Breeding performance of a univoltine population of Ips typographus

(Coleoptera: Curculionidae) at epidemic level in Central Europe:

Parasitoids and pathogens lag their host

Jaroslav Holuša and Karolina Lukášová

Department of Forest Protection and Game Management, Faculty of Forestry and Wood

Sciences, Czech University of Life Sciences, Kamýcká 129, CZ-16521 Prague 6 – Suchdol,

Czech Republic

Abstract

1. The purpose of the present study was to compare the levels of pathogen infection in

maternal beetles, parasitism of the offspring, abundance of predators, and reproductive

success of the univoltine generation of I. typographus in areas characterized by small-

scale and short-term outbreaks, and the other is large-scale and long-term outbreaks. A

lag in the rising densities of parasitoids and pathogens in long-term outbreaks can be

expected, as can be higher reproductive success in short-term outbreaks.

2. We selected two localities in the Sumava Mts in altitudes ca 1100 m within which

pairs of study plots were defined. The first study plot is representative of large-scale

(>100 ha) and long-term (>10 years) outbreak, and the volume of progressively

infested wood >1000 m3. The second study plot represents the small-scale (<1 ha) and

short-term (2–3 years) outbreak which originated in 2009-2010 in a complex of

previously uninfected forests (>10 ha) at a distance ca 700 m from the first plot. The

volume of infested trees were <100 m3. Five trees were studied on each study plot.

3. No significant differences in mean values of colonization density, abundances of

surviving specimens of I. typographus and length of maternal galleries were

determined. Mean values of eggs laid were larger in study plots characterized by

short-term outbreak.

4. Mean values of parasitoids per m2 of bark were higher on study plots with long-term

outbreak, as was the percentage of parasitism by ectoparasitoids. No statistically

significant differences in the percentages of adult larvae of endoparasitoids in maternal

beetles were determined, as was the case also for Tomicobia seitneri and the

percentages of maternal beetles in which eggs of endoparasitoids were found.

5. No statistically significant differences in the percentages of maternal beetles infected

by I. typographus entomopoxvirus ItEPV and Chytridiopsis typographi were

determined between plots with short-term outbreak versus long-term outbreak.

Significantly higher infection rates occurred only for Mattesia schwenkeiin long-term

outbreak areas.

6. The number of parasitoids and entomopathogens respond numerically to bark beetle

density. Predation and/or parasitism did not play a significant role in reducing the

outbreak population.

Keywords Epidemic population, intraspecific competition, natural enemies, spruce bark

beetle.

Introduction

Ips typographus (Linnaeus, 1758) is one of the economically most serious pest species

attacking Norway spruce in Eurasia (Christiansen & Bakke, 1988). During the past century, I.

typographus outbreaks have occurred in many places across all of Europe (Grégoire & Evans,

2004). Since 1950, 2–9 million m3 of wood have been damaged annually by bark beetles, and

predominantly by I. typographus (Schelhaas et al., 2003). In the 1990s, gradations began

appearing also in places where these had not occurred previously (Grégoire & Evans, 2004).

For successful colonization of living trees, a high density of attacking I. typographus is

needed in order to overcome the trees’ defensive system (Mulock & Christiansen, 1986;

Christiansen et al., 1987). The bark beetles’ reproductive success depends upon three main

conditions: temperature, natural enemies, and inter- as well as intraspecific competition

(Faccoli & Bernardinelli, 2011).

Thanasimus formicarius (Linnaeus, 1758) and other predatory beetles (Cleridae) and flies

(Dolichopodidae, especially Medeterinae), as well as parasitic wasps (Pteromalidae and

Braconidae) may cause significant mortality, but their net effect remains debated and may be

difficult to detect due to the strong influence of resource-based dynamics (Christiansen &

Bakke, 1988; Weslien, 1994; Lawson et al., 1997; Wermelinger, 2002, 2004; Kenis et al.,

2004; Økland & Berryman, 2004; Fayta et al., 2005; Ryall & Fahrig, 2005; Feicht, 2006;

Hulcr et al., 2006; Økland & Bjørnstad, 2006; Warzee et al., 2006; Hedgren, 2007;

Hilszczanski et al., 2007; Johansson et al., 2007). Other wasps, beetles, flies, ants, fungi,

birds, shrews and entomopathogens such as viruses and microsporidia have also been reported

as possible predators (Wegensteiner & Weiser, 1996a; Reeve, 1997; Gilbert & Grégoire,

2003; Hedgren, 2004; Kenis et al., 2004; Hilszczanski et al., 2007), but their population-level

effect is rarely quantified (Kenis et al., 2004).

It is generally accepted that bark beetles’ population dynamics are affected mainly by

factors influencing the resistance of the tree, while the beetles’ natural enemies are regarded

as comprising only a minor factor, and that, at best, those enemies only accelerate the collapse

of the bark beetle population (Reeve, 1997). If the combination of basic factors favours it, a

population can remain in outbreak for a long time. These factors include an adequate supply

of suitably nourishing plants, sufficient population density, suitable climatic conditions, and

low levels of predation by natural enemies (Raffa et al., 2008).

To date, no case has been confirmed wherein a population of parasitoids would stop a bark

beetle outbreak. Even when parasitism is high, the numbers of I. typographus per metre can

reach dangerous values (Feicht, 2004). The quantities of predators, pathogens and parasitoids

present tend to correspond to the beetles’ population density, but their response can be

delayed by weeks or even as much as a year. The Cleridae, Diptera (Dolichopodidae,

especially Medeterinae) as well as parasitic Hymenoptera (Pteromalidae and Braconidae) can

cause significant mortality, but their influence remains unclear (Kenis et al., 2004).

Similarly, influence of pathogens on population dynamics remains unknown (Lukášová &

Holuša, 2012). In the case of parasitisation by nematodes, we presume an influence on bark

beetles’ speed of development, fertility, survival and flight activity (Nickle, 1963; Thong &

Webster, 1975; Lieutier, 1981; Kaya, 1984; Tenkáčová & Mituch, 1986; Forsse 1987).

In cases of long-term overabundance, with high population densities and an absence of

forestry management, significant increase of mortality and parasitism is often presumed

(Weslien & Schroeder, 1999, Wegensteiner & Weiser,1996b, Holuša et al. 2009).

It is difficult to quantify the effects of predators on bark beetles. Measuring the

consumption of prey in the field is a complicated matter, and predators may forage not solely

on the target bark beetle but also on other subcortical insects, including other predators and

parasitoids (Mendel et al., 1990), and thereby even reduce the overall detrimental effect on a

bark beetle population. For example, T. formicarius is an important mortality factor for

Medetera (Fischer von Waldheim, 1819) larvae (Nuorteva, 1959).

On the other hand, most studies on parasitoids of Scolytidae have provided some

quantitative evaluations of parasitism, either as parasitism rates or as relative abundance of

parasitoid species. Parasitism rates varying from 0 to 100 % have been found. However,

parasitism rates and consumption rates are poor indicators of the real impact of natural

enemies on bark beetle populations (Kenis et al., 2004). Several authors state that natural

enemies do not play an important role in regulating bark beetle populations (e.g. Sachtleben,

1952; Bombosch, 1954; Faccoli, 2001) while a few others assert just the contrary (e.g.

