-366
© Global Science Publications
ISSN-0972-3005
Address : Dr. Ilya Digel, Laboratory of Cell- and Microbiology, FB9 FH Aachen University of Applied Sciences, 52428,
Jülich, Germany
SPECIES COMPOSITION AND INJURIOUSNESS OF STRANGER
XYLOPHILOUS FAUNA AFFECTING INDIGENOUS URBAN
DENDROFLORA OF CENTRAL ASIA
M. TURALIYEVA1, A. YESHIBAEV1, A. SAPARBEKOVA1, L. AKYNOVA1, R. ABILDAYEVA1, M.
SADENOVA1, K. SARTAYEVA1, A. SCHIEFFER2 AND I. DIGEL2
1 Department of Biotechnology, South Kazakhstan State University named after
M. Auezov, Shymkent, Kazakhstan
2´FH Aachen University of Applied Sciences, Institute of Bioengineering,
Laboratory of Cell- and Microbiology, Jülich, Germany
(Received 20 September, 2015; accepted 10 January, 2016)
Key words : Neobionta, Adventive species, Xylophilous fauna, Invasion, Central Asia, Invasion
Abstract – At the present time, one of the most serious environmental problems of Central Asia and South
Kazakhstan is the ongoing large-scale deterioration of principal urban tree populations. Several major
centers of massive spread of invasive plant pests have been found in urban dendroflora of this region. The
degree of damage of seven most wide-spread aboriginal tree species was found to range from 21.4±1.1 to
85.4±1.8%. In particular, the integrity of the native communities of sycamore (Platanus spp.), willow (Salix
spp.), poplar (Populus spp.) and elm (Ulmus spp.) is highly endangered. Our taxonomic analysis of the most
dangerous tree pests of the region has revealed them as neobiontic xylophilous insects such as Cossus cossus
L. (Order: Lepidoptera L.) Monochamus urussovi Fisch., Monochamus sutor L., Acanthocinus aedelis L. and Ñetonia
aureate L. (Order: Coleoptera L.). We relate the origin of this threatening trend with the import of industrial
wood in the mid 90’s of the last century that was associated with high degree of the constructional work in
the region. Because of the absence of efficient natural predators of the pest species, the application of
microbiological methods of the pest control and limitation is suggested.
INTRODUCTION
Nowadays, the uncontrolled spread and rapid
reproduction of non-native (also known as neozoa,
alien, foreign, stranger and adventitious) organisms
is of global ecological importance (Aukema et al.,
2011). Invading alien insects cause huge ecological
and economic damage over vast regions covering
thousands of hectares (Maslyakov, 1999; Liebholdi et
al., 2012). Their vital activities and rapid
reproduction sharply suppress the productivity of
the whole ecosystem and often result in a dramatic
alteration of natural process of the regional floro-
and faunogenesis (Fomina, 2012). Even single
massive outbreaks can lead to vanishing of rare,
disappearing and relic species of trees. According to
the estimation of experts, the damage resulting from
the alien pests globally makes up billions of dollars
annually (Aukema et al., 2011). The magnitude of
economic problems caused by neobiontic species
often requires a coordination of efforts of the
international community (Tishkov, 2012).
Due to the globalization of economic relations,
the problem of global adventitious species invasion
becomes topical and urgent for Central Asia as well.
Over the last 30 years, repeated outbreaks of
massive reproduction of different non-native insects
such as Pineus pini and Oligonychus piceae Reck were
observed after the introduction of new trees like
Pinus sylvestris L., Larix sibirica Ledeb. and Ulmus
pumila L. in different regions of Central Asia and
Kazakhstan (Gnienko et al., 1999).
In some cases, irreversible destruction of the
whole wood communities has been observed. For
example, in the cities Almaty and in Taldykorgan
the abundance of insect pests virtually completely
prohibited the growth of shoots and young trees. In
the natural forest stands of U. pumila L., the area of
360 TURALIYEVA ET AL.
mass reproduction of Exàereta ulmi Schiffermüller
reportedly reached 3.0-3.5 thousand hectares
(Bogacheva, 2004). Another threatening outbreak of
several alien species of genus Rhynchaenus (syn.
Orchestes) has been observed in artificial forest
stands of U. pumila in the Central, Southern and
Northern Kazakhstan. The area of massive
reproduction of pests since 2004 has exceeded 10
thousand hectares (Nurtazaev and Aleuova, 2010).
