Bj-rkman_et_al-2005-Ecological_Entomology

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Foraging behaviour influences the outcome of
predator–predator interactions
CHRISTER BJ O¨RKMAN and ANNA - SARA L IMAN Department of Entomology,
Swedish University of Agricultural Sciences, Uppsala, Sweden
Abstract. 1. Interactions among predators may influence the total efficiency of a
predator complex. The effect of intra- and interspecific interactions of the general-
ist predators Orthotylus marginalis (Heteroptera: Miridae) and Anthocoris
nemorum (Heteroptera: Anthocoridae) was investigated in a laboratory experi-
ment. Outcomes of the interactions were determined by comparing predation rates
on eggs and larvae of the blue willow beetle Phratora vulgatissima of single
individuals with those of two individuals of the same or different species.
2. A non-additive, antagonistic effect on predation rates due to intraspecific
interactions was found between individuals of A. nemorum. No such effect was
found in O.marginalis. These results are as expected as a consequence of differ-
ences in behaviour of the two predator species: A. nemorum is a much more active
and mobile predator than O.marginalis.
3. Contrary to expectation, interspecific interactions between A. nemorum and
O.marginalis did not affect the total predation rate.
4. An observation from the field corroborated the results obtained in the
laboratory study; there was no negative relationship between the densities of the
two predator species, indicating that the two species do not interact negatively in
the field at their natural densities.
5. It is concluded that the additive effect of multiple predator species is of
potential value in biological control.
Key words. Anthocoridae, Anthocoris nemorum, Heteroptera, interspecific inter-
actions, intraspecific interactions, Miridae, Orthotylus marginalis, polyphagous
insect predators, willow leaf beetles.
Introduction
Understanding how a predator complex interacts and influ-
ences herbivore populations is of vital importance for both
population ecology and integrated pest management (Losey
& Denno, 1998; Sih et al., 1998; Symondson et al., 2002).
Multiple predators often affect prey in ways that cannot be
predicted simply by adding the independent linear effects of
single predator types. Indeed, either more or fewer prey may
be consumed in the combined release of predators com-
pared with adding two single predators individually (Spiller,
1986; Rosenheim et al., 1993; Losey & Denno, 1998; Sih
et al., 1998). However, a negative interaction between pre-
dators may not necessarily hinder a depression of the prey
population (Lang, 2003). A combined release of multiple
species may also add up to the sum of the individual species
effect (Chang, 1996; Sokol-Hessner & Schmitz, 2002).
Several studies have demonstrated the ability of general-
ist predators to reduce prey populations (Jervis & Kidd,
1996). Nevertheless, the intensities of intra- and interspecific
interactions among generalist predators have seldom been
investigated experimentally within the context of biological
control (Symondson et al., 2002). Symondson et al. (2002)
concluded that interactions between species of generalist
predators and their prey are important for successful bio-
logical control. New insights into the regulation of herbivore
populations may, thus, be provided through a detailed
determination of interactions between generalist predators
Correspondence: Christer Bjo¨rkman, Department of Entomol-
ogy, Swedish University of Agricultural Sciences, PO Box 7044,
SE-750 07 Uppsala, Sweden. E-mail: christer.bjorkman@entom.
slu.se
Ecological Entomology (2005) 30, 164–169
164 # 2005 The Royal Entomological Society
and the mechanisms that underlie these interactions (Sih
et al., 1998; Symondson et al., 2002).
Generalistic heteropteran predators seem to be important
in the population dynamics of willow leaf beetles (Bjo¨rkman
et al., 2000a, 2004). Leaf beetles (Coleoptera:
Chrysomelidae) are the most serious and widespread insect
pests of willows grown as short-rotation coppice used for
example, for biomass production (Peacock et al., 2001).
High defoliation by the blue willow beetle, Phratora
vulgatissima L. (especially by the larvae) may reduce willow
growth substantially (Bjo¨rkman et al., 2000b). Heteropteran
predators, such as Anthocoris nemorum (L.) (Anthocoridae)
and Orthotylus marginalis Reuter (Miridae), are two of the
most common generalist predators of eggs and young larvae
of P. vulgatissima (Bjo¨rkman et al., 2003).
