Outbreaking herbivore escapes parasitoid by attaining

only a small body size

JOHAN A. STENBERG
Swedish University of Agricultural Sciences, Department of Plant Protection Biology, P.O. Box 102, SE-23053 Alnarp, Sweden
Citation: Stenberg, J. A. 2015. Outbreaking herbivore escapes parasitoid by attaining only a small body size. Ecosphere
6(2):21. http://dx.doi.org/10.1890/ES14-00378.1

Abstract. The reason why parasitoids are often unable to control insect herbivores during outbreak
years has remained unclear to modern ecologists. Here I show that the blue willow beetle (Phratora
vulgatissima) can escape parasitoids (Perilitus brevicollis) by reaching only a small body size during the
increased competition which coincides with outbreaks. Different phases of outbreaks were simulated by
allowing leaf-beetle larvae to develop at different densities on willow. The denser the herbivore
populations, the smaller body sizes they attained. In the field too, herbivore body size decreased when the
level of defoliation increased. The parasitoids were clearly limited by herbivore body size, exhibiting
reduced survival in parallel with decreasing herbivore size, with none of them surviving in beetles from
larvae reared at the highest density. The results demonstrate how bottom-up control of the herbivore
becomes more important as outbreaks intensify, while top-down control gradually becomes less important
and collapses during the outbreak peak. Because the mechanism limiting P. brevicollis parasitoids involves
herbivore body size, which is reduced at high densities, I anticipate that these parasitoids are unable to
terminate herbivore outbreaks.
Key words: biocontrol; conservation biological control; herbivory; integrated pest management; IPM; Perilitus
brevicollis; Phratora vulgatissima; population cycles; population dynamics; Salix cinerea; Salix viminalis; trophic interaction.
Received 10 October 2014; revised 2 December 2014; accepted 5 December 2014; final version received 1 January 2015;
published 10 February 2015. Corresponding Editor: D. P. C. Peters.
Copyright: 2015 Stenberg. This is an open-access article distributed under the terms of the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited. http://creativecommons.org/licenses/by/3.0/
E-mail: johan.stenberg@slu.se

INTRODUCTION

suggest that some parasitoid populations become

marginalized during herbivore outbreaks, and
contribute little to arresting herbivore population
growth during these critical events (Parry et al.
2003, Schott et al. 2010). Thus, parasitoids are
often not significant factors in terminating
herbivore outbreaks (Satake et al. 2004, Hagen
et al. 2010). In fact, parasitism often does not
increase until later when the outbreak has
already peaked and the situation is stabilizing
(Bylund 1995, Tanhuanpaa et al. 2002, Turchin et
al. 2003). Consequently, the release of parasitoids
in agroecosystems is often only recommended as
long as the target herbivore has not reached
critical densities. The absence of positive density-

Parasitoids are used as biocontrol agents

against pest insects in many forest and agroecosystems. This practice builds on the idea that
parasitoids are important natural enemies of
herbivores, and really can exert top-down control
over herbivore populations (Hassell and Waage
1984, Murdoch et al. 1995, Stenberg et al. 2007).
Nevertheless, although this approach to control
normally works well (Murdoch et al. 1995), there
are sometimes outbreaks of herbivores with
devastating effects on their host plants (Bylund
1995). Long-term field data on the population
dynamics of parasitoids and herbivores actually
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dependent parasitism, and the presence of