Mendel, 1987), but few of these statements are based on solid data.

To better evaluate the impacts of parasitoids and predators on bark beetle populations,

various methods have been used, such as consumption rate-based assessments (e.g. Dippel et

al., 1997; Wermelinger, 2002), life table analyses, and natural enemy exclusion experiments.

Life tables are not easy to construct for bark beetles because of the problem of overlapping

generations.

Kenis et al. (2004) suggest that factors can be assessed easily because sample logs can be

considered as separate populations with different beetle densities. But question is if boxed

populations develop naturally, if there is change parameters of the bast, the microclimate and

thereby lend further support to survival of the parasitoid.

The influences of predation and parasitism could be examined by comparing populations

with identical densities but originating from different time periods. We can hypostatized if

reproduction were identical in the populations but parasitism different, then this fact would

prove that there was negligible influence of predation and/or parasitism on the populations.

A shortcoming of all studies is also the fact that they observe predation and parasitism only

in the offspring generation and no data are known for parental beetles. The purpose of the

present study was to compare the levels of pathogen infection in maternal beetles, parasitism

of the offspring, abundance of predators, and reproductive success of the univoltine

generation of I. typographus in areas characterized by small-scale (<1 ha) and short-term (2–3

years) outbreaks, and the other is large-scale (>100 ha) and long-term (>10 years) outbreaks.

Both areas had high population densities. A lag in the rising densities of parasitoids and

pathogens in long-term outbreaks can be expected, as can be higher reproductive success in

short-term outbreaks. In this work, we studied all stages under field conditions so that

identical conditions were ensured for all trees.

Materials and methods

Study area

The study area was situated in the Šumava Mountains. Whereas in past centuries these

mountain forests had been significantly altered by economic activities, today they are

dominated by artificially established forests. There has been an I. typographus outbreak

ongoing in the Šumava Mts for more than 15 years. During the 1990s, there was a widespread

outbreak of I. typographus in the central part of the Šumava which led to wholesale

disintegration of spruce stands. On the Czech side of the border with Germany, two

approaches were implemented during that period: part of the stands was left without

intervention, and on the remaining area bands of clear-cuts were created in the vicinity of the

so-called intervention-free zone (Mánek & Ešnerová, 2007). In January 2007, the Kyrill

windstorm left approximately 15,000 m3 of damaged wood in its path in areas of those second

zones around the so-called “Calamity Skidway” area (Svoboda, 2007). A year after this event,

there was sharp increase in the volume of trees infected by bark beetles. In 2011, more than

235,000 m3 of bark beetle wood was recorded, which represents a slight decrease in

comparison to the 2009 and 2010 seasons.

Table 1 Main characteristics of the monitored stands.

Locality Coordinates

Altitude

m a.s.l.

Mean

tree age

Duration of

outbreaks

Oblík

49°3'38.629"N,

13°25'52.932"E 1,140 160 >10

Oblík

49°4'2.974"N,

13°25'59.411"E 1,170 90 2

Ztracený

48°59'7.603"N,

13°30'22.735"E 1,120 170 >10

Ztracený

48°59'23.617"N,

13°30'40.858"E 1,100 150 3

The study localities are situated in areas of the 8th altitudinal forest vegetation zone

consisting of spruce on so-called acid stands (i.e. firm, not waterlogged with stands of small-

reed or blueberry). The main trees are spruce Picea abies (Linnaeus) Karsten, rowan Sorbus

aucuparia Linnaeus, and, on peat-bogs, also mountain pine Pinus mugo Turra. The area has

above-average precipitation (1,224 mm per year). Average annual temperature is in the range

of 5–6 °C (Culek, 1996). Due to their elevation, the studied localities are in an area where

only one generation of I. typographus (Wermelinger, 2004) occurs regularly.

We selected two localities within which pairs of study plots were defined (Table 1). The

first study plot is representative of large-scale (>100 ha) and long-term (>10 years) outbreak,

and the volume of progressively infested wood >1000 m3. The second study plot represents

the small-scale (<1 ha) and short-term (2–3 years) outbreak which originated in 2009-2010 in

a complex of previously uninfected forests (>10 ha) at a distance ca 700 m from the first plot.

The volume of infested trees were <100 m3.

Experimental procedure

The mean diameter (d1.3) of studied trees was 26.0±6.1 cm. At the edges of the plots, trees

were cut where there were groups of trees or areas with trees infested or abandoned by bark

beetles. Norway spruce trees (Picea abies) displaying symptoms of bark beetle infestation

(i.e. presence of entry holes in the bark, wood dust, oozing of resin) were selected and cut

down on 23 August 2012. Five spruce trees distributed along a horizontal line of

approximately 100 m were chosen.

After subsequently stripping the trees of their branches, always four sample areas of bark

were analysed. These were debarked bands with length equal to half the circumference of the

trunk and width of approximately 0.5 m (sample area). Sample area I (base) was situated 0.5

m from the tree base, sample area II (stem) at middle distance between the base and the

bottom of the tree’s crown, sample area III (break) at the beginning of the crown, and sample

area IV (crown) at the centre of the crown. For each analysed tree, its total height, trunk

diameters at the individual sections, thickness of the bast and bark, and the dimensions of

each section were recorded.

Within each sample, the number of maternal I. typographus galleries was recorded, as were

total number of eggs laid by the females (in 10 examined maternal galleries), number of

individuals of the different development stages (larva of 1st–3rd instars, pupae, callow

beetles). Also recorded was the presence of other bark beetle species (Scolytinae subfamily).

Ectoparasitoids (in particular representatives of the Braconidae and Pteromalidae families

of the Hymenoptera order) were determined by visual examination. The numbers of their

larvae, pupae and cocoons were recorded. The presence and numbers of larvae and adults of

spruce bark beetle predators were recorded, and especially from the Raphidioptera order and

the Diptera and Thanasimus (Coleoptera) genera.

All maternal beetles were collected from the individual sections using an exhauster. The

individual beetles were placed in 2 cl Eppendorf micro test tubes and a piece of damp gauze

added to maintain 100 % relative humidity. The beetles were immediately frozen and stored at

−4 °C. All internal organs, including the fat body, were later dissected in a water drop using

surgical tweezers. Each dissected beetle was examined under an Arsenal LPE 5013i-T light

microscope (Arsenal s.r.o., Prague, Czech Republic) at 40–400x magnification to determine

its sex, whether it was infected with one or more pathogens, and pathogen identity. The

presence of viruses, microsporidia, protozoa, nematodes and parasitoids (of the Braconidae

and Pteromalidae families) was detected.

Data analysis

Sex ratio, numbers of eggs laid per gallery, and length of maternal galleries are summarized

as mean (±SD).

Production (per m2 bark) was calculated as the numbers of bark beetles in all living stages

(L3 larvae, pupae, callow beetles reduced by the number of parasite-infected larvae.

Parasitism was calculated as the ratio of the total number of parasitoids (larvae on the bark

beetle larvae, parasitoid larvae outside bark beetle larvae, cocoons, pupae and adults of the

parasitoids) to the total number of parasitoids (as listed) and to all the living development

stages of the bark beetles.