Larvae of Rhynchaenus have done irreversible
damages on U. pumila in a large number of locations
so that most of the existing windbreak fields were
lost completely.
Urban dendroflora of Central Asia and South
Kazakhstan represents the exclusive community
including local and introduced species from
different physiographic regions of the world. The
present species composition of dendroflora of the
region counts about 250 species of trees; suffruticous
(having wood in the lower part of the stem, with
yearly branches, herbaceous) and fruticous (having
the form of a shrub) plant life forms (Sikhymbaeva,
2006). From this species variety 40.2 % is accounted
for native and 58.8 % for introduced species, some of
them such as Fraxinus angustifolia Vahl., Fraxinus
americana Bunge., Fraxinus excelsior L. and Acer
negundo L. were established in native tree
communities decades ago (Sikhymbaev et al., 2005).
Here we report about an ongoing spreading of
xylophilous insect pests in the urban dendroflora of
the Central Asian region. Our previous pilot study
has shown that five to six principal native tree
species are highly endangered. The main purposes
of this study were (1) evaluation of harmfulness, (2)
investigation of host (feeding tree) preferences and
(3) analysis of species composition of the
adventitious xylophilous fauna in the affected tree
communities. We also briefly addressed the issues of
the peculiarities of the tree’s damage as well as
counteraction measures that could be undertaken.
MATERIALS AND METHODS
Here we report the data on alien xylophilous pest
invasion collected over the period 2009-2012 in the
tree communities in seven cities and settlements
(Shymkent, Aksukent, Arys, Tamerlanovka, Turar
Ryskulov, Shayan and Chulak-Kurgan) of the
Central Asian region. At least 500 trees were
examined in each settlement. The objects of the
research were the dominant native species of
Central Asian dendroflora comprising Ulmus pumila
L., Salix. alba L., Populus. alba L., P.nigra L.,
U.macrocarpa Hance., P. orientalis L., S. babilonica L..
Each of these species contributes with 8% to 17%
into the trees populations of most settlements of this
region and thus together they buildup the principal
basis of the whole Central Asian dendroflora. The
species composition was determined using the
illustrated identification guide of Kazakhstan’s and
Central Asian flora (1969).
Collection and counting of xylophagous insects
was carried out using the standard techniques
introduced by Dunaeva (1997); Alekseyeva and Lure
(1970). In brief, the insects were partly manually
gathered from an occupied substratum, and partly
collected by fenestrated traps. In total, more than
1700 imagoes and about 3500 larvae were collected
and subjected to taxonomical analysis according
toof Dedyukhin (2005) and Mamaeva et al., (1976);
Mamaeva and Denilevsky, 1975). In parallel, the
correlation between the pest species and feeding
tree species has been analyzed in order to discover
the pest’s host preferences.
The peculiarities of xylophage distribution
throughout the stem and brunches of the affected
trees were examined on greenwood chumps (length
of 50 cm). The counting was mainly carried out in
March and April, when young imago exit from
cocoons and larvae awake from winter catalepsy.
The greenwood pieces were examined at four levels
of a tree stem: (1) three sections at the very basis of
tree stem, where the main stem is not branched out
(diameters varied from 45 to 70 cm); (2) nine
sections on the stems of the first order (at the height
of 2.0-2.5 m., 25-40 cm in diameter); (3) eighteen
sections of the second order stems (at the height of
4.0-4.5 m., 15-25 cm in); (4) thirty six brunches of the
3rd order.
Statistical processing of the results was carried
out by calculating the mean value and standard
deviation for the 95% confidence interval. All size-
and number measurements were carried out in
fourfold replication. The data were recorded and
processed using Microsoft® Excel2010 package.
RESULTS AND DISCUSSION
Analysis of the overall level of the urban
dendroflora damage in the Central Asian region
The overall harmfulness of adventitious
xylophilous fauna has been measured on the basis of
the current level of dendroflora damage by pests.
Our counts have shown that in average 74.8±4.56 %
Species Composition and Injuriousness of Stranger Xylophilous Fauna Affecting Indigenous 361
of the trees in the investigated region died and
partially died. Onwards, all of them have traces of
stem damage by pests. Showing variations, the
greatest quantity of the damaged trees has been
found in cities Shymkent and Arys, as well as in
settlements Shaian and T. Ryskulov (Fig. 1).