inverse density-dependence, seems to be especially apparent in coleopteran herbivores (Stiling
1987, Rand 2013). Bottom-up factors, like resource limitation or induced plant defenses, are
increasingly considered to be more significant
than parasitoids for arresting population growth
and reducing herbivore numbers when these
have reached outbreak levels (Kapari et al. 2006).
In cropping systems, this means that outbreaks
are brought to an end only at the cost of reduced
yield or the use of insecticides.
Plant-herbivore-parasitoid dynamics have
been surprisingly resistant to explanation, and
the literature provides no definitive conclusion as
to which mechanism is most significant. Hyperparasitoids and intraguild predation are factors
that, in some systems, can restrict the effectiveness of parasitoids especially in agricultural
landscapes with low structural complexity
(Mackauer and Volkl 1993, Sullivan and Volkl
1999, Jonsson et al. 2012, Poelman et al. 2013). For
example, in a well-studied system based on
Brassica plants, Poelman, Harvey, and colleagues
have shown that field hyperparasitism rates of a
common primary parasitoid (Cotesia glomerata)
can reach 90% (e.g., Poelman et al. 2013).
Previous studies also have tested whether bottom-up food limitation of herbivores affects
parasitoids by weakening herbivore immune
responses (Myers et al. 2011). Little evidence,
however, has been found for this hypothesis.
Finally, several studies have tested whether plant
quality, including induced plant defenses which
increase with increasing herbivore density, have
negative effects on parasitoids (Haukioja 2005,
Soler et al. 2005, Kapari et al. 2006, Stenberg
2012). Here I introduce a new hypothesis, namely
that insect herbivores attain smaller sizes during
outbreaks than otherwise, and that parasitoids,
which are restricted to the limited resources
within their herbivore hosts (Harvey et al. 1995,
Harvey et al. 2005, Pennacchio and Strand 2006,
Stenberg and Hamback 2010, Stenberg 2012), fail
to develop when their hosts are small. I test the
hypothesis in a system based on willows (Salix),
which is widely used as a bioenergy crop in
European short rotation coppices. Outbreaks of
the detrimental Blue willow beetle (Phratora
vulgatissima) are often reported to occur both in
coppices and in natural populations (Dalin et al.
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2009). Both natural enemies and intraspecific

competition play important roles in the population growth of the herbivore (Bjorkman et al.
2003), but it is still unclear how important these
two factors are during the different phases of
herbivore outbreaks. The beetle is gregarious,
often reaching high densities on individual host
plants, which during outbreaks are completely
defoliated, while neighboring host plants are
ignored and remain intact ( personal observation).
One of the most important natural enemies of the
beetle is the braconid solitary parasitoid Perilitus
brevicollis (Baffoe et al. 2012, Stenberg 2012),
which in turn is not known to host hyperparasitoids. In order to test the hypothesis, I
measured beetle body size in 16 different wild
populations with varying levels of outbreak
intensity. I also reared beetle larvae in a
controlled laboratory environment at eight different density classes (from no competition,
representing normal years, to very high competition, representing outbreak peaks), and parasitized the emerging adults individually. Both field
and laboratory studies showed that the beetles
attain a smaller body size in parallel with the
decreasing food availability during outbreaks.
The parasitoids, which are not able to utilize
small beetles (Stenberg 2012), showed decreasing
survival in parallel with increasing beetle density,
and the population collapsed at the highest
density classes. These results suggest that the
herbivore is able to escape parasitoids when
outbreaks intensify and provide a mechanistic
explanation as to why parasitoids are sometimes
unable to bring herbivore outbreaks to an end.

METHODS
Study species
Two Salix (Salicaceae) species were used for
this study: S. viminalis L. and S. cinerea L. The
former is fast-growing, but susceptible to Phratora vulgatissima (Stenberg et al. 2010, Lehrman et
al. 2012), and is commonly used in short rotation
willow coppices in Sweden. It was introduced to
Sweden in the 18th century and has become
naturalized. The latter (S. cinerea) is native and is
the most common wild host plant for the Blue
willow beetle, Phratora vulgatissima (L.) (Coleoptera: Chrysomelidae). S. cinerea has, in contrast to
S. viminalis, an induced trichome-based defense
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against the beetle (Dalin and Bjorkman 2003,