For explorative reasons, bark beetle mortality inflicted by predators was assessed

(consumption of hatched bark beetle larvae). Based upon their estimated consumption during

juvenile development, the mortalities of the scolytid population were calculated for each

group. Thanasimus spp. (Cleridae) consumes 47 (44–57) larvae bark beetles (Gauß, 1954;

Mills, 1985; Heidger, 1994; Hérard & Mercadier, 1996; Dippel et al., 1997) and Diptera

larvae consume 6 (5–10) larvae bark beetles (Hopping, 1947; Nuorteva, 1959; Hérard &

Mercadier, 1996; Dippel et al., 1997). The larvae of some Raphidioptera are predators on or

beneath the bark. A few species of Raphidiidae are known to forage non-specifically on

cerambycids, bark beetles, and other subcortically living organisms (Schimitschek, 1931;

Wichmann, 1957). They may be able to access scolytid galleries only after the bark is

loosened, (e.g. by maturation feeding of bark beetles or by woodpeckers [Wichmann, 1957]).

Therefore their proportional contribution to mortality cannot easily be calculated.

The mean breeding performance of I. typographus was assessed using population growth

rate (PGR), indicating the multiplication of a population over a unit time period (one

generation). PGR is defined as the number of emerging daughters (total offspring/2) per

mother (i.e. per maternal tunnel). The offspring sex ratio was assumed to be 1:1 (Annila,

1971).

Colonization density, population growth rate, production and abundance of predators per

m2 of bark were calculated for each sample. Infection level was calculated as the percentage

of beetles positive for infection at a given tree (where >30 mature beetles had been collected

from such tree). Summary parameters were calculated for each study plot as mean values

(±SD) per m2 of bark.

Homogeneity of variance was tested by Cochran’s C test and normality by the

Kolmogorov–Smirnov test (D statistic). Mean values for parameters of all samples and

infection levels of beetles per tree were compared between plots with short-term and log-term

outbreak (Wilcoxon test, paired t-test). Densities of parasitoids were determined for individual

tree sections using Friedman’s ANOVA and Kendall’s coefficient of concordance. The

acquired data was statistically evaluated using Statistica 9.

Results

I. typographus was detected on all infested trees. This species was present in 86.1 % of all the

studied samples. Polygraphus poligraphus (Linnaeus, 1758) was detected in 26.7 % and

Pityogenes chalcographus (Linnaeus, 1758) in 12.5 % of studied samples. Places where

infestation by I. typographus was not detected were dry or the beetles were covered in resin,

or these were places with healthy bast but not colonized.

Table 2 Main findings for Ips typographus populations in studied plots. The population growth rate,

defined as the number of emerging daughters (total offspring/2) per mother (i.e. per maternal tunnel)

was calculated for each sample. Bark beetle consumption is calculated like percentage of hatched bark

beetle larvae killed by parasitoids and predators (estimated consumption during juvenile development)

Item Oblík Oblík Ztracený Ztracený

Duration of outbreak (years) 2 >10 3 >10

Colonization density (mature galleries) per m2 of bark 370.2±316.4 340.6±149.0 408.3±200.3 315.0±214.8

Sex ratio (females/males) 1.4±0.4 1.4±0.4 1.4±0.3 1.4±0.5

Gallery length (mm) 45.0±9.1 44.8±19.5 55.1±18.7 65.5±19.3

Eggs per gallery 26.3±4.2 22.5±8.4 27.0±13.7 26.5±9.8

Production per m2 of bark 238.4±265.5 314.7±172.9 354.8±367.7 344.3±408.2

Population growth rate 0.8±0.9 0.8±0.9 0.5±0.5 0.5±0.7

Ectoparasitoids per m2 of bark 41.6±58.9 148.6±175.3 32.5±74.7 152.7±198.3

Bark beetle consumption by ectoparasitoids (%) 0.4 1.9 0.3 1.9

Parasitism (ectoparasitoids larvae) (%) 10.3±11.6 50.3±41.7 15.0±30.0 42.7±38.1

Diptera larvae per m2 of bark 4.8±12.4 8.4±16.6 16.6±21.2 29.1±39.1

Bark beetle consumption by Diptera larvae (%) 0.3 0.6 0.9 0.4

Thanasimus larvae per m2 of bark 12.5±17.6 4.79±7.06 12.2±45.3 2.2±5.4

Bark beetle consumption by Thanasimus larvae (%) 5.9 3.0 5.1 1.1

Raphidioptera larvae per m2 of bark 0 19.2±23.8 3.0±5.5 0

The population was found to be in the larvae (L3), pupae and callow beetle stages. No

emergence holes were observed. Mean values for colonization density of mature galleries, sex

ratio, and average number of eggs laid per female, length of maternal galleries, population

growth rate, production, and predator abundances (including larvae of Diptera, Thanasimus

spp., and snakefly [Raphidioptera]) are shown in Table 2.

No significant differences were determined in mean values for colonization density (z =

0.12, p > 0.10), abundances of surviving specimens of I. typographus (L3 larvae, pupae,

callow beetles) (z = 1.39, p > 0.10), or length of maternal gallery (t = −1.75, p > 0.10)

between short-term and long-term outbreaks (Figs. 1-2). Mean values for number of eggs laid

were higher in study plots with short-term outbreak (t = −3.06; p < 0.01).

No statistically significant differences were determined in abundances for larvae of Diptera

(z = 0.45, p > 0.10), of the genus Thanasimus (z = 0.24, p > 0.10), or of snake flies (z = 1.10,

p > 0.10). Consumption by predators (Diptera and Thanasimus larvae) did not exceed 7 %

(Table 2).

Larvae of ectoparasitoids were detected on larvae of the third instar and pupae of the bark

beetles, while pupae of Chalcidoids from the Pteromalidae family or cocoons of Braconidae

and (exceptionally) adults were found in the galleries. Mean value of ectoparasitoids per m2 of

bark was higher on study plots with long-term outbreak (z = 2.83; p < 0.01), as was the

percentage of parasitism by ectoparasitoids (z = 3.23, p < 0.01). Consumption by parasitoids

did not exceed 2% (Table 2). No significant differences in density of parasitoids were

determined for individual tree sections (Friedman’s ANOVA [N = 8, df = 3] = 3.98, p > 0.10,

and Kendall’s coefficient of concordance r = 0.16).

From all samples of the 20 studied trees, 889 live maternal beetles were extracted. In the

acquired samples, the presence of intestinal (10.5 %) and extra-intestinal nematodes (12.0 %)

was determined by dissection. In most cases, these were invasive larvae which were very

difficult to identify. In 4.0 % and 3.3 % of the samples, respectively, the species

Contortylenchus diplogaster (von Linstow, 1890) Rühm, 1956 and Parasitylenchus dispar

(Fuchs, 1915) were detected.

The microsporidium Chytridiopsis typographi [(Weiser 1954) Weiser, 1970] was observed

in 2.1 % of material beetles in the form of thin-walled cysts within the stomodeum. The

neogregarine Mattesia schwenkei (Purrini, 1977) was identified in the fat body in 32.6 % and

gregarine Gregarina typographi (Fuchs, 1915) in 0.4 % of maternal beetles. The

entomopoxvirus ItEPV was detected in the middle intestine of only 17.1 % of those

individuals analysed. The eggs of endoparasitoids were detected in 4.8 % of adult I.

typographus individuals, Tomicobia seitneri (Ruschka, 1924) in the first larval instar in 7.6 %

of those individuals, and endoparasitoids not closely specified were detected in 20.2 % of

adults.