Predators have broadly been characterised as having a
searching or sit and wait foraging strategy (Sih et al., 1998).
Searching predators are more likely to interact than sit and
wait predators. A high encounter rate is likely to result in
fewer prey consumed than expected, whereas a low encoun-
ter rate between predators is less likely to affect predation
rates (Sih et al., 1998). The two heteropterans, A. nemorum
and O.marginalis, show a striking difference in behaviour:
A. nemorum is a much more active and mobile predator
than O.marginalis (Bjo¨rkman et al., 2003). However, they
do not fit perfectly into the searching and sit and wait
terminology. Here it has been suggested that run and eat
and find and stay foraging strategies would be more suitable
terms to describe the feeding habits of A. nemorum
and O.marginalis, respectively (Bjo¨rkman et al., 2003).
Anthocoris nemorum feeds on one or a few eggs in a food
patch (e.g. a batch of leaf beetle eggs) before moving on
whereas O.marginalis typically stays near a food patch until
all food items have been consumed.
The primary objective of this study was to quantify the
effect of intra- and interspecific interactions between
predator individuals of A. nemorum and O.marginalis on
predation rates of eggs and larvae of the blue willow beetle,
P. vulgatissima. The overall hypothesis was that the more
active and mobile A. nemorum would be more affected by
both intra- and interspecific interactions than the less
mobile O.marginalis. More specifically, three predictions
were addressed: (1) Intraspecific interactions between
A. nemorum individuals have a non-additive antagonistic
effect on predation rates because the active lifestyle of this
species is expected to result in frequent encounters. (2)
Intraspecific interaction between O.marginalis individuals
has an additive effect on predation rates because the less
active lifestyle of this species is expected to result in less
frequent encounters. (3) Interspecific interaction between
predatory individuals of A. nemorum and O.marginalis has
a non-additive, antagonistic effect on predation rates,
although weaker than the one expected for the intraspecific
interaction between A. nemorum individuals. For simplicity,
these predictions were addressed in a laboratory experi-
ment. In this experiment prey-type preference was also
studied because species-specific prey-type preferences may,
if they exist, explain the outcome of interspecific interac-
tions. The preference for eggs and larvae in A. nemorum and
O.marginalis was therefore determined.
To determine whether the results obtained in the labora-
tory study could be applicable to the field, data from 12
willow plantations collected between 2000 and 2002 were
used to address the hypothesis that the density of the two
predator species should be negatively correlated, at least at
high densities.
Materials and methods
Laboratory experiment
Intra- and interspecific interactions between the general-
ist predators O.marginalis and A. nemorum were investi-
gated in a laboratory experiment in 2002.
Potted plants of Salix viminalis L. were arranged in a
randomised block design with five plants in a block. Eggs
andlarvae of P. vulgatissima were applied to leaves on the
plant. Each plant was assigned randomly a specific treat-
ment consisting of a certain combination of the predator
species. Five treatments were used: (O), one O.marginalis
individual; (2O), two O.marginalis individuals; (A), one
A. nemorum individual; (2A), two A. nemorum individuals;
and (OþA), one O.marginalis and one A. nemorum indivi-
dual together.
The number of surviving eggs and larvae remaining on
the plant were counted after 48 h. Mortality was determined
by subtracting the number of eggs and larvae remaining at
the end of the exposure period from the initial number.
Host plant
The experiment was carried out on 5- to 6-week-old
S. viminalis plants of clone 78021. Plants were kept in a
greenhouse until the experiment started. The experiment
was conducted in an environmentally controlled room
(20 �C, LD 16:8 h, RH 70%). Each plant was isolated in a
plastic cylinder (d¼ 40 cm, h¼ 90 cm), which was pushed
into a sand-filled pot (d¼ 50 cm) forming a seal at ground
level. The experiment was carried out on the upper 25 cm of
the willow sapling, including 10–15 leaves. A plastic cup
ringed on the inside with the slippery material Fluon1 (ICI,
Herts, U.K.) limited the experimental area and prevented
the predators from leaving the area.
