Cent. Eur. J. Biol. • 4(4) • 2009 • 567–573
DOI: 10.2478/s11535-009-0044-y
Central European Journal of Biology
Pathogens of the spruce bark beetles
Ips typographus and Ips duplicatus
Research Article
Jaroslav Holusa1*, Jaroslav Weiser1, Zdenek Zizka2
1
Department of Forest Protection and Game Management,
Faculty of Forestry and Wood Sciences, Czech University of Life Sciences,
CZ-16521 Praha 6-Suchdol, Czech Republic
Institute of Microbiology, Academy of Sciences,
CZ-142 20 Praha 4, Czech Republic
2
Received 21 May 2009; Accepted 29 July 2009
Abstract: Pathogens of two important bark beetles, Ips typographus and Ips duplicatus, both in outbreaks connected with infestation
of spruces by the fungus Armillaria ostoyae, were compared at four localities in the eastern Czech Republic. Low infestations of
Chytridiopsis typographi, Nosema typographi, Menzbieria chalcographi, and Gregarina typographi were detected in I. typographus.
In I. duplicatus, only C. typographi and G. typographi were found and with low infection levels. The microsporidium, Larssoniella
duplicati, was not detected in I. typographus, but was detected in I. duplicatus at all localities in almost 80% of the samples (a sample
consisted of 40-50 beetles collected at one locality in one period) and often with a very high infection level (up to 57% of the beetles
infected in a sample). The infection level of L. duplicati did not differ between generations of I. duplicatus. I. duplicatus overwinters
mainly in the adult stage, and no decrease in the number of infected overwintering I. duplicatus was observed. The relatively constant
infection level of L. duplicati suggests that transmission is unlikely to be horizontal via oral ingestion.
Keywords: Microsporidia • Gregarina • Ips typographus • Ips duplicatus • Outbreak by Armillaria ostoyae
© Versita Warsaw and Springer-Verlag Berlin Heidelberg. 1. Introduction
Declining and dead spruce trees have occurred on
thousands of hectares in the eastern Czech Republic [1],
southern Poland [2], and northwestern Slovakia [3]. In
accordance with Manion’s theory, the decline of spruce
forests, is a result of predisposing factors and those
factors that actually kill the tree. Predisposing factors
include low soil pH, nutrient deficiency, water deficit,
and mechanical damage by logging machines. Trees
stressed by drought are further stressed by decreased
water supply because roots break in the drying soil [1].
Once the trees have been stressed and their
roots damaged, infection by the honey fungus
(Armillaria ostoyae (H. Romagnesi) Herink) become
obvious, and the trees are often then colonized and
567
killed by bark beetles. The bark beetles Pityogenes
chalcographus (Linnaeus, 1761) and Pityophthorus
pityographus (Ratzeburg, 1837) are the most abundant
in young forests while Ips duplicatus (Sahlberg, 1836),
I. typographus (Linnaeus, 1758), I. amitinus (Eichhoff,
1871), and P. chalcographus are predominant in mature
forests [1,2].
The pathogens of I. typographus have been
studied by many authors [4-26]. On the other hand,
only two reports on pathogens of I. duplicatus have
been published [27-28]. The recently described
microsporidium, Larssoniella duplicati Weiser, Holusa
et Zizka, 2006 was observed in I. duplicatus (but not
in I. typographus and I. amitinus) in the eastern Czech
Republic as well as in its area of origin in northeastern
Poland [27-28].
* E-mail: [email protected]
J. Holusa, J. Weiser, Z. Zizka
Both I. typographus and I. duplicatus aggregate
on Norway spruce (Picea abies (L.) Karst.), feed on
phloem [29], and thus may have similar pathogens.
The objectives of the current study were (i) to identify
and compare the pathogens of these two bark beetles
in one area and (ii) to determine the infestation levels
of pathogens over several generations of these bark
beetles.
2. Experimental Procedures
The study area is situated in the eastern Czech Republic.