No statistically significant differences in the percentages of adult endoparasitoid larvae

were determined in maternal beetles (z = 0.16, p > 0.10), the percentages of T. seitneri in

maternal beetles (z = 0.73, p > 0.10), and the percentages of maternal beetles where eggs of

endoparasitoids were found (z = 0.52, p > 0.10).

No statistically significant differences in the percentages of maternal beetles infected by

ItEPV (z = 0.33, p > 0.10) or C. typographi (z = 1.15, p > 0.10) were determined for plots

with short-term outbreak versus those in long-term outbreak areas. Significantly higher

infection rates occurred only for M. schwenkei (z = 2.37; p < 0.05) in long-term outbreak

areas.

Table 3 Infection (%) by nematodes and pathogens in mature I. typographus beetles at studied

localities

Locality Oblík Oblík Ztracený Ztracený

Duration of outbreaks (years) 2 >10 3 >10

Number of studied beetles 96 111 174 508

Nematodes – intestinal 8.4±6.1 6.6±7.2 15.4±6.6 11.5±10.2

Nematodes – extraintestinal 6.6±2.6 5.9±4.3 10.4±3.9 25.2±11.7

Contortylenchus diplogaster 1.8±1.4 0.9±1.3 2.9±1.7 8.1±11.1

Parasitylenchus dispar 3.5±2.7 6.3±7.4 0 3.2±4.0

Chytridiopsis typographi 1.8±1.4 0 4.2±2.9 2.5±2.0

Gregarina typographi 0 0 1.4±2.0 0.1±0.1

ItEPV 24.8±6.5 24.3±7.3 3.9±2.4 15.5±22.8

Mattesia schwenkei 19.6±5.0 35.6±10.4 24.9±3.8 50.1±8.7

Tomicobia seitneri 2.2±3.1 8.4±6.8 10.0±5.9 9.8±2.3

Endoparasitoids larvae 23.6±4.9 19.7±18.1 20.1±9.9 17.5±10.2

Long Short Long Short Long Short

Lasting of outbreaks

-200

0

200

400

600

800

1000

De

nsity p

er

m2

Population Emerged adults Parasitism

Figure 1 Population density, numbers of emerged beetles and parasitism in small-scale, short-term

outbreaks versus long-term, large-scale outbreaks (Box plots show median plus upper and lower

quartiles for all samples. Minimum and maximum values are shown by the upper and lower whiskers

(1.5 × interquartile range)).

long short long short long short long short

Lasting of outbreaks

-10

0

10

20

30

40

50

60

70

Infe

ctio

n le

ve

l (%

)

Endoparasitoids Tomicobia

seitneri

Mattesia

schwenkeiItEPV

Figure 2 Infection levels of mature Ips typographus beetles sampled in small-scale, short-term

outbreaks versus long-term, large-scale outbreaks (Box plots show median plus upper and lower

quartiles for all samples. Minimum and maximum values are shown by the upper and lower whiskers

(1.5 × interquartile range).

No statistically significant differences were determined in the numbers of maternal beetles

infected by intestinal nematodes (z = 0.84, p > 0.10), extra-intestinal nematodes (z = 1.69, p >

0.05), eggs of nematodes (z = 1.18, p > 0.10), P. dispar (z = 1.52, p > 0.10) or C. diplogaster

(z = 0.31, p > 0.10) in plots with short-term outbreak versus long-term outbreak areas.

Discussion

At all the studied plots, there exist I. typographus at high population densities. The numbers

of maternal galleries in the sections ranged between 300 and 400 per m2. This conforms to

published data about the large number of maternal galleries in standing trees (Komonen et al.,

2010).

The low number of eggs per female (from 22.5 ± 8.4 to 27.0 ± 13.7) (compare with e.g.

Pfeffer, 1952; Martínek, 1961; Zumr, 1985) at the studied plots can be explained by

intraspecific competition (Anderbrant, 1990; Weslien, 1994; Skuhravý, 2002). Delayed

density dependence occurs, as beetles produced in lower numbers at high gallery densities

also tend to produce fewer offspring themselves. This suggests that density may affect

reproduction in both the current and next generations (Anderbrant et al., 1985; de Jong &

Grijpma, 1986; de Jong & Sabelis, 1988; Sallé et al., 2005) through maternal effects. While

maternal effects may have consequences for population dynamics (Ginzburg & Taneyhill,

1994), this is difficult to quantify from field data (Berryman, 2002). Delayed density

dependence also occurs on very long time scales, as it takes at least 30–50 years for killed

trees to be replaced by mature spruce. This period may be even considerably longer in

systems where natural forest succession stages delay the reestablishment of spruce (Kausrud

et al., 2012).

When population densities are high, the competition among larvae naturally increases –

thus decreasing their chance for survival. Fewer offspring then accrue to any individual

female (Anderbrant, 1990). Although the larvae seek to avoid one another in the galleries

(Mart et al., 1986), cannibalism has been observed in cases of an accidental crossing of their

corridors (Doležal & Sehnal, 2007). This resulted in low population growth rate that was <1

for emerging daughters per maternal beetle (total offspring/2) at all study plots, and it

accorded with known data with reference to similar population density (Anderbrant et al.,

1985; Anderbrant & Schlyter, 1989). Therefore, competition resulting from high population

densities can be regarded as the main factor influencing mortality and fertility (Mart et al.,

1986; Anderbrant 1988, 1990; Wermelinger, 2004; Faccoli & Bernardinelli, 2011).

Lower numbers of eggs on plots with long-term outbreak probably result from delayed and

gradually decreasing fertility, although there was no difference in the densities of maternal

galleries. As the reproductive success is identical, larval mortality is higher. Larval mortality

was caused especially by intraspecific competition, as consumption by parasitoids and

predators was very low and did not exceed 2 % and 10 %, respectively.

The rates of occurrence for all natural enemies are dependent upon the species of the host

tree and even vary by individual species, as the bark texture is especially important (Lawson

et al., 1997). In certain cases, the predators consume up to 90 % of bark beetle larvae. In

particular, larvae of the Medetera flies sometimes surpass in number the larvae of the pest

(Weslien, 1992; Ounap, 2001). In another study, however, the predation rate was always less

than 10 % of the eggs laid (Faccoli & Bernardinelli, 2011). In early stages of the development

cycle for the offspring generation of spruce bark beetles, there is significant mortality due to

predators. For example, the genus Medetera can kill as much as 20 % to 26 % of the offspring

(Hérard & Mercardier, 1996). T. formicarius (Linnaeus, 1758) is able to reduce the offspring

generation of bark beetles by as much as 18 % (Mills, 1985). According to Kausrud et al.

(2012), the question remains open as to whether predation is able also to reduce an outbreak

of bark beetles back to the endemic population level. Even without having to perform long-

term regular studies, it is apparent that, inasmuch as densities are levelled out over 10 years

and mortality caused by parasitoids and predators is less than 10 %, this level of predation did

not cause a collapse of the population.