Dalin et al. 2004, Bjorkman et al. 2008). The beetle
is restricted to the genus Salix; there are frequent
reports of it completely defoliating coppices, as
well as wild Salix plants.
P. vulgatissima is gregarious and univoltine in
the study area (Dalin 2011). It overwinters as an
adult, and in Uppsala it normally emerges in late
April when it feeds on the leaves of Salix. Even
though the adult beetles can cause substantial
damage to the plants, the greatest defoliation is
caused by the larvae. Egg clutches (normally
consisting of 120 eggs) are laid on Salix leaves in
May, and the emerging larvae defoliate the plants
in May and June. Both larvae and adults feed
gregariously on the leaves. As indicated previously, the defoliation can be very intense during
outbreak years, and in such situations the larvae
experience extreme intraspecific competition
through depletion of resources (Dalin et al.
2009). The body size of the adult beetle is plastic
and is determined by larval development. Small
beetles are fecund (J. A. Stenberg et al., unpublished data), but may potentially suffer from
reduced winter survival (not tested). The larvae
pupate in the ground, and the emerging beetles
feed on Salix leaves for a few weeks before they
move to their overwintering sites outside the
coppices.
Perilitus brevicollis Haliday 1835 (Hymenoptera: Braconidae) is a solitary endoparasitoid that
attacks adult P. vulgatissima beetles. It is imagobiont, meaning that it parasitizes the adult stage
of the beetles. This parasitoid has a wide
geographical distribution, occurring at least from
Spain in the south to Scandinavia in the north. In
Central Europe it has occasionally been reported
to parasitize a few closely related beetle species
in addition to P. vulgatissima, but in Sweden it is
restricted to P. vulgatissima. Two other chrysomelids (Galerucella lineola and Lochmea capreae) of
similar size to P. vulgatissima occur on Salix but
they have never been found parasitized.
The parasitoid overwinters inside the living
adult host, and the parasitoid larva emerges 12
weeks after the beetle starts to feed in the spring.
The emerging parasitoid larva immediately spins
a cocoon in which it pupates. The adult
parasitoid emerges from the cocoon after about
12 weeks and starts to parasitize new beetles. It
is currently not known whether the parasitoid
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can produce two generations per summer in the

study area.
Parasitism levels in the field are typically
around 15 40% in Uppsala during normal
(non-outbreak) conditions, and it occurs in all P.
vulgatissima populations in the study area (pers.
obs.). I only know of one other parasitoid that
attacks P. vulgatissima in the area, namely
Anthomyiopsis nigrisquamata (Diptera: Tachinidae), which is very rare (;1% parasitism).
Hyperparasitism has not been observed in the
study area ( personal observation).
In order to obtain beetles and parasitoids for
this study, I collected overwintering P. vulgatissima beetles from several populations around
Uppsala, Sweden. The overwintering parasitoid
generation is present within adult beetles. The
beetles and the emerging parasitoids were reared
in plastic containers in climate chambers at 198C,
80% RH, with a 16:8 light regime. Salix plants
were reared from winter cuttings in a greenhouse
at 208C, with a 16:8 light regime.

Experimental setup
In order to test for the effect of herbivore larval
crowding on intraspecific competition and parasitoid survival, I established different densities of
neonate herbivore larvae in plastic containers (30
ml, 26 3 67 mm cylinders, perforated lid). Group
sizes of 1, 2, 3, 5, 7, 9, 11, and 15 larvae were used.
Forty replicates (containers) were established for
group sizes 13, and twenty replicates for group
sizes 515. Thus, in total, 1180 herbivore larvae
were reared. Extra replicates were established for
the small group sizes because random mortality
can wipe out such groups completely, and I
wanted adult beetles to emerge from at least
twenty containers per group size. One Salix
viminalis leaf was inserted into each container
every third day, so that small larval groups
would have an abundance of food at all times,
while large groups would quickly consume the
leaf, and suffer starvation. The leaves used were
detached from the middle part of the host plants,
and varied little in size. The larvae were checked
every day and the larval development time,
survival, and pupal weight were measured for
each individual larva when it had reached the
pupal stage. A Mettler Toledo MX5 microbalance
with a precision of 1 lg was used for all weight
measurements. One pupa from each container
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was randomly selected and placed individually

in a plastic container until the adult emerged.
The beetles were parasitized by a randomly
chosen parasitoid as soon as they reach adulthood (sensu Stenberg 2012). They were placed in
individual plastic jars to be parasitized, and were
watched continuously until parasitization took
place to ensure that every beetle really was
parasitized. Parasitized beetles were kept individually in the plastic containers and fed one
Salix leaf every second day to ensure that they
never experienced food shortage during parasitoid development. The reason for giving all
parasitized beetles a surplus of food was to
make sure that any effect on parasitoid survival
was the result of herbivore density during the
beetles larval development (i.e., before parasitization). The parasitized beetles were kept in
climate chambers at 198C, 80% RH, with a 16:8
light regime. All parasitized beetles were examined every day and the parasitoids larval
development time, cocoon survival, as well as
successful parasitism (number of adult parasitoids divided by the number of parasitized
beetles), were calculated for each herbivore larval
density class. Parasitoid cocoon size was not
measured in this experiment, but has previously
been shown to be related to beetle size (Stenberg
2012).

possible as the skeletonized leaves remain on the

plant for the whole summer. All beetle individuals located below a height of 3 m were collected
and weighed using a Mettler Toledo MX5
microbalance with a precision of 1 lg.