Prey
Eggs and larvae of P. vulgatissima were collected in
willow plantations prior to the experiment. Two or three
masses of eggs and two or three assemblages of larvae
were applied to each plant. Rectangular fragments of leaves
with eggs or larvae were attached with insect pins to the
lower side of randomly chosen leaves in the experimental
area. In total, 40–50 eggs and 30–40 larvae were present on
Behaviour and predator–predator interactions 165
# 2005 The Royal Entomological Society, Ecological Entomology, 30, 164–169
each plant. The number of eggs in an egg mass varied
between 10 and 20 eggs and the number of larvae in a
group was 8–15. To ensure that the consumption of eggs
and larvae by predators did not exhaust the prey supply
before the experiment was terminated, the number of prey
on each plant was adjusted to levels based on predation
rates in previous experiments (Bjo¨rkman et al., 2003).
Second- to third-instar larvae were used and only relatively
undeveloped eggs were used to reduce the likelihood that
they would hatch during the experiment. Because the aim
was to obtain a good estimate of predation rate and since
the number of prey items presented in each individual trial
did not vary substantially, the number of eggs and larvae
disappearing was used as the dependent variable in the
analyses.
Predators
Nymphs in the fourth to fifth developmental stages of the
generalist predators, O.marginalis and A. nemorum, were
collected in willow plantations within 1week prior to the
experiment. Nymphs in captivity were kept at 7 �C and fed
identical food, i.e. eggs of P. vulgatissima, until 24 h before
the experiment when they were starved to ensure equal
motivation to eat. The predators were kept isolated from
each other in Eppendorf vials (1.5ml) to avoid cannibalism.
At the beginning of the experiment the predators were
applied to the plant on one of the lower leaves in the
restricted experimental area. In treatments that included
more than one predator individual, the predators were put
on different leaves but at the same level on the plant.
Cannibalism was never observed. All predator individuals
in each block were equal in size/developmental stage, but
distributed randomly among treatments. The densities used
in the laboratory experiments corresponded to densities
commonly observed in the field.
Statistical analyses
The effect of predation by O.marginalis and A. nemorum
on P. vulgatissima was first compared among all five
treatments to justify further pairwise comparisons using a
General Linear Model (ANOVA). The Statistical Analysis
System (SAS# release 6.12) was used (SAS Institute, 1996).
To test the prediction that intraspecific interactions
between predator individuals of A. nemorum have a non-
additive antagonistic effect on predation rates, whereas
intraspecific interactions have an additive effect in
O.marginalis, pairwise comparisons were performed. Treat-
ments with one single predator were compared with treat-
ments with two conspecific predators. Twice the value of
the single predators effect was applied in the comparison,
i.e. 2� (A) vs. (2A) and 2� (O) vs. (2O).
To test the prediction that interspecific interactions bet-
ween predatory individuals of A. nemorum and O.marginalis
have a non-additive, antagonistic effect on predation
rates, treatments with one single predator and both preda-
tor species together were compared. In other words, the sum
of the single individual treatments was compared with the
treatment with both species together, i.e. (O)þ (A) vs.
(OþA). Because the different densities of predators may
affect the results, a second comparison was carried out
where only the results of treatments with an equal number of
predatorswere compared. Insteadof using the sumof the single
individual treatments, i.e. (O)þ (A), to determine the effect of
interspecific interactions, half the value of the combined con-
specific treatment was applied, i.e. (2O)/2þ (2A)/2 vs. (OþA).
To test whether the predator species showed a preference
for eggs or larvae of P. vulgatissima the ratio of egg and
larvae eaten by A. nemorum and O.marginalis in the single
individual treatments was compared.
Field density
The density of the two predator species was estimated for
three years (2000–2002) in 12 willow plantations in an
agricultural area situated north-west of Stockholm in cen-
tral Sweden (59�400N, 17�300E). The sizes of the plantations
vary between 0.2 and 11.8 ha (mean¼ 3.2, SD¼ 3.0). The
distance between individual plantations was at least 400m
and therefore dispersal between plantations was assumed to
be limited (see also Bjo¨rkman et al., 2004). All plantations
are planted completely with S. viminalis except for one large
plantation with a few rows of S. dasyclados.
The density of A. nemorum and O.marginalis (and other
generalist predators, most of which occurred at significantly
lower densities) was estimated by knockdown sampling in
late spring (mid May to early June) in all 12 plantations.
