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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.
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