The four study localities (Table 1) were located in
intensively cultivated hills with forest coverage of 9-70%
and a dominance of Norway spruce, which constitutes
30-50% of the trees [30]. All spruce forests in this area
are planted and managed and have recently been
stressed by drought and A. ostoyae [1]. The localities
were located at a similar latitude, the distance between
adjacent localities ranged from 18 to 28 km, and locality
altitude ranged from 380 to 450 m above sea level.
I. typographus and I. duplicatus emerge from the
forest duff on warm spring days and fly to host trees
that are stressed. These species use aggregation
pheromone to attract more individuals of the same
species to the tree for the purpose of killing the tree and
for mating. The pheromone attracts both sexes. The
attracted males join the attack and secure an area for
mating and oviposition; this area consists of a hole and
chamber beneath the bark called a “nuptial chamber”.
The females construct a tunnel (“maternal gallery”)
beneath the nuptial chamber in which to lay eggs. In
all species of the genus Ips, several females join each
male in his nuptial chamber [31-32]. Both beetle species
have two or three generations per year with the main
peaks of bark beetle emergence in April/May, July and
August/September [31].
Mature beetles were collected from five trees
(adjacent trees were about 100 m apart) in each of the
four localities in each of six sample periods. Different
trees were used for each sample period because
beetle-infested trees are removed by forest managers.
Samples periods were selected based on the times
when new generations begin, however this is associated
with weather and vegetation season. In 2002, the
sampling periods were 25-27 May, 29-30 July, and
17-19 September. In 2003, the sampling periods were
16-27 May, 26-27 June, and 27-30 August.
The beetles were collected from trees that had
been recently invaded by beetles and that had signs of
infestation by A. ostoyae (bulging trunk base, root decay,
and syrrocium under bark). In spring (the first sampling
period), adult beetles of the parental generation (P) were
collected as they emerged from their nuptial chambers in
the tree trunks. In summer (the second sampling period),
the beetles of the parental generation (P) were collected
by removal from the maternal galleries and offspring
adult beetles of F1 generation were also collected.
Thus, in the summer beetles of two generations were
collected from the same tree. Only mature beetles of
the F1 generation at the end of maternal feeding were
studied because beetle pathogens become easier to
detect as the beetle mature [13]. At the end of summer
(the third sampling period), we collected mature beetles
of the F1 generation after they had mated and laid eggs
and mature beetles of the F2 generation (Figure 1). The
same collection methods were repeated in the second
year of study. In total, five generations (P, F1, F2, F3,
F4) of beetles were collected from the trees. For each
locality and sample period, 40(-50) beetles of each
species were collected. Sometimes it was problematic
to find mature beetles that had already left galleries
or were not mature, but this was mainly limited to the
locality of Bystřice nad Olší. Beetles and associated
bark were stored in small film boxes (volume of 30 cm3)
at 4°C and were dissected within 10 days. Because the
beetles were inactive at 4°C, transmission of diseases
among beetles within one box was not possible.
2002
May
July
P
P
F1
2003
September
May
June
F2
F2
August
F1
F2
F3
F3
F4
Figure 1.
The generations of adult bark beetles in six sampling
periods in 2002 and 2003 (P = parental; F1 = offspring
of P; F2 = offspring of F1 and overwintering generation
for 2003, and so forth).
Given the specific interactions between L. duplicati
and their host beetles [27], only beetles that were living
when collected were dissected. Midguts of all beetles
were removed with the last abdominal segment and were
examined according to the method of Wegensteiner et al.
(1996) [15]. The beetles were decapitated and dissected
in a drop of water on a microscopic slide, and the whole
gut together with the Malpighian tubules, the gonads,
and parts of the adipose tissue were examined for the
presence of pathogens using a light microscope (150x
and 500x magnification).