Samples were taken along six transects within a plantation
and along the entire edge of the plantation. Transects were
evenly distributed to obtain samples from the entire planta-
tions. Transect length varied with plantation size. However,
at least 30 samples were collected from each plantation,
which is a sufficient number to arrive at a stable estimate
of density; in several independent pre-studies it was found
that 22–24 samples are sufficient to obtain stable estimates
of mean and variance of densities in a plantation. This
means that the distance between samples was somewhat
shorter than the standard 15m in the smallest plantations.
Each knockdown sample was taken from the top part
(40 cm long) of a shoot. To estimate the number of predator
individuals per stool (a stump with re-sprouting shoots) the
number of individuals in a sample was multiplied by the
number of 40-cm pieces of leaf-bearing shoots. The number
and size of leaf-bearing shoots varies with years after har-
vesting (willow plantations are harvested each third to fifth
year). This was accounted for by using different correction
values for different times after harvesting. The number of
stools per hectare is normally 10 000 in the plantations.
The relationship between the densities of the two preda-
tor species was first observed by eye to possiblydetect any
trends of a negative correlation, at least at higher densities.
166 Christer Bjo¨rkman and Anna-Sara Liman
# 2005 The Royal Entomological Society, Ecological Entomology, 30, 164–169
When no such pattern could be detected a simple correla-
tion was applied to the data.
Results
Laboratory experiment
There was a significant difference in prey mortality
among all treatments (F4,75¼ 5.76, P< 0.0001; Fig. 1).
This justified further pairwise comparisons in order to
investigate the specific effect of intra- and interspecific
interference.
Intraspecific interactions
Fewer prey than expected were killed when two predators
of the species A. nemorum was compared with twice the
effect of one predator, i.e. there was a significant non-
additive, antagonistic effect on predation rates due to
intraspecific interactions between individuals of
A. nemorum [comparison 2� (A) vs. (2A) in Table 1; cf.
Fig. 1]. There was no significant effect on prey mortality
due to intraspecific interactions between individuals of
O.marginalis [comparison 2� (O) vs. (2O) in Table 1; cf.
Fig. 1]. The combined effect was additive and did not differ
significantly from the sum of the individual impacts.
Interspecific interaction
There were no significant effects of interspecific interac-
tions between A. nemorum and O.marginalis [comparison
(O)þ (A) vs. (OþA) in Table 1; cf. Fig. 1]. The result of
the second complementary comparison, where a possible
effect of different predator densities was considered, indi-
cated the same result [comparison (2O)/2þ (2A)/2 vs.
(OþA) in Table 1; cf. Fig. 1]. The combined effect did not
differ significantly from the sum of the individual species’
single impact on prey mortality.
Prey-type preference
Orthotylus marginalis predated more frequently on eggs
than larvae (F1,30¼ 4.73, P¼ 0.038) in the control treatment
with only one predator individual. In total 76% of the prey
consumed by O.marginalis were eggs (Fig. 1). Anthocoris
nemorum did not have a preference for either of the prey
types (F1,30¼ 2.03, P¼ 0.16). Forty-eight per cent of the
prey consumed by A. nemorum were eggs (Fig. 1).
Field density
The density of the two species showed no sign of any
negative relationship but tended to be positively correlated
when viewed over all three years (Fig. 2; R¼ 0.306,
P¼ 0.08).
Discussion
The results presented here support the hypotheses that pre-
dation rates of mobile predators (A. nemorum) are nega-
tively affected by intraspecific interaction and that
predation rates of less mobile predators (O.marginalis) are
not. However, no support was found for the hypothesis that
interspecific interaction between a more sedentary predator
species and a mobile predator species affect the predation
rates negatively. The data from the field agreed with this
result: there was no negative correlation between the den-
sities of the two species.
In theory, two searching (mobile) predators should have
high encounter rates and thus affect each other’s predation
rates negatively whereas two sit and wait (less mobile) pre-
dators should rarely encounter each other and thus show
O + A2AA2OO
0
5
10
15
20
25
30
35
Treatment
N
um
be
r o
f p
re
y 
co
ns
um
ed
Larvae
Eggs
Fig. 1. Effect of intra- and interspecific interactions between two
generalist heteropteran predators on total (eggs þ larvae) mortality
of the prey species Phratora vulgatissima. The five predator
treatments were: one Orthotylus marginalis (O); two O.marginalis
(2O); one Anthocoris nemorum (A); two A. nemorum (2A); and one
O.marginalis and one A. nemorum (OþA). Means (þSE) are
presented.
