SiC

D

R

A

ospsofbhtempwpb

Z

uRSdiztzm

1d

Basic and Applied Ecology 12 (2011) 516–522

patial distribution of interacting insect predators: Possible roles ofntraguild predation and the surrounding habitathrister Björkman∗, Hans Johansson, Tord Snäll

epartment of Ecology, Swedish University of Agricultural Sciences, P.O. Box 7044, SE-750 07 Uppsala, Sweden

eceived 15 November 2010; accepted 14 July 2011

bstract

Predator foraging behaviour affects the outcome of enemy–enemy interactions. Using a combination of fieldwork and lab-ratory experiments, we show that intraguild predation may be important in the field distribution of generalist predators thathare a common prey: the eggs (and larvae) of the leaf beetle Phratora vulgatissima, a major insect pest in coppicing willowlantations. We focused on a species from the hoverfly genus Parasyrphus (Syrphidae), which may exhibit large temporal andpatial variation in density. Predator and prey densities were quantified in 40 field plots in willow plantations. The likelihoodf finding hoverfly eggs declined with increasing densities of two predatory mirids, Orthotylus marginalis and Closterotomusulvomaculatus, which exhibit less mobile behaviour similar to that of hoverfly larvae. The density of a more mobile predatoryug species, the anthocorid Anthocoris nemorum, was not associated with hoverfly occurrence. These results corroborate theypothesis that less mobile predators should be stronger intraguild predators than mobilepredators. Further partial support forhis hypothesis was obtained in the laboratory study where individual predators were presented with clutches of P. vulgatissimaggs containing one hoverfly egg: the less mobile C. fulvomaculatus and O. marginalis tended to consume the hoverfly eggore readily than the more mobile A. nemorum. However, most individuals of all three bug species consumed the egg of the

otential competitor – the syrphid – within 24 h. The field study also showed that hoverfly occurrence was positively associatedith the density of their prey and with the presence of nearby forests. We conclude that intraguild predation, abundance ofrey and the surrounding habitat affect the distribution of hoverflies in this system and should be considered when developingiological control methods.

usammenfassung

Das Beutesuchverhalten beeinflusst das Ergebnis von Räuber-Räuber-Interaktionen. Mit einer Kombination aus Freiland-ntersuchungen und Laborexperimenten zeigen wir, dass die intraguild predation wichtig sein kann für die generalistischenäuber, die eine gemeinsame Beute teilen: die Eier (und Larven) des Blattkäfers Phratora vulgatissima, eines bedeutendenchädlings in Weiden-Kurzumtriebsplantagen. Wir betrachteten eine Schwebfliegenart aus der Gattung Parasyrphus (Syrphi-

ae), die große zeitliche und räumliche Dichtevariation aufweisen könnte. Räuber- und Beutedichten wurden auf 40 Probeflächenn den Weidenplantagen erhoben. Die Wahrscheinlichkeit Schwebfliegeneier zu finden ging mit zunehmenden Dichten vonwei räuberischen Miriden, Orthotylus marginalis und Closterotomus fulvomaculatus, zurück, die sich weniger mobil verhal- en als die Schwebfliegenlarven. Die Dichte einer mobileren räuberischen Wanzenart, der Anthocoride Anthocoris nemorum,eigte keinen Zusammenhang mit dem Auftreten der Schwebfliege. Diese Ergebnisse bestätigen die Hypothese, dass wenigerobile Prädatoren stärkere intraguild predators sein sollten als mobile Prädatoren. Diese Hypothese fand weitere Unterstützung

∗Corresponding author. Tel.: +46 18 67 1532; fax: +46 18 67 2890.E-mail address: christer.bjorkman@ekol.slu.se (C. Björkman).

439-1791/$ – see front matter © 2011 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.oi:10.1016/j.baae.2011.07.006

iSstddSw©

Kf

I

iifi1indctG

piieemeSti(1(esD

opiu(Alfab(

C. Björkman et al. / Basic and Applied Ecology 12 (2011) 516–522 517

n den Laboruntersuchungen, in denen einzelnen Räuberindividuen Gelege von P. vulgatissima angeboten wurden, die einchwebfliegenei enthielten. Die weniger mobilen C. fulvomaculatus und O. marginalis tendierten dazu, das Schwebfliegeneichneller zu fressen als die mobile A. nemorum. Allerdings konsumierten die Individuen aller drei Wanzenarten das Ei des poten-iellen Konkurrenten, der Schwebfliege, innerhalb von 24 Stunden. Die Freilanduntersuchung zeigte auch, dass das Auftretener Schwebfliege positiv mit der Beutedichte und dem Vorhandensein von Wäldern in der Nähe verknüpft war. Wir schließen,ass Prädation innerhalb der Gilde, die Beuteabundanz und das umgebende Habitat die Verteilung der Schwebfliegen in diesemystem beeinflussen und berücksichtigt werden sollten, wenn Methoden der biologischen Schädlingsbekämpfung entwickelterden.2011 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.