To estimate the abundance of bark beetles, the
presence of bark beetles in 50 trees that had been
infested by beetle, cut, and left on the forest floor were
568
Pathogens of the spruce bark beetles
Ips typographus and Ips duplicatus
examined in each of the six sampling periods. For each
of these trees, the beetle entry holes were counted
on four 1 m sections; the sections were located in the
middle of the crown, at the base of the crown, in the
middle of trunk below the crown, and near the trunk
base.
The levels of pathogen infection between the two
species of bark beetle were compared with a twosample t-test. Infection levels between generations
were compared by Kruskal Wallis one-way analysis
of variance. Regression and all other analyses used
α=0.05 and were performed with the Statistica 8.0 [33].
In the analyses, the term infection level indicates the
percentage of beetles infected in each sample of beetles,
and the term constancy indicates the percentage of
samples with at least one infected beetle.
3. Results
During the two years of sampling (2002 and 2003),
715 and 653 specimens of I. typographus and 863
and 588 specimens of I. duplicatus were dissected
Beetle
species
Locality
Latitude;
Longitude
Number of beetles
(P/F1/F2/F3/F4)
Pustá
Polom
49°48-52';
17°58'18°04'
Václavovice
and inspected. In total, five species of pathogens were
diagnosed (Table 1). The microsporidium Chytridiopsis
typographi (Weiser, 1954) and the gregarine Gregarina
typographi (Fuchs, 1915) were found in both bark beetles,
but the microsporidium Nosema typographi (Weiser,
1954) and the gregarine Menzbieria chalcographi
(Weiser, 1955) were found only in I. typographus.
The microsporidium L. duplicati was detected only in
I. duplicatus. Mixed infections were also observed in
the studied hosts.
In I. typographus, the infection levels of the pathogen
species differed slightly between sampling localities
(Table 1). N. typographi and M. chalcographi infection
was very low and rare: in both cases, they were found
in only two beetles (≤5% of the beetles sampled).
In 2003, no case of infection with N. typographi or
M. chalcographi was found. Infection by C. typographi
was found in 17.5% of the samples although its
infection level was rather low in most cases (≤5%) and
never exceeded 25%. C. typographi was even missing
in some localities. G. typographi was present in 35%
of the samples, and its mean infection level was lower
than 5%. Occasionally it reached 20% (Table 1).
Pathogens and infection levels (%)
Chytridiopsis
typographi
Nosema
typographi
Menzbieria
chalcographi
Larssoniella
duplicati
Gregarina
typographi
455
(80/80/145/100/50)
2.6
0.0
0.003
0.0
4.3
49°44';
18°21'
420
(80/80/120/100/40)
0.0
0.2
0.0
0.0
0.7
Jánské
Koupele
49°44';
17°43'
375
(80/85/150/40/40)
0.3
0.3
0.0
0.0
0.5
Bystřice nad
Olší
49°36´;
18°43'
118
(40/40/0/0/38)
0.0
0.0
0.0
0.0
1.6
Constancy
17.5
5.0
5.0
0.0
35.0
Ips
typographus
Ips
duplicatus
Pustá
Polom
49°48-52';
17°58'18°04'
422
(80/80/120/92/50)
10.6
0.0
0.0
25.0
1.4
Václavovice
49°44';
18°21'
370
(50/80/120/80/40)
0.0
0.0
0.0
21.8
1.6
Jánské
Koupele
49°44';
17°43'
416
(90/86/120/80/40)
0.9
0.0
0.0
12.6
0.0
Bystřice nad
Olší
49°36´;
18°43'
243
(40/40/83/40/40)
0.0
0.0
0.0
3.4
0.0
Constancy
10.0
0.0
0.0
78.0
28.0
Table 1. Infection of adult bark beetles Ips typographus and Ips duplicatus by five pathogens in four localities. Infection levels are the percentage of
beetles infected and the total number of beetles collected over six sample periods in 2002 and 2003. Constancy indicates the percentage
of samples with at least one infected beetle.