Statistical analysis
Controlled laboratory experiment.First, mean
values for the herbivore larval development time
and pupal weight for each individual group
(container) were calculated. These mean values
were used in one-way ANOVAs to evaluate the
importance of herbivore larval density class on
herbivore larval development time and pupal
weight. In addition, linear regression analyses
were performed to evaluate the relationship
between density and larval development time
or pupal weight. The survival rate (number of
herbivore larvae that reached the pupal stage
divided by the original number of beetles in the
container) was also calculated for each individual
group (container) and a linear regression analysis
was performed to evaluate whether the survival
rate was related to density for group sizes 315.
The smallest group sizes (12) were not included
in the latter linear regression because they
obviously fell outside the seemingly linear part
of the range. Finally, the effect of herbivore
density on successful parasitism, cocoon survival, and parasitoid development time was evaluated using linear regression. The analysis of
parasitoid development time was only undertaken for a proportion of the data (n 48) as some
data points were lost. The statistical software
package R 2.14.1 was used when analyzing the
laboratory experiment.
Field study.A generalized additive model
(GAM) (Wood 2011) was used to test whether
the beetles mean body size was reduced with
increased defoliation. The R package mgcv 1.7
27 in R 3.0.2 was used for the GAM analysis.

Field observations of body sizes

during outbreaks
A field survey was undertaken during the last
week in July, 2013 in order to investigate P.
vulgatissima body sizes on plants in different
outbreak phases in the wild. The timing of the
survey was chosen to coincide with adult beetle
emergence after pupation in the field. The young
adult beetles found at this time have not yet been
parasitized. The distribution of beetle body sizes
is thus mainly due to bottom-up effects of food
availability, and not due to any possible selection
by parasitoids. Because higher beetle densities
were found on Salix cinerea than S. viminalis in the
wild, the former host species was chosen for the
field study. Sixteen wild S. cinerea plants located
in Uppsala (59848 0 N, 17838 0 E), North of Stockholm, Sweden, were included in the survey. The
minimum distance between the plants was at
least two kilometers. The level of defoliation (%)
was estimated by eye for each plant. This is
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RESULTS
Controlled laboratory experiment
Herbivore larval density class had a highly
significant effect on larval development time
(ANOVA: df 7, MS 86.69, F 21.27, P ,
0.001), pupal weight, (ANOVA: df 7, MS
36.27, F 40.40, P , 0.001; Fig. 1) and survival
(ANOVA: df 7, MS 0.58, F 4.97, P , 0.001)
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Fig. 1. Effects of larval densities of the blue willow beetle, Phratora vulgatissima, on its pupal weight and the
survival of imagobiont Perilitus brevicollis parasitoids (from egg to cocoon and adult, respectively). Each data
point in the top panel represents a mean value, and in the bottom panel, a fraction (number of surviving cocoons,
and adult parasitoids, respectively, divided by the total number of cocoons and adults), derived from all the
herbivores in a group with a certain herbivore density (115 herbivore larvae per group). In the top panel, n , 40
for group sizes 13, and n , 20 for group sizes 315. In the lower panel, n 1 per group size. Note that many data
points overlap.

of the herbivore Phratora vulgatissima (Fig. 1).

Larval development time increased linearly (Fig.
2a), and pupal weight decreased linearly (Fig. 1)
with increasing larval densities. Larval survival
decreased linearly with increasing larval densities (Fig. 2). Although, statistically, the relationv www.esajournals.org

ship between density and body size is linear, the

decline in mean body size seems to be reduced at
the very highest herbivore larval density (Fig. 1).
This is probably an effect of the high larval
mortality, which eventually reduced larval density as well as competition in the groups which,
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Fig. 2. Effects of larval densities of the blue willow beetle, Phratora vulgatissima, on (a), larval development time
(from egg hatching to pupa), and (b), larval survival. Each data point in (a) represents a mean value, and in (b), a
fraction (number of surviving larvae divided by the total number of larvae), derived from all the larvae in a group
with a certain herbivore density (115 larvae per group). For group sizes 13, n , 40 and n , 20 for group sizes
315. Note that many data points overlap. The linear trend line in (b) covers group sizes 315 as larval survival
peaked at a group size of 3.

initially, were most crowded.