Table 1. Effect of intra- and interspecific interactions between two
heteropteran generalist predators (Anthocoris nemorum and Ortho-
tylus marginalis) on predation rates of eggs and larvae of the blue
willow beetle Phratora vulgatissima. Predation rates of single
individuals were compared with those of two individuals of the
same or different species using a General Linear Model (ANOVA).
n¼ 16, d.f.¼ 1 and error d.f.¼ 30 for all comparisons.
Comparison Interaction F P
2� (O) vs. (2O) Intraspecific 0.20 0.65
2� (A) vs. (2A) Intraspecific 6.85 0.014
(O)þ (A) vs. (OþA) Interspecific 1.20 0.28
2O/2þ (2A)/2 vs. (OþA) Interspecific* 0.05 0.83
*Possible effects of differences in predator density removed.
Behaviour and predator–predator interactions 167
# 2005 The Royal Entomological Society, Ecological Entomology, 30, 164–169
additive predation or weak antagonistic effects (Sih et al.,
1998). Even though the two predator species studied here do
not fit perfectly into the dichotomy used by Sih et al. (1998),
their behaviour (run and eat vs. find and stay) differs enough
to make relevant comparisons. The laboratory study pre-
sented here is believed to be the first to confirm theoretical
predictions of how predator behaviour may determine the
effect of intraspecific interactions on predation rates.
The environment used in the laboratory experiment was
restricted and physical interference was likely to occur fre-
quently, especially for mobile predators such as
A. nemorum. Anthocorids are also known to produce what
may be an alarm substance when disturbed. A combination
of a high degree of physical interference and the occurrence
of an alarm substance may be the mechanisms responsible
for the effect of anthocorid intraspecific interactions on
prey mortality. A consequence of physical interference
may be a willingness to migrate. Evans (1976) showed that
interference between fecund Anthocoris confusus triggers a
tendency to leave an area with high density of conspecific
predators even when prey was abundant. Mirids, on the
other hand, show migration behaviour in response to low
prey densities, but no such behaviour has been observed at
high prey densities (Foglar et al., 1990). The prey densities
used in the present experiment were probably high enough
not to trigger any migration behaviour in the mirid. The
lack of visible impact on predation rates in the treatment
with two O.marginalis individuals suggests that these pre-
dators interacted neither physically nor through alarm sub-
stances.
The results of the laboratory study showed no effect of
interspecific interaction between the less mobile predator
O.marginalis and the mobile predator A. nemorum on total
predation rates. The data from the field, showing no
negative relationship between the two species with respect
to density, gave the same indication. These results contra-
dict earlier studies on interspecific interaction, which
have shown reduced predation rates as a consequence of
interspecific interference between an actively searching
predator and a sedentary predator (Soluk & Collins, 1988;
Rosenheim et al., 1993; Soluk, 1993). Sometimes, the seden-
tary predator attacks or even kills the active predator,
leading to reduced search rates (Soluk & Collins, 1988;
Rosenheim et al., 1993; Soluk, 1993). By contrast Connel
(1983) came, in a review of field experiments, to the conclu-
sion that intraspecific interaction is more intense than inter-
specific interaction. However, among very similar species,
interspecific interaction may sometimes be just as intense as
intraspecific interaction (Evans, 1991). It seems likely that
the behaviour of the two heteropterans studied here differed
enough to avoid any strong negative interactions.
Effects of interactions are not only related to behavioural
characteristics, but also to species characteristics such as
defensive behaviour, density dependence, and prey-type
preferences. Prey-type preferences may partly explain addi-
tive effects inan interspecific interaction. In this study, 76%
of the prey consumed by O.marginalis were eggs. This
indicates a preference for eggs over larvae for the prey
species P. vulgatissima. Anthocoris nemorum, on the other
hand, did not show a preference for either of the available
prey. One possible mechanism behind the preference of
O.marginalis for eggs is the defensive behaviour of larvae.