Small-scale, short-term outbreaks were characterized by fewer parasitoids and lower

percentage of parasitism in comparison with long-term, large-scale outbreaks (10 % and 15 %

vs. 50 % and 43 %, respectively) even though the population densities of maternal galleries

and the production were the same. The parasitism values are within the realm of known data,

as parasitism rates most often vary in a range of 5–55 % (Mills, 1986; Eck, 1990;

Wermelinger, 2002; Feicht, 2004), but these can be even higher (Weslien, 1992; Markovic &

Stojanovic, 2003).

This does not prove any dependence upon density. Rather, the explanation consists in lag

time, and specifically delay among the parasitoids, as the small-scale, short-term outbreaks

occurred in the middle of healthy forest. There are no studies of dispersal distances among

bark beetle parasitoids and predatory flies of the genus Medetera. Considering the expansive

dispersal capacity of I. typographus, however, the dispersal capacity of both parasitoids and

predatory flies could be assumed to be less (Schroeder, 2007). No significant differences in

predator abundances were determined. In cases of outbreak, their own paces of reproduction

lag behind that of bark beetles, and therefore they cannot affect the onset of gradation (see e.g.

Turchin et al., 1999; Wermelinger, 2002). The explanation consists in the fact that the

predators exhibit a type II functional response. The influence of the predator decreases with

the increasing density of the prey (Aukema & Raffa, 2004).

It is evident that parasitoids need not have any response to density, although the

ectoparasitoids showed a density-dependent response only above a certain host density

(Beaver, 1966, 1967) or, on the contrary, larval parasitism tended to show an inversely

density-dependent response (Lozano et al., 1993, 1994, 1996a, 1996b). Delayed density

dependency was shown by Turchin et al. (1999), which corresponds with our findings.

Turchin et al. (1999) suggest that antagonists could be more important during the declining

phase of an outbreak than at the beginning.

Mills (1986) and Mills & Schlup (1989) produced basic partial life tables for I.

typographus in Switzerland and Germany. They suggested that clerid predators Thanasimus

spp. and larval ectoparasitoids had a significant influence on brood survival. This can mean

just about anything. Predators showed a density-dependent response at low beetle densities

but became inversely density-dependent at higher densities (Beaver, 1966, 1967). Our data

confirm this fact as there is no difference in predator abundances between small-scale, short-

term outbreaks and long-term, large-scale outbreaks. Distances of study plots should not be a

reason of low population density of Thanasimus. No dispersal studies have been conducted

with the two predatory beetles of the genus Thanasimus occurring in Europe, but a mark–

recapture study demonstrated a greater long-distance dispersal for a North American

Thanasimus species than for its bark beetle prey (Cronin et al., 2000).

The pathogen species found in this study have often been reported in earlier investigations

on I. typographus associates. C. typographi, ItEPV and eugregarine G. typographi (Fuchs,

1915) are the pathogens detected at the largest number of sites and their infection rates can be

notably large (Weiser et al., 2000; Weiser, 2002; Wegensteiner, 2004; Takov et al., 2010).

Infection levels of ItEPV were high at three study plots known from the Šumava (Weiser et

al., 2000; Lukášová et al., 2012). The absence or low infection levels of the eugregarine G.

typographi (Fuchs, 1915) are very surprising, as this is one of the most common pathogens

(Wegensteiner, 2004; Takov et al., 2010), and it is also very intensively transferred in the

nuptial chambers (Lukášová and Holuša, 2011). The situation had been similar, though, also

in the preceding season (Lukášová et al. 2012).

A higher level of infection was displayed by the neogregarine M. schwenkei (see also

Lukášová et al. 2012). This data about the level of infections can be overstated, however, as it

concerns beetles which remained in the galleries and never left them while M. schwenkei

infection occurring in the fat body in the form of scaphoid spores can, in theory, influence the

beetles’ tendency to emerge. It is presumed that only the newly infected individuals leave the

galleries and, therefore, that the pathogen occurs at higher rates towards the end of the

vegetation season (Weiser, 2002). The levels were significantly higher on long-term outbreak

study plots. This is confirmed by the opinions of Wegensteiner and Weiser (1996b) and by

Holuša et al. (2009) that levels of infection by pathogen species are influenced by beetle

population density. If densities are low, the beetles do not encounter individuals from other

galleries. Pathogen spores are only transferred among beetles within a gallery system, and so

infection of other beetles by faeces and the remains of dead bodies are almost excluded when

galleries do not intercept (Wegensteiner & Weiser 1996b). This situation is typical for

locations with managed forests. In unmanaged forests, bark beetles can become more

abundant and concentrated, resulting in a greater probability of pathogen transmission and

therefore higher levels of infection (Holuša et al., 2009). Even here, however, a marked delay

in ItEPV development behind the densities of I. typographus is apparent at the Ztracený

locality.

Parasitism of maternal beetles by entomophagous nematodes was greater than expected.

For example, Tenkáčová & Mituch (1986, 1987, 1991), in their works from various locations

(e.g. Tatra National Park), report the presence of nematodes in bark beetles in the range of

4.3–5.1 % of those individuals examined. The higher figures recorded from Šumava National

Park can be due to the higher density of the spruce bark beetle population there such that the

nematodes probably have easier access to their host. In the case of the monitored species

Contortylenchus diplogaster, the same studies report occurrence in about 9 % of I.

typographus individuals in the spring generation and just less than 1 % in the summer

generation. The measured values of bark beetle parasitism by this nematode species conform

to the findings of these studies, therefore, as the Šumava population of the spruce bark beetle

is univoltine.

T. seitneri is a common endoparasite in the adults (Eck, 1990), but the rate of parasitization

is at a low 0–9.5 % (Feicht, 2004). The data in this instance fall entirely within the expected

range, even though it concerns only larvae of the first instar, at which stage the species

affiliation is clear. Total parasitization (some endoparasitoid larvae cannot be identified

precisely) reached 30 %, which corresponds with a range of 20–50 % reported earlier

(Faccoli, 2000).

In summary, a number of parasitoids and entomopathogens respond numerically to bark

beetle density. Even though the great majority of mortality was caused by larval competition,

in view of the identical reproductive success, we cannot consider this to constitute feedback.

The stochastic distribution of storm-disturbed stands may offer a temporary decrease in

relative predation pressure, at least under some circumstances (Reeve, 1997; Wermelinger,

2002, 2004; Schroeder, 2007). Predation and/or parasitism did not play a significant role in

reducing the outbreak population.

Acknowledgments

The research was supported by project NAZV QH81136 of the Ministry of Agriculture of the

Czech Republic.

References

Anderbrant. O. (1988) Survival of parent and brood adult bark beetles, Ips typographus, in relation to

size, lipid content and re-emergence or emergence day. Physiological Entomology, 13, 121–129.

Anderbrant, O. (1990) Gallery construction and oviposition of the bark beetle Ips typographus

(Coleoptera: Scolytidae) at different breeding densities. Ecological Entomology, 15, 1–8.

Anderbrant, O. & Schlyter, F. (1989) Causes and effects of individual quality in bark beetles.

Ecography, 12, 488–493.

Anderbrant, O., Schlyter, F. & Birgersson, G. (1985) Intraspecific competition affecting parents and

offspring in the bark beetle Ips typographus. Oikos, 45, 89–98.