The analysis of the overall species composition of
the investigated forest stands has shown that seven
native dominating species were damaged to the
greatest degree: P. orientalis, S. alba, P. alba, S.
babilonica, U. macrocarpa, P. nigra and U. pumila. The
average value of these species’ damage ranged from
21.4±1.1 to 85.4±1.8 % (Fig. 2).
U. pumila and P. orientalis have revealed
themselves as the most and the least affected
species, correspondingly. This may be related with
the anatomical, biochemical and physiological
peculiarities of the trees as well as with a different
abundance of species. Indeed, as the insert graph
(Fig.2) indicates, there is an obvious correlation
between the occurrence of the species and the
percentage of their damaged representatives.
In all investigated communities the visual
symptoms of the tree damage were almost identical,
with destructions ranging from the flat-headed
growth to the death of the whole tree,
corresponding to the number and vital activities of
the pest in a tree stem. In the case of deletion of the
sieve tissue (phloem) all around the main stem, the
top part of the tree becomes isolated from the root
system and dies quickly. In the case of longitudinal
pest propagation, a single segment of the phloem is
affected and just a part of the tree dies. Such a type
of the stem damage often manifests itself as a flat-
headed growth (Fig. 3).
Tree damage and extinction is often accelerated
by rotting of damaged tree parts, caused by the
phytopathogenic and saprophytic microbial flora.
Tree sap, excrements of larvae and living tissues of
tree serve as a nutrient medium enabling fast
proliferation of phytopathogenic and saprophytic
microorganisms, which in turn contribute to the
Fig. 1. Degree of trees community damage in cities and settlements of the Central Asian Region
Fig. 2. Comparative degree of the native trees species
damage. The insert graph shows the correlation
between the abundance of the tree species (all
investigated species accumulated) and the degree
of their damage by adventitious xylophages.
362 TURALIYEVA ET AL.
rapid destruction of the stem.
Peculiarities of pest distribution in the host trees
The investigation of xylophages distribution
throughout the various parts of a stem of the host
tree have shown that the most preferable part for the
pests is the main stem at a height of 150-250 cm
having a diameter above 17 cm. From the bottom to
the top of a tree there was always a distinct gradient
in the number of pest organisms (Fig. 4). The least
occupied sector of a stem of trees was always its top
part, i.e. the brunches of the 3rd and higher orders).
The next least populated sector was the group of the
2nd order, and so forth. Apparently, the orientation of
stem sides towards the cardinal directions and thus
the level of exposure to the light did not have a
significant impact on the pest’s population (by
means of their number).
Concerning the relationship between the overall
size of the tree and the level of its damage it was
found that a number of 95.4±5.3 % of stems of
damaged trees had a diameter of more than 17 cm.
Young trees having stems thinner than 16 cm
showed no symptoms of stem damages caused by
pests. This pattern was typical for all seven studied
tree species, which differed only by the absolute
quantity of larvae inside the stems. We suppose that
the distinct preference of thick stems might be
related to better protection against predators but the
role of nutritional factors cannot be excluded too.
In general, the affected trees with a stem diameter
from 40 to 70 cm had 19 up to 48 larvae per tree (l/
t). In particular, the greatest number of pest’s larvae
has been found in the stems of U. pumila (number of
studied trees n=1280) and U. macrocarpa (n=582):
43.8±4.6 and 34.3±2.5 (l/t), correspondingly. In S.
babilonica (n=345), S. alba (n=245), P. nigra (n=636)è P.
orientalis (n=147) the larvae numbers were 31.9±3.8;
27.9±2.4; 26.7±2.6 and 23.3±3.1 (l/t) respectively. The
least average larvae quantity was found in the stems
ab
Fig. 3. Appearance of partially and completely dead trees – (A-B) U. pumila group of
partially dead trees and a completely dead tree. (C-E): Pathological changes caused
by the pest species and microorganisms in the stem of Populus nigra L.
Species Composition and Injuriousness of Stranger Xylophilous Fauna Affecting Indigenous 363
of P. alba (n=265): 21.5±2.7 (l/t).