569
J. Holusa, J. Weiser, Z. Zizka
In I. duplicatus, C. typographi was found in only 10% of
the samples and in only two localities; these samples had
very low infection levels. G. typographi was also present
in only 10% of the samples and with low mean infection
levels (≤5%); its highest infection level in a sample was
30% (Table 1). Another microsporidium, L. duplicati, was
present in I. duplicatus in all localities in almost 80% of
the samples and often with a very high infection level (as
high as 57%; Table 1). Infection levels of C. typographi
were equal in both bark beetles species (t=1.21; P>0.10),
but L. duplicati was found only in I. duplicatus (t=-6.55;
P<0.001) and G. typographi prevailed in I. typographus
(t=2.63; P<0.01).
The volume of wood infested by bark beetles differed
between forests districts (each of the four districts was ca
1500 ha) where the study localities were designated. This
volume varied between 0.16 and 23.28 m3 of infested
trees/ha, but there was no significant correlation between
volume of infested wood per year and total yearly infection
levels of all pathogens (I. typographus: C. typographi:
r=0.61; P>0.10; G. typographi: r=0.62; P>0.05;
I. duplicatus: C. typographi: r=0.06; P>0.10; L. duplicati:
r=0.68; P>0.05; G. typographi: r=0.24; P>0.10).
Infection levels of particular generations in both
species were very low for most pathogens and varied
between 0 and 6% for C. typographi and G. typographi.
Differences in infection levels among generations were
not significant (C. typographi in I. typographus: χ2=5.13,
P>0.10; G. typographi in I. typographus: χ2=12.82,
P>0.10; C. typographi in I. duplicatus: χ2=13.71, P>0.10;
G. typographi in I. duplicatus: χ2=6.08, P>0.10).
Infection levels of L. duplicati among generations
varied between 5 and 35% (Figure 2), but differences
among generations were not significant (χ2=13.59,
P>0.05). Post hoc tests did not show differences
between generations (Kruskal-Wallis test: H
(8, n=30)=11.98; P>0.10.
4. Discussion
Fewer pathogens of I. typographus were detected
in this study and in Holusa et al. (2007) [28] than in
some former studies. Two pathogens appearing in
I. typographus in the Sumava Mountains [34] and in
Austria [10,15,21-23] were absent in our samples:
Entomopoxvirus
typographi
Wegensteiner
and
Weiser, 1995 and Malamoeba scolyti Purini, 1980.
The microsporidium Unikaryon montanum (Weiser,
Wegensteiner & Zizka, 1998), known from the foci in
Austria and Germany [3,19], also was not found in our
study.
Infection rates of C. typographi and G. typographi
varied little among samples. They were very similar
to those recorded by some authors [14,15,21,23].
Although both pathogens often occur together with
high infection levels [35], a high infection level is also
possible when only one pathogen is present, e.g., in
G. typographi [24]. Low prevalence of N. typographi is
common [6,14,22,34]. Infection by M. chalcographi is
rare but can be very high in some cases [23,34].
Figure 2. Larssoniella duplicati infection levels in five consecutive generations of Ips duplicatus in the eastern Czech Republic. The inner square,
the mean; the rectangle, ± SE; the bars, ± SD).
570
Pathogens of the spruce bark beetles
Ips typographus and Ips duplicatus
Although infection levels should depend on the
population density of bark beetles, infection levels in
this study were not related to the abundance of bark
beetles as represented by the volume of infested trees
in the different localities. As noted by Wegensteiner
and Weiser (1996) [21], however, the different levels
of pathogen infection in an area may not correlate with
different numbers of beetles when the beetles in that area
represent one, highly mobile population. The potential
mobility of beetles can prevent the development of
beetle subpopulations with different pathogen sets [22].
Because the localities in the present study were only
separated by about 20 to 30 km, the bark beetles could
have readily moved from one locality to another; beetles
are known to migrate regularly more than 1 km [32,36].
It follows that the bark beetles present in the entire study
area (encompassing all four localities) represented one
population for each species, and each of the two bark
beetle populations in this study had a relatively constant
pathogen infection level among the different localities.