Annila, E. (1971) Sex ratio in Ips typographus L (Col, Scolytidae). Annales Entomologici Fennici, 37,

7–14.

Aukema, B.H. & Raffa, K.F. (2004) Does aggregation benefit bark beetles by diluting predation?

Links between a group-colonisation strategy and the absence of emergent multiple predator

effects. Ecological Entomology, 29, 129–138.

Beaver, R.A. (1966) Development and expressions of population tables for bark bettle Scolytus

scolytus (F.). Journal of Animal Ecology, 35, 27–41.

Beaver, R.A. (1967) Regulation of population density in bark beetle Scolytus scolytus (F). Journal Of

Animal Ecology, 36, 435–451.

Berryman, A. (2002) Population: a central concept for ecology? Oikos, 9, 439–442.

Bombosch, S. (1954) Zur Epidemiologie des Buchdruckers (Ips fypographus L.). Die grosse

Borkenkäferkalamität in Südwestdeutschland 1944-1951. (ed. by G. Wellenstein), pp. 239–283.

Forstschutzstelle Sudwest, Ringingen, Germany.

Christiansen, E. & Bakke, A. (1988) The spruce bark beetle of Eurasia. Dynamics of forest insect

populations. (ed. by A. Berryman), pp. 480–503. Plenum Publishing Corporation, UK.

Christiansen, E., Waring, R.H. & Berryman, A.A. (1987) Resistance of conifers to bark beetle attack:

searching for general relationship. Forest Ecology and Management, 22, 89–106.

Culek, M. (ed.) (1996) Biogeographical classification of the Czech Republic. Enigma, Prague, Czech

Republic, 347 pp.

de Jong, M.C.M. & Gripjpma, P. (1986) Competition between larvae of Ips typographus. Entomologia

Experimentalis et Applicata, 41, 121–133.

de Jong, M.C.M. & Sabelis, M.W. (1988) How bark beetles avoid interference with squatters: an ESS

for colonization by Ips typographus. Oikos, 51, 88–96.

Dippel, C, Heidger, C, Nicolai, V. & Simon, M. (1997). The influence of four different predators on

bark beetles in European forest ecosystems (Coleoptera: Scolytidae). Entomologia Generalis, 21,

161–75.

Doležal, P. & Sehnal, F. (2007) Effects of photoperiod and temperature on the development and

diapause of the bark beetle Ips typographus. Journal of Applied Entomology, 131, 165–173.

Eck, R. (1990) Die parasitischen Hymenopteran des Ips typographus in der Phase der Progradation.

Entomologische Abhandlungen, 53, 152–178.Faccoli, M. (2000) Notes on the biology and ecology

of Tomicobia seitneri (Ruschka) (Hymenoptera: Pteromalidae), a parasitoid of Ips typographus

(L.) (Coleoptera: Scolytidae). Frustula Entomologova, 23, 47–55.

Faccoli, M. (2001) Tomicobia seitneri (Ruschka), Ropalophorus clavicornis (Wesmael) and Coeioides

bostrychorum Giraud: three hymenopterous parasitoids of Ips typographus (L.) (Col., Scolytidae)

new to Italy. Bollettino della Societa Entomologica Italiana, 133, 237–46.

Faccoli, M. & Bernardinelli, I. (2011) Breeding performance of the second generation in some

bivoltine populations of Ips typographus (Coleoptera Curculionidae) in the south-eastern Alps.

Journal of Pest Science, 84, 15–23.

Fayta, P., Machmer, M.M. & Steeger, C. (2005) Regulation of spruce bark beetles by woodpeckers—a

literature review. Forest Ecology and Management, 206, 1–14.

Feicht, E. (2004) Parasitoids of Ips typographus (Col., Scolytidae), their frequency and composition in

uncontrolled and controlled infested spruce forest in Bavaria. Journal of Pest Science, 77, 165–

172.

Feicht, E. (2006) Frequency, species composition and efficiency of Ips typographus (Col., Scolytidae)

parasitoids in infested spruce forests in the national Park “Bavarian Forest” over three consecutive

years. Journal of Pest Science, 79, 35–39.

Forsse, E. (1987) Flight duration in Ips typographus L.: Insensitivity to nematode infection. Journal of

Applied Entomology, 104, 326–328.

Gauß, R. (1954) Der Ameisenbuntkäfer Thanasimus (Clerus) formicarius Latr. als Borkenkä ferfeind.

Die grosse Borkenkäferkalamität in Südwestdeutschland 1944-1951. (ed. by G. Wellenstein), pp.

417–429. Forstschutzstelle Südwest, Ringingen, Germany.

Gilbert, M. & Grégoire, J.-C. (2003) Site condition and predation influence a bark beetle’s success: a

spatially realistic approach. Agricultural and Forest Entomology, 5, 87–96.

Ginzburg, L.R. & Taneyhill, D.E. (1994) Population cycles of forest Lepidoptera—a maternal effect

hypothesis. Journal of Animal Ecology, 63, 79–92.

Grégoire, J.C. & Evans, H.F. (2004) Damage and control of BAWBILT organisms–an overview. Bark

and wood boring insects in living trees in Europe, a synthesis. (eds. by F. Lieutier, K.R. Day,A.

Battisti, J.-C. Grégoire & H.F. Evans ), pp. 19–37. Kluwer Academic Publishers, Dordrecht, the

Netherlands.

Hedgren, P.O. (2004) The bark beetle Pityogenes chalcographus (L.) (Scolytidae) in living trees:

reproductive success, tree mortality and interaction with Ips typographus. Journal of Applied

Entomology, 128, 161–166.

Hedgren, P.O. (2007) Nordamerikas största barkborreutbrott pågår i Kanadas tallskogar. Entomologisk

Tidskrift, 128, 1–8.

Heidger, C.M. (1994) Die Ökologie und Bionomie der Borkenkäfer-Antagonisten Thanasimus

formicarius (Cleridae) und Scoposcelis pulchella Zett (Anthocoridae): Daten zur Beurteilung ihrer

prädatorischen Kapazität und der Effekte beim Fang in Phermonfallen. Dissertation Philipps-

Universität Marburg, 330 pp.

Hérard, F. & Mercadier, G. (1996) Natural enemies of Tomicus piniperda and Ips acuminatus (Col.,

Scolytidae) on Pinus sylvestris near Orléans, France: temporal occurrence and relative abundance,

and notes on eight predatory species. Entomophaga, 41, 183–210.

Hilszczanski, J., Gibb, H. & Bystrowski, C. (2007) Insect natural enemies of Ips typographus (L.)

(Coleoptera, Scolytinae) in managed and unmanaged stands of mixed lowland forest in Poland.

Journal of Pest Science, 80, 99–107.

Holuša, J., Weiser, J. & Žižka, Z. (2009) Pathogens of the spruce bark beetles Ips typographus and Ips

duplicatus. Central European Journal of Biology, 4, 567–573.

Hopping, G.R. (1947) Notes on the seasonal development of Medetera aldrichü Wheeler (Díptera,

Dolichopodidae) as a predator of the Douglas fir bark- beetle, Dendroctonus pseudotsugae

Hopkins. Canadian Entomologist, 79, 150–153.