Analysis of pest species composition and their
correlations with preferred species of trees
Taxonomical analysis of the tree pests was carried
out on the basis morphological characteristics of
imago and larvae. It was found that 27 pest species
(xylophages and folivores (leaf-eating)) are
parasitizing on the seven dominating species of
Central Asia dendroflora. Twenty of them are
butterflies (Lepidoptera L.) and 7 are beetles
(Coleoptera L.). Lepidoptera are presented by 9 species
from Tortricidae Laterelle, 10 species of Notodontidae
and one species of Cossidae. The 19 species belonging
to Tortricidae and Notodontidae are representatives of
normal local entomofauna and live on the leaves of
trees, whereas Cossus cossus L. has been one of the
region’s dendroflora deleterious adventive
xylophages over last 4-5 years.
Table 1. Distribution and occurrence of xylophilic adventitious species throughout the tree species.
Pests Ulmus Ulmus Populus Populus Salix Salix Platanus
pumila macrocarpa nigra alba alba babilonica orientalis
Cossus cossus L. * ++++++-
Xanthogaleruca luteolà Muller†+------
Monochamus urussovi Fisch. ° ++-----
Monochamus sutor L. ° ++----+
Acanthocinus aedelis L. † +------
Ñetonia aureata L. * +++++++
* polyphages ° oligophages † monophages
Fig. 4. Regularity of pests’ larvae distribution throughout the tree stem. The vertical axis shows
the percentage of the larvae found in wood respectively to the number of all trees taken in
the study. The horizontal axis represents the location in the tree (the stem’s order; see
materials and methods).
364 TURALIYEVA ET AL.
Coleopterous pests are represented by seven
species belonging to three families:
1. Cerambycidae Laterelle:
a. Monochamus urussovi Fisch.;
b. Monochamus sutor L.;
c. Acanthocinus aedelis L.;
d. Lamia textor L.;
e. Oberea oculata L.;
2. Scarabaedae:
a. Ñetonia aureate L.;
3. Chrysomelidae L.
a. Xanthogaleruca luteolà Muller
For the period 2009-2012 we observed that the
xylophagous species C. cossus. M. urussovi, M. sutor,
A.aedelis and Ñ aureate increasingly became the
dominating pests of dendroflora in the investigated
Central Asia’s settlements. According to their host
preferences and the level of host specialization these
and the other encountered pests can be classified in
three trophic groups: polyphages, oligophages and
monophages (Table 1). It should be noted, however,
that me interpret this classification only regarding
the preferred tree species as a food source. If the
insects not only feed on substances the tree provides
but also feed on other organisms ‘associated’ to the
trees, the meaning of the ‘thropic group’ needs to be
defined more accurately in the future.
Ñ aureate and C. cossus use 6 and 7 species as
feeding hosts. M. sutor is found on P. orientalis, and
on two more species of elm trees. Monochamus
urussovidevelop only on U. pumila and U.
macrocarpa. Finally, Acanthocinus aedelis and
Xanthogaleruca luteolà are narrowly adapted to elm
trees U. pumila), but in Central Asia’s climatic
conditions normally do not result in the death of the
tree(s) (Sikhimbaev et al., 2005).
Analysis of specific distribution geography and
ecological features of the adventive xylophylous
fauna
Our further research of the invasive pest
distribution areas showed that the most occuring
species on the territory of South Kazakhstan area are
Ñ. aureate and C. cossus. Populations of these species
are high abundant in the forest stands of cities like
Shymkent, Lenger, settlements T. Ryskulov,
Tamerlan and Aksukent. The next high by number
are populations of M. urussovi, which is one of
dominating species of the xylophylous fauna of the
dendroflora of the city of Shymkent, settlements
Shaian and Sholak-Korgan. By contrast, the
populations of M. sutor and A. aedelis pests were
only found in the dendroflora of the city of
Shymkent. The population areal for M. sutor was
established only within the territory of the
Shymkent arboretum.
The observed high rate of reproduction and the
great harm caused by adventitious pests indicate
that climatic conditions of Central Asia are highly
suitable for their vital activities In the climatic
conditions of Central Asia the peak of summer
activity of pests’ young imagoes occurs (depending
on the weather conditions of the year) from the first
decade of April until the second decade of May. The
imagoes feed predominantly on tree sap running
from damaged parts of trees before they reach the
sexual maturity. From the end of May until the first
decade of June the females fly blow on the trees.
The harmful developmental stage of the
adventitious xylophages the larval stage. The larvae
emerge in the middle of June and penetrate into a
tree stem. The larvae of all these pests live in the
trees for a duration of three to five years , digging
deep (15-35 cm) paths inside the tree stem.