As is normal within the genus Perilitus
(Berkvens et al. 2010, Stenberg 2012), the parasitoid larvae experienced a relatively high mortality. Successful parasitism varied between 0 (no
parasitoids survived to adulthood) and 0.25 (one
in four of the parasitoids survived to adulthood)
(Fig. 1). Parasitoid survival decreased in parallel
with increasing herbivore larval density. The
decline was evident for the whole developmental
period (egg stage to adult stage, linear regression: df 6, R 2 0.753, t 4.272, P 0.005; Fig.
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1), but most pronounced in the cocoon stage

(linear regression: df 6, R 2 0.800, t 4.897, P
0.003; Fig. 1). Thus, even though many
parasitoids managed to develop and spin a
cocoon, they often died before emerging as
adults. Those few parasitoid larvae that survived
to the cocoon stage despite having been reared in
association with high-density herbivores (15
herbivores per cage) all died during the cocoon
stage, while all cocoons produced by parasitoids
of low-density herbivores (12 herbivores per
cage) survived and emerged as adults (Fig. 1).
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decline much further until more than about 70%

defoliation, after which it (the third group) again
drops markedly. Altogether, the field data on
how herbivore body weight declines in parallel
with increased defoliation resemble the laboratory data, although the latter indicate a more
continuous decline as compared to the putative
thresholds identified in the field.

DISCUSSION
This study was undertaken to investigate why
parasitoids often fail to utilize the increased
number of hosts available during herbivore
outbreaks. Two distinct patterns emerged when
rearing herbivores in different density classes.
First, the herbivore was increasingly controlled
bottom-up; herbivore body size decreased, and
larval development time increased in parallel
with increasing herbivore larval density class. At
high herbivore larval densities, the food plant
was eventually totally consumed, suggesting that
the beetles faced starvation and sometimes had
to pupate prematurely. A similar pattern was
found on S. cinerea in the field: beetle body size
declined markedly and significantly in parallel
with increasing level of defoliation (see Fig. 4 for
an example of wild Salix plant skeletonized by
Phratora vulgatissima). However, on S. cinerea in
the field, the decline is not gradual, but occurs in
two major steps. The first major decline in body
weight happened at around 3% defoliation,
which fits nicely with previous findings showing
that moderate beetle grazing induces trichomes
in S. cinerea which drastically reduce larval
performance, including body weight (Dalin and
Bjorkman 2003). The initial reduction in body
weight on plants with relatively low defoliation
may thus be due to induced defense in the plant.
The second reduction in body weight occurs at
roughly 70% defoliation, and this is probably due
to food limitation.
Second, while bottom-up control increased, it
is evident that parasitoid survival declined at
high herbivore densities. This suggests that, in
this case, the top-down control is itself controlled
bottom-up. That parasitoid fitness is dependent
on herbivore size has been shown in a number of
studies (e.g., Harvey et al. 1995, Harvey et al.
2005, Pennacchio and Strand 2006, Stenberg and
Hamback 2010), not least for this particular

Fig. 3. Effects of defoliation level on sixteen Salix

cinerea plants in the field (Uppsala, Sweden) on the
mean adult body weight of the blue willow beetle
(Phratora vulgatissima) individuals on them. The
number of beetle individuals on each plant varied
between 1 and 81.

Parasitoid body size was not measured in this

experiment, but has previously been shown to be
negatively related to beetle size (Stenberg
2012).The parasitoids larval development time
was not affected by herbivore larval density class
(linear regression: df 48, R 2 , 0.001, t 0.132, P
0.895).