Hulcr, J., Ubik, K. & Vrkoc, J. (2006) The role of semiochemicals in tritrophic interactions between

the spruce bark beetle Ips typographus, its predators and infested spruce. Journal of Applied

Entomology, 130, 275–283.

Johansson, T., Gibb, H., Hjältén, J., Pettersson, R.B., Hilszczanski, J., Alinvi, O., Ball, J.P. & Danell,

K. (2007) The effects of substratemanipulations and forest management on predators of saproxylic

beetles. Forest Ecology and Management, 242, 518–529.

Kausrud, K., Okland, B., Skarpaas, O., Grégoire, J.C., Erbilgin, N. & Stenseth, N.C. (2012) Population

dynamics in changing environments: the case of an eruptive forest pest species. Biological

Reviews, 87, 34–51.

Kaya, H.K. (1984) Nematode parasites of bark beetles. Plant and Insect Nematodes. (ed. by W.R.

Nickle), pp. 727–754. Marcel Dekker, Inc., New York.

Kenis, M., Wermelinger, B. & Grégoire, J.-C. (2004) Research on parasitoids and predators of

Scolytidae - a review. Bark and wood boring insects in living trees in Europe, a synthesis. (eds. by

F. Lieutier, K.R. Day,A. Battisti, J.-C. Grégoire & H.F. Evans), pp. 237–290. Kluwer Academic

Publishers, Dordrecht, the Netherlands.

Komonen, A., Schroeder, L.M. & Weslien, J. (2010) Ips typographus population development after a

severe storm in a nature reserve in southern Sweden. Journal of Applied Entomology, 135, 132–

141.

Lawson, S.A., Furuta, K. & Katagiri, K. (1997) Effect of natural enemy exclusion of Ips typographus

japonicus Niijima (Col., Scolytidae). Journal of Applied Entomology, 121, 89–98.

Lieutier, F. (1981) Influence des nématodes parasites sur l´essaimage du scolytide Ips sexdentatus

(Boern.). Action régulatrice du froid. Acta Oecologica, Oecologia Applicata, 2, 357–368.

Lozano, C. Campos, M., Kidd, N.A.C. & Jervis, M.A. (1994) The role of parasitism and intra-specific

competition in the population dynamics of the baik beetle Leperisinus varius (Fabr.) (Col..

Scolytidae) on European olives (Olea europaea). Journal of Applied Entomology, 117, 182–189.

Lozano, C., Campos, M., Kidd, N.A.C. & Jervis, M.A. (1996a) The role of parasitism in the

population dynamics of the bark beetle Phloeotribus scarabaeoides (Col, Scolytidae) on European

olives (Olea europaea). Journal of Applied Entomology, 120, 347–351.

Lozano, C., Kidd, N.A.C. & Campos, M. (1993) Studies on the population-dynamics of the bark beetle

Leperisinus varius (Fabr.) (Col, Scolytidae) on European olives (Olea europaea). Journal of

Applied Entomology, 16, 118–126.

Lozano, C., Kidd, N.A.C. & Campos, M. (1996b) The population dynamics of the bark beetle

Leperisinus varius (Fabr.) (Col, Scolytidae) on European olive (Olea europaea). Journal of

Applied Entomology, 116, 118–26.

Lukášová, K. & Holuša, J. (2011) Gregarina typographi (Eugregarinorida: Gregarinidae) in the bark

beetle Ips typographus (Coleoptera: Curculionidae): changes in infection level in the breeding

system. Acta Protozoologica 50, 311–318.

Lukášová, K. & Holuša, J. (2012) Patogeny lýkožroutů rodu Ips (Coleoptera: Curculionidae:

Scolytinae): review. [Pathogens of bark beetles of the genus Ips (Coleoptera: Curculionidae:

Scolytinae): review]. Zprávy lesnického výzkumu, 57, 160–164.

Lukášová, K., Holuša, J. & Grucmanová, Š. (2012) Reproductive performance and natural antagonists

of univoltine population of Ips typographus (Coleoptera, Curculionidae, Scolytinae) at epidemic

level: a study from Šumava Mountains, Central Europe. Beskydy, 5, 1–10.

Mánek, J. & Ešnerová, J. (2007) Studium genetické variability a ověřování původnosti smrkových

populací v Národním parku Šumava jako podklad pro záchranná managementová opatření.

Aktuality šumavského výzkumu III. (eds. by L. Dvořák, P. Šustr & V. Braun), pp. 87–89. Sborník z

konference Srní 4-5 October 2007. Správa Národního parku a Chráněné krajinné oblasti Šumava,

Vimperk, Czech Republic.

Markovic, C. & Stojanovic, A. (2003) Significance of parasitoids in the reduction of oak bark beetle

Scolytus intricanus Ratzeburg (Col., Scolytidae) in Serbia. Journal of Applied Entomology, 127,

23–28.

Mart, C.M., De Jong, & Grijpma, P. (1986) Competition between larvae of Ips typographus.

Entomologia Experimentalis et Applicata, 41, 121–133.

Martínek, V. (1961) Problém natality a gradace kůrovce Ips typographus L. ve střední Evropě.

Rozpravy Československé Akademie Věd, Řada MPV, 71, 1–78.

Mendel, Z. (1987) Major pests of man-made forests in Israel: Origin, biology, damage and control.

Phytoparasitica, 15, 131–37.

Mendel, Z., Podoler, H. & Livne, H. (1990) Interactions between Aulonium ruficorne (Coleoptera:

Colydiidae) and other natural enemies of bark beetles (Coleoptera: Scolytidae). Enthomophaga,

35, 99–105.

Mills, N.J. (1985) Some observations on the role of predation in the natural regulation of Ips

typographus populations. Zeitschrift für Angewandte Entomologie, 99, 209–15.

Mills, N.J. (1986) A preliminaiy analysis ofthe dynamics of within tree populations lps typographus

(L.) (Coleoptera: Scolytidae). Zeitschrift für Angewandte Entomologie, 102, 402–16.

Mills, N.J. & Schlup, J. (1989) The natural enemies of Ips typographus in Central Europe: Impact and

potential use in biological control. Potential for Biological Control of Dendroctonus and Ips Bark

Beetles. (eds. by D. L. Kulhavy & M. C. Miller), pp. 131–146 Stephen F. Austin State University

Press, Nacogdoches.

Mulock, P. & Christiansen, E. (1986) The threshold of successful attack by Ips typographus on Picea

abies: a field experiment. Forest Ecology and Management, 14, 125–132.

Nickle, W.R. (1963) Observations on the effect of nematodes on Ips confusus (LeConte) and other

bark beetles. Journal of Insect Pathology, 5, 386–389.

Nuorteva, M. (1959) Untersuchungen über einige in den Frassbildern der Borkenkäfer lebende

Medetera-Arten (Dipt, Dolichopodidae). Suomen Hyönteistieteellinen Aikakauskirja, 25, 192-210.

Nuorteva, M., & Saari, L. 1980. Larvae of Acanthocinus, Pissodes and Tomicus (Coleoptera) and

the foraging behaviour of woodpeckers (Picidae). Annales Entomologici Fennici, 46, 107–10.

Økland, B. & Berryman, A. (2004) Resource dynamic plays a key role in regional fluctuations of the

spruce bark beetles Ips typographus. Agricultural and Forest Entomology, 6, 141–146.