Depending on the environmental temperature, the
larvae migrate along the path to the positions where
the temperature conditions correspond to their
physiological optimum. In the Central Asian region
the peak the larvae’s nutrition activity in a
subcortical sieve tissue occurs in two phases: from
the end of March until the end of May and from the
beginning of September until the beginning of
November, when the air temperature does not
exceed 22-25°C.
During summer (when the air temperature is
about 35-400C) and autumn (before the approach of
steady colds), the larvae migrate to the depth of a
stem. The winter period, when larvae are in a
catalepsy condition, lasts not more than 60-70 days
which guarantees their successful over wintering. In
the autumn of the last year of development the larva
pupates. In the following spring the young imagoes
emerge of the cocoons, thereby closing the pest’s
developing cycle.
Baidulova (2006) previously reported that the
species composition and the number of various
pests in forest stands of the oak tree Quercus robur L
has sharply increased within the recent years. In that
study, the most dangerous pest groups were
apparently the specialized ones: leaf-eating - 9
species, gall gnat - 3, sucking - 4, leaf miners - 3,
stem damagers- 6. The leaf-eating pests are arguably
particularly deleterious, since they attack healthy
trees and completely eradicate the leaf. They give
periodic and constant outbreaks of numbers,
Species Composition and Injuriousness of Stranger Xylophilous Fauna Affecting Indigenous 365
approximately in every 3-4 years. Stem pests were
mostly beetles Scolitus intricatus Ratz.; Plagionotus
arcuatus L., Mesosa myops Dalm. P - Agrillus
angustulis Illig., A. biguttatus F., A. affinis F.
Here we report an ongoing invasion and
spreading of several non-native xylophiolous pests
belonging to the genera Monochamus, Acanthocinus,
Lamia, Ñetonia, Oberea and Xanthogaleruca (all
Coleoptera) and one Lepidopterous species Cossus
cossus L in the Central Asian region. Expansion of
these pests is continuing at a high rate.
A similar case of the xylophilous foreign pests
invasion has been recently reported by Telegina
(2004), which has indicated the massive expansion
of pests such as Apocheima cinerarius Erschoff, Lycia
hirtaria Clerck and Exàereta ulmi Schiffermüller on
species like Ulmus sp. and Salix sp. in northern
regions of Kazakhstan. It wasobserved that the
massive invasion of these pests has caused the full
destruction of many anthropogenic forest stands.
All invasive alien species found in this study are
the primary pests of coniferous trees (Danilevsky,
1980; Lobanov, 1981; Yanovsky, 2003; Borisova,
2004). According to our estimations, the pests were
transferred to the southern region of Kazakhstan
and Central Asia in the mid 90’s of the last century,
which is associated with the high degree of
constructional work in this region. During this
period, significant amounts of wooden construction
materials were imported presumably from different
Siberian regions, presumably introducing a great
number of foreign species of xylophilic insects and
accompanying microorganisms, which began to
expand throughout the local wood communities.
The ongoing expansion of the alien xylophilous
species results from combined action of several
factors:
1) Suitable climatic conditions (mild winter
allows high survival rate of larvae);
2) High abundance of appropriate susceptible
hosts (the studied (introduced)tree species
replace conifersas food substrate for the
xylophilous pests)
3) absence of the natural enemies (the paths made
in the local tree stems are deep enough to
protect the larva from eradication by local bird
species).
In fact, the alien species adapted very well to the
arid conditions of Central Asia, to the new nutritive
substrata and hosts and by the past period of time
have accomplished 3-5 full reproduction cycles
(generations)(Nurtazaev et al., 2010; Serikbai, 2011).
The present occurrence of these pest species is
seriously threating the existence of at least six
species of native trees, which build the basis of the
all large region’s settlements dendroflora.
Taking the unacceptability of using chemical
insecticides in cities and settlements and the absence
of natural enemies in the affected regions into
account, some alternative solutions need to be
found. We suppose that the design, development
and application of microbiological preparations
enriched with natural pest-specific bacterial
pathogens could bring a solution of the problem.
Bacterial insecticides have been successfully applied
against butterflies, beetles, and mosquitoes (Canan,
2013). Highly-efficient insect-specific toxins
produced by B. thuringiensis and other
microorganisms have little or no effect on other
organisms (worms, birds, mammalians) and are
considered to be environmentally friendly
(European Comission, 2008 ).
ACKNOWLEDGEMENT
The study is financed by the research foundation of
the Shymkent University (Shymkent, Kazakhstan).
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