Larvae of Chrysomelinae, such as P. vulgatissima, evert
dorsal exocrine glands. The larval secretions are generally
considered to contain chemical defence substances, which
deter predators and parasites (Pasteels et al., 1984). Thus,
O.marginalis seems to avoid eating larvae possibly due
to the larval defensive behaviour, whereas A. nemorum
does not avoid larvae and eats an equal number of eggs
and larvae. It is here interesting to note that the main
feeding period of O.marginalis is when the number of
P. vulgatissima eggs peak whereas the main feeding period
of A. nemorum is slightly later when both eggs and larvae
are available. The difference in prey-type preference
between the two species may thus be a result of what prey
types the species normally encounter.
In practice, intra- and interspecific interactions between
generalist predators within multispecies systems under the
influence of biotic and abiotic variables are difficult to
predict (Symondson et al., 2002). Evaluations of multiple
biocontrol agents should be conducted in settings that
mimic the environment of the field as closely as possible.
The experiments reported here were carried out on plants in
a multidimensional, but restricted, environment. The cage
may have limited the natural foraging or migration beha-
viour of the predators and especially that of A. nemorum,
which has a more active searching behaviour. Another
aspect that may have affected the results is that only one
density of prey was used, whereas two different densities of
predators were applied. The densities of prey should affect
the probability that two predators encounter each other and
interact. If lower densities of prey had been tested, it may
have been possible to detect a weak interaction effect
between the predator species.
0
10
20
30
40
50
0 1 2 3
Density of Anthocoris nemorum
D
en
si
ty
 o
f O
rth
ot
ylu
s 
m
ar
gi
na
lis
Fig. 2. Relationship between the densities of two common general-
ist insect predators (Anthocoris nemorum and Orthotylus margin-
alis) in 12 willow (Salix viminalis) plantations during three years.
168 Christer Bjo¨rkman and Anna-Sara Liman
# 2005 The Royal Entomological Society, Ecological Entomology, 30, 164–169
The tendency for a positive correlation in density between
the two predator species was an unexpected finding. This
may indicate that they both prefer certain habitats or that
their numbers are affected by the same factors (e.g. their
numerical response to changes in prey density). Further
studies are needed to reveal the mechanisms behind this
positive relationship, not least because such knowledge
may provide opportunities to promote natural enemies in
an effort to make biological control operational in the field.
In summary, it is concluded that the two heteropteran
species studied here seem to have foraging behaviours that
differ sufficiently to minimise negative, antagonistic inter-
specific interactions. The two species might thus be suitable
to use in combination in biological control; however, the
type of prey and crop system may raise obstacles in practice.
For example, the biological control of leaf beetles in willow
plantations seems to be disrupted by harvesting, taking
place during winter (Bjo¨rkman et al., 2004). The reason
for this is probably that the main natural enemies (i.e.
heteropteran predators) overwinter within the plantations,
and is thereby removed at harvest, whereas the prey mainly
overwinter outside the plantations (Bjo¨rkman et al., 2004).
In natural willow stands, not subject to harvesting, hetero-
pteran predators seem able to control P. vulgatissima and
other willow leaf beetle species (P. Dalin & C. Bjo¨rkman,
unpub. data; Bjo¨rkman et al., 2000a). Moreover, the intra-
specific interaction between individuals of O.marginalis
did not affect predation rates and this species is therefore
likely to predate effectively within an aggregated population
as long as prey is abundant. However, the strong negative
effect of intraspecific interaction shown for A. nemorum
may be a disadvantage in the control of an aggregated
pest such as P. vulgatissima. On the other hand, the intras-
pecific interaction between individuals of A. nemorum may
lead to migration of individual predators from areas with
high predator density. The consequence of migration is a
more even distribution of predator individuals throughout
the prey population. This could, in turn, increase the readi-
ness of predators to respond to an increase in prey numbers
when prey is occurring at lower densities.
Acknowledgements
We wish to thank Karin Eklund, Peter Dalin, Karin Ahrne`,
Sandra O¨berg, and Martin Wetterstedt for support,
assistance, comments, and advice. We thank Martin
Schroeder and Barbara Ekbom for valuable comments on
the manuscript. Steve Scott-Robson corrected the English.
The Swedish National Energy Administration supported
the study financially.