Field study
The degree of defoliation varied between 1%
and 90% on the investigated S. cinerea plants (Fig.
3). The number of beetles found on the plants
varied between 1 and 81 individuals; low
numbers were found on plants with ,2% or
.85% defoliation. The GAM analysis showed
that the percentage defoliation significantly
affected the mean beetle body weight (F
5.041, P 0.0133, R 2 0.543) on the 16 S. cinerea
plants examined. The body weights found can be
roughly divided into three groups with respect to
the plant defoliation pattern. First, by far the
highest body weights were found on plants with
very limited defoliation (,3% defoliation; Fig. 3),
thereafter rapidly declining. Second, the mean
body weight seems to stabilize at an intermediate
level above about 3% defoliation and does not
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Fig. 4. Wild Salix being skeletonized by Phratora vulgatissima leaf beetles.

species (Stenberg 2012). Generally, parasitoids

perform less well in small host bodies. In the
current context, this relationship should provide
an opportunity for the herbivores to escape the
parasitoids and increase until they are unable to
sustain themselves and the outbreak collapses.
One of the findings that has emerged from the
literature on parasitoids and the impact of host
body size is that many parasitoids are able to
discriminate between host sizes and preferentially oviposit on hosts of a more optimal size (Jervis
et al. 2008). Such behavior could potentially
stabilize the system and mitigate the parasitoid
decline suggested by my data. Even though this
is a possibility, the potential to find hosts of
optimal size will be greatly reduced during
outbreaks (Fig. 1).
The results presented here suggest that the
parasitoid decline is principally self-driven once
the herbivore population has reached a high
density. When the herbivore population grows,
the individual herbivores reach a smaller average
size due to increased competition (Figs. 1 and 3).
Parasitoids respond immediately with a reduction in their fitness (Fig. 1), which in turn should
produce lower parasitism pressure in the next
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beetle generation. Following this train of thought

the reduced top-down pressure should result in
higher herbivore survival, and even increased
herbivore competition, leading to even smaller
herbivore body sizes, and so on until the
parasitoid population collapses. In the absence
of efficient trophic interactions, the herbivore
population should be able to survive and grow
until the outbreak is countered by bottom-up
forces. Although speculative, this suggestion
accords with previous findings that herbivores
are food limited during outbreaks, rather than
being regulated by parasitoids (White 2011).
Many previous studies have examined whether parasitoids control the population dynamics of
their herbivore hosts, or if the herbivores control
the parasitoids (Hassell and Waage 1984, Tanhuanpaa et al. 2002, Turchin et al. 2003, Hagen et
al. 2010, Schott et al. 2010, White 2011). This
study suggests that, during P. vulgatissima outbreaks, it is the herbivores that control the
parasitoids, and not vice versa. Parasitoids
undoubtedly play a very important role between
outbreaks in many systems, and may very well
constitute an important reason why herbivores
rarely reach the threshold level above which
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Lehrman, A., M. Torp, J. A. Stenberg, R. JulkunenTiitto, and C. Bjorkman. 2012. Estimating direct
resistance in willows against a major insect pest,
Phratora vulgatissima, by comparing life history
traits. Entomologia Experimentalis et Applicata

outbreaks are initiated (DeBach and Rosen 1991).

Thus, the solution to outbreaks in cropping
systems is not to stop using parasitoids, but to
use additional biocontrol agents that are less
sensitive to herbivore body size during outbreaks
(e.g., predators). In the Salix system it has been
suggested that omnivorous egg-feeding heteropterans could be used for this purpose (Bjorkman
et al. 2003, Stenberg et al. 2010).
As indicated previously, plant-herbivore-parasitoid dynamics have been surprisingly resistant
to explanation and their complexity should not
be underestimated. Nevertheless, density-dependent body size seems to be one important factor,
and I hope that this study will inspire theoretical
ecologists to incorporate it into future models. In
addition, the seemingly negative interaction
between induced plant defenses affecting herbivore body size, and indirect defenses through
parasitoids that are sensitive to reduced prey
sizes, should be studied further. Taking herbivore
body size into consideration will probably
improve mathematical models of species interactions as well as programs for biological control of
insect pests.

ACKNOWLEDGMENTS
I thank Warren Kunce and Ling Shen for technical
assistance in the laboratory. This study was funded by
The Foundation in Memory of Oscar and Lili Lamm
and the Swedish Research Council Formas.

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