Økland, B. & Bjørnstad, O.N. (2006) A resource-depletion model of forest insect outbreaks. Ecology,

87, 283–290.

Ounap, H. (2001) Insect predators and parasitoids of bark beetles (Col., Scolytidae) in Estonia, PhD

Thesis. Institute of Plant Protection, Faculty of Agronomy, Estonian Agricultural University,

Estonia.

Pfeffer, A. (1952) Kůrovec lýkožrout smrkový a boj proti němu. Nakladatelství brázda, Prague, Czech

Republic, 45 pp.

Raffa, K.F., Aukema, B.H., Bentz, B.J., Carroll, A.L, Hicke, J.A., Turner, M.G. & Romme, W.H.

(2008) Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the

dynamics of bark beetle eruptions. Bioscience, 58, 501–517.

Reeve, J.D. (1997) Predation and bark beetle dynamics. Oecologia, 112, 48–54.

Ryall, K.L. & Fahrig, L. (2005) Habitat loss decreases predator/prey ratios in a pine-bark beetle

system. Oikos, 110, 265–270.

Sachtleben, H. (1952) Die parasitischen Hymenopteren des Fichtenborkenkäfers Ips typographies L.

Beitrage zur Entomologie, 2, 137–89.

Sallé, A., Baylac, M. & Lieutier, F. (2005) Size and shape changes of Ips typographus L. (Coleoptera:

Scolytinae) in relation to population level. Agricultural and Forest Entomology, 7, 297–306.

Schelhaas, M.J., Nabuurs, G.J. & Schuck, A. (2003) Natural disturbances in the European forests in

the 19th and 20th centuries. Global Change Biology, 9, 1620–1633.

Schimitschek, E. (1931) Der achtzähnige Larchenborkenkäfer Ips cembrae Heer. Zeitschrift für

Angewandte Entomologie, 17, 253–344.

Schroeder, L.M. (2007) Escape in space from enemies: a comparison between stands with and without

enhanced densities of the spruce bark beetle. Agricultural and Forest Entomology, 9, 85–91.

Skuhravý, V. (2002) Lýkožrout smrkový (Ips typographus L.) a jeho kalamity [Der Buchdrucker und

ihre seine Kalamitäten]. Agrospoj, Prague, Czech Republic, 196 pp.

Svoboda, M. (2007) Efekt disturbance a hospodářských zásahů na stav lesního ekosystému –

případová studie z oblasti tzv. Kalamitní svážnice na Trojmezné. Aktuality šumavského výzkumu

III. (eds. by L. Dvořák, P. Šustr & V. Braun), pp. 109–114. Sborník z konference Srní 4-5 October

2007. Správa Národního parku a Chráněné krajinné oblasti Šumava, Vimperk, Czech Republic.

Takov, D., Pilarska, D. & Wegensteiner, R. (2010) List of protozoan and microsporidian pathogens of

economically important bark beetle species (Coleoptera: Curculionidae: Scolytinae) in Europe.

Acta Zoologica Bulgarica, 62, 201–209.

Tenkáčová, I. & Mituch, J. (1986) Prispevok k poznaniu nematofauny chrobákov čeladě Scolytidae na

smreku obyčajném v Košickém lesnom parku. Lesnický časopis, 32, 381–387.

Tenkáčová, I. & Mituch, J. (1987) Nematodes new for the fauna of the Czechoslovak Socialist

Republic with the affinity to scolytids (Coleoptera: Scolytidae). Helmintologia, 24, 281–291.

Tenkáčová, I. & Mituch, J. (1991) Nematoda podkornikovitých (Coleoptera: Scolytidae) z Vysokých

Tatier. Zborník prác o Tatranskom národnom parku, 31, 173–182.

Thong, C.H.S. & Webster, J.M. (1975) Effects of the bark beetles nematode, Contortylenchus reversus

on gallery construction, fecundity and egg viability of the douglas fir beetle Dendroctonus

pseudotsugae (Coleoptera: Scolytidae). Journal of Invertebrate Pathology, 26, 235–238.

Turchin, P., Taylor, A.D. & Reeve, J.D. (1999) Dynamical Role of predators in population cycles of a

forest insect: an experimental test. Science, 285, 1068–1071.

Warzee, N., Gilbert, M. & Grégoire, J.-C. (2006) Predator/prey ratios: a measure of bark-beetle

population status influenced by stand composition in different French stands after the 1999 storms.

Annalls of Forest Science, 63, 301–308.

Wegensteiner, R. (2004) Pathogens in bark beetles. Bark and wood boring insects in living trees in

Europe, a synthesis. (eds. by F. Lieutier, K.R. Day,A. Battisti, J.-C. Grégoire & H.F. Evans), pp.

291–313. Kluwer Academic Publishers, Dordrecht, the Netherlands.

Wegensteiner, R. & Weiser, J. (1996a) Occurrence of Chytridiopsis typographi (Microspora,

Chytridiopsida) in Ips typographus L. (Col., Scolytidae) field population and in a laboratory stock.

Journal of Applied Entomology, 120, 595–602.

Wegensteiner, R. & Weiser, J. (1996b) Untersuchungen zum Auftreten von Pathogen by Ips

typographus (Coleoptera: Scolytidae) aus einem Naturschutzgebiet in Schwartzwald (Baden-

Württemberg). Anzeiger für Schädlingskunde, Pflanzenschutz, Umweltschutz, 69, 162–167.

Weiser, J. (2002) Patogenní organismy. Lýkožrout smrkový (Ips typographus L.) a jeho kalamity. Der

Buchdrucker und seine Kalamitäten. (ed. by. V. Skuhravý), pp. 97-100. Agrospoj, Prague.

Weiser, J., Pultar, O. & Žižka, Z. (2000) Biological protection of forest against bark beetle outbreaks

with poxvirus and other pathogens. IUAPPA, Section B, 168–172.

Wermelinger, B. (2002) Development and distribution of predators and parasitoids during two

consecutive years of an Ips typographus (Col., Scolytidae) infestation. Journal of Applied

Entomology, 126, 521–527.

Wermelinger, B. (2004) Ecology and management of the spruce bark beetle Ips typographus – a

review of recent research. Forest Ecology and Management, 202, 67–82.Weslien, J. (1992) The

arthropod complex associated with Ips typographus (L.) (Coleoptera, Scolytidae): species

composition, phenology, and impact on bark beetle productivity. Entomologica Fennica, 3, 205–

213.

Weslien, J. (1994) Interactions within and between species at different densities of the bark beetle Ips

typographus and its predator Thanasimus formicarius. Entomologia Experimentalis et Applicata,

71, 133–143.

Weslien, J. & Schroeder, L.M. (1999) Population levels of bark beetles and insects in managed and

unmanaged spruce stands. Forest Ecology and Management, 111, 267–275.

Wichmann, H.E. (1957) Untersuchungen an Ips typographus L. und seiner Umwelt - Die

Kamelhalsfliegen. Zeitschrift für Angewandte Entomologie, 40, 433–440.

Zumr, V. (1985) Biologie a ekologie lýkožrouta smrkového (Ips typographus) a ochrana proti němu.

[Biology and ecology of eight-toothed spruce bark beetle (Ips typographus L.), and forest

protection measures]. Academia, Prague, 124 pp.