References
Bjo¨rkman, C., Bengtsson, B. & Ha¨ggstro¨m, H. (2000a) Localised
outbreak of a willow leaf beetle: plant vigour or natural enemies?
Population Ecology, 42, 91–96.
Bjo¨rkman, C., Bommarco, R., Eklund, K. & Ho¨glund, S. (2004)
Harvesting disrupts biological control of herbivores in a short-
rotation coppice system. Ecological Applications, 14, 1624–1633.
Bjo¨rkman, C., Dalin, P. & Eklund, K. (2003) Generalist natural
enemies of a willow leaf beetle (Phratora vulgatissima):
abundance and feeding habits. Journal of Insect Behaviour, 16,
747–764.
Bjo¨rkman, C., Ho¨glund, S., Eklund, K. & Larsson, S. (2000b)
Effects of leaf beetle damage on stem wood production in
coppicing willow. Agricultural and Forest Entomology, 2, 131–139.
Chang, G.C. (1996) Comparison of single versus multiple species of
generalist predators for biological control. Environmental
Entomology, 25, 207–212.
Connel, J.H. (1983) On the prevalence and relative importance of
interspecific competition: evidence from field experiments.
American Naturalist, 122, 661–696.
Evans, E.W. (1991) Intra- versus interspecific interactions of
ladybeetles (Coleoptera: Coccinellidae) attacking aphids. Oeco-
logia, 87, 401–408.
Evans, H.F. (1976) Mutual interference between predatory
anthocorids. Ecological Entomology, 1, 283–286.
Foglar, H., Malausa, J.C. & Wajnberg, E. (1990) The functional
response and preference of Macrolophus caliginosus (Hetero-
ptera: Miridae) for two of its prey: Myzus persicae and
Tetranychus urticae. Enthomophaga, 35, 465–474.
Jervis, M. & Kidd, N. (1996) Insect Natural Enemies: Practical
Approaches to their Study and Evaluation. Chapman&Hall, London.
Lang, A. (2003) Intraguild interference and biocontrol effects of
generalist predators in a winter wheat field.Oecologia, 134, 144–153.
Losey, J.E. & Denno, R.F. (1998) Positive predator–predator
interactions: enhanced predation rates and synergistic suppres-
sion of aphid populations. Ecology, 79, 2143–2152.
Pasteels, J., Rowell-Rahier, M., Braekman, J.C. & Daloze, D.
(1984) Chemical defences in leaf beetles and their larvae: the
ecological, evolutionary, and taxonomic significance. Biochem-
ical Systematics and Ecology, 12, 395–406.
Peacock, L., Lewis, M. & Herrick, S. (2001) Factors influencing the
aggregative responseof the blue willow beetle Phratora vulga-
tissima. Entomologia experimentalis et applicata, 98, 195–201.
Rosenheim, J.A., Wilhoit, L.R. & Armer, C.A. (1993) Non-
additive effects of multiple natural enemies on aphid popula-
tions. Oecologia, 108, 375–379.
SAS Institute (1996) SAS/Stat User Guide. SAS Institute Inc.,
Cary, North Carolina.
Sih, A., Englund, G. & Wooster, D. (1998) Emergent impacts of
multiple predators on prey. Trends in Ecology and Evolution, 13,
350–355.
Sokol-Hessner, L. & Schmitz, O.J. (2002) Aggregate effects of
multiple predator species on a shared prey. Ecology, 83, 2367–2372.
Soluk, D.A. (1993) Multiple predator effects: predicting combined
functional response of stream fish and invertebrate predators.
Ecology, 74, 219–225.
Soluk, D.A. & Collins, N.C. (1988) Synergistic interactions
between fish and stoneflies: facilitation and interference among
stream predators. Oikos, 52, 94–100.
Spiller, D.A. (1986) Interspecific competition between spiders and
its relevance to biological control by generalist predators.
Environmental Entomology, 15, 177–181.
Symondson, W.O.C., Sunderland, K.D. & Greenstone, M.H.
(2002) Can generalist predators be effective biocontrol agents?
Annual Review of Entomology, 47, 561–594.
Accepted 2 November 2004
Behaviour and predator–predator interactions 169
# 2005 The Royal Entomological Society, Ecological Entomology, 30, 164–169