As discussed below, patches or subpopulations with
very large numbers of beetles can occur when groups of
beetle-infested trees are left in the forest, which was not
the case in this study.
Except for L. duplicati, pathogens were not abundant
and infection levels were generally low in our study. This
could be due to the low number of beetles in sampled
at Bystřice nad Olsi. We suspect, however, that this
arises from forest management and to the distribution of
stressed trees. How a forest is managed likely affects
the buildup of bark beetles and the pathogens of bark
beetles. In unmanaged or poorly managed forests,
trees infested by bark beetles usually occur in groups
which generate hot spots of high beetle and pathogen
numbers. The repeated development of new generations
of bark beetles is common in these groups of infested
trees and beetle numbers can remain very high over
many generations. When their numbers are very high,
young beetles often cannot find enough space for their
maturation feeding, and are forced to continue feeding
by crossing other nearby galleries. Such movement
increases the chance of pathogen transmission and
therefore results in an increase in pathogens [13].
Consequently, groups of infested trees generate hot spots
of high beetle and pathogen numbers. This is the case
in the Sumava Mountains (Czech Republic) and Austria
localities, where C. typographi and Entomopoxvirus
typographi can be abundant pathogens of bark beetles
[15,28,34].
In contrast, beetle infestations in well-managed
forests, like the forests in our study, are more patchy
because foresters rapidly remove infested trees. Removal
of trees heavily infested by bark beetles prevents the kind
571
of pathogen buildup that occurs in unmanaged forests.
This has led to a substantial decrease in pathogens of
bark beetles and even the disappearance of N. typographi
and M. chalcographi in 2003 (this study) and 2004 [28].
Another reason why groups of trees with bark beetles
were observed only occasionally during this study was
that beetles usually infested individual spruce that were
scattered in forests and were stressed and dying from
drought and infection by honey fungus [1,37]. In some
periods the key mortality factors are still drought [38]
and infection by the honey fungus [1] rather than bark
beetles. Given the removal of beetle-infested trees by
foresters and the patchy nature of the infestation (as
related to stress by drought and the honey fungus),
it is perhaps not surprising that pathogens (except
L. duplicati, see further) were not abundant and infection
levels were generally low.
Differences in the infection levels of C. typographi
and G. typographi among generations in both bark beetle
species were not significant. This could result from a low
infestation level, but even when infection levels were
higher, the numbers of infected beetles did not differ
between generations [13].
L. duplicati is definitely specific to I. duplicatus
[27-28]. L. duplicati can achieve a high infection level in
I. duplicatus (present study, [28]) and the high infection
level frequently occurs throughout the beetle’s range
[28]. Infection levels did not show any trend over time
in our study and has also been reported previously in
one locality [28]. The lack of difference in the infection
level of L. duplicati between bark beetle generations
was confirmed by our study. I. duplicatus overwinters
mainly in the adult stage [31,39], leading one to expect
a decrease in the percentage of overwintering infected
adults because of death resulting from infection. In an
earlier study, high winter mortality resulted in relatively
low numbers of living infected beetles in spring [13].
A relatively constant infection level of L. duplicati is
consistent with the hypotheses that transmission is not
horizontal or the result of oral ingestion of pathogen
propagules [28].
In summary, C. typographis and G. typographi were
detected in both I. typographus and I. duplicatus. These
pathogens are known to overlap in host range and have
been observed in various beetle species [22,26,35].
The microsporidium L. duplicati was very common in I.
duplicates. The high infection level occured throughout
the beetle’s range and did not show any trend over time
[28]. N. typographi and M. chalcographi were found only
in a few specimens of I. typographus at the beginning of
our study. Their disappearance could be a result of very
intensive forest management and elimination of bark
beetle hot spots.
J. Holusa, J. Weiser, Z. Zizka
Acknowledgements
This work was partly supported by the grant No. QH 81136
of the grant agency of the Ministry of Agricultural of the
Czech Republic. The authors would like to thank to Dr.
Bruce Jaffee for linguistic and editorial improvements.
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