eywords: Predator foraging behaviour; Enemy–enemy interactions; Syrphidae; Predatory bugs; Orthotylus marginalis; Closterotomusppicin

ppesetoitisbstm

ii&tiab&mped

aoKofcseBA

ulvomaculatus; Anthocoris nemorum; Biological control; Salix; Co

ntroduction

Intraguild predation is an enemy–enemy interaction thats common in many ecological systems. It has been stud-ed in both terrestrial and aquatic systems, in mammals,sh, amphibians, insects and other invertebrates (e.g. Polis984; Polis & Myers 1989; Arim & Marquet 2004). Its studys typically motivated by the need to better understand theature and consequences of ecological interactions and toevelop effective and sustainable methods for biological pestontrol by using complementary combinations of predatorshat do not interact negatively (Symondson, Sunderland, &reenstone 2002).However, the study of intraguild predation presents a

ractical challenge. Natural systems often involve manynteracting species and experimental approaches necessar-ly involve simplifying the natural system. One powerful andlegant method for studying intraguild predation and othernemy–enemy interactions is to conduct semi-field experi-ents in large cages where predator species are included or

xcluded in a controlled manner (e.g. Finke & Denno 2004;nyder, Snyder, Finke, & Straub 2006). These experimen-

al approaches are accurate and provide significant insightnto the mechanisms underpinning the processes in questione.g. Rosenheim, Wilhoit, & Armer 1993; Losey & Denno998; Carey & Wahl 2010), but may be somewhat unrealisticLetourneau, Jedlicka, Bothwell, & Moreno 2009). In gen-ral, such experiments are not performed in conjunction withtudies of the species in question in nature (but see Finke &enno 2002; Rickers, Langek, & Scheu 2006).In this study, field observations were paired with lab-

ratory experiments to test the hypothesis that intraguildredation affects the distribution of potentially compet-ng insect predators. The predators involved are an as-yetnidentified species of the hoverfly genus ParasyrphusDiptera: Syrphidae) and three zoophytophagous bugs:nthocoris nemorum (Heteroptera: Anthocoridae), Orthoty-

us marginalis (Heteroptera: Miridae) and Closterotomusulvomaculatus (Heteroptera: Miridae). These species have

common prey: the eggs and larvae of the blue willow leafeetle Phratora vulgatissima (Coleoptera: Chrysomelidae)Björkman, Dalin, & Eklund 2003), the most severe insect

m(a

g willow plantations

est in coppicing willow (Salix) plantations used for biofuelroduction (Sage & Tucker 1998). The three bugs are all gen-ralist predators, but like many other predators, they seem topecialize in preying on species that are abundant. The hov-rfly seems to be more specialized on the eggs and larvae ofhe leaf beetle P. vulgatissima, as demonstrated by its habitf laying its eggs, which resemble those of the leaf beetle,n leaf beetle egg clutches. Thus, all four species may poten-ially compete for the same prey and are commonly observedn the vicinity of each other in natural and planted willowtands (Björkman et al. 2003). We focused on the hoverflyecause it exhibits the greatest variation in population den-ity (C. Björkman et al., unpublished data), suggesting thathere may be scope for increasing its population density by

anipulating its environment.It is evident that the foraging behaviour of predators

nfluences the outcome of enemy–enemy interactions, includ-ng intraguild predation (Losey & Denno 1998; Björkman

Liman 2005; Carey & Wahl 2010). One prediction ishat predator species with sedentary or less mobile forag-ng behaviour should, to a higher extent than predators with

more active foraging behaviour, include not only her-ivores but also other predators in their diet (Rosenheim

Corbett 2003). If this is true, predators with a lessobile foraging behaviour should be stronger intraguild

redators than more actively foraging predators. How-ver, relatively few studies have tested this predictionirectly.

As the four species of predators studied here differ in for-ging behaviour, one would expect variation in the strengthf enemy–enemy interactions (Björkman et al. 2003; Dalin,indvall, & Björkman 2006): When the mirids find a clutchf eggs they often consume them all before starting the searchor a new clutch (‘find-and-stay’ feeding strategy). The antho-orid is more active, and only consumes a few eggs from aingle clutch before moving on (‘run-and-eat’ feeding strat-gy). All stages of these zoophytophagous bugs are predatory.y contrast, only the larvae of the hoverfly are predatory.lthough adult hoverflies are strong fliers, the larvae are

uch less mobile; they typically feed on leaf beetle eggs

and larvae) in the vicinity of where they hatch and consumell nearby prey before moving on.

518 C. Björkman et al. / Basic and Applied Ecology 12 (2011) 516–522

Table 1. Information concerning the five sampled willow plantations.

Locality Geographic coordinates Plantation perimeter (m) Plantation area (ha) No. plots Latest harvest (year)

Buskvreten 59◦37′N, 17◦27′E 1940 7.6 7 2005Varpsund 59◦37′N, 17◦29′E 964 5.2 3 2007Tullstugan 59◦38′N, 17◦48′E 1164 3.5 7 N.A.GK

sl

(

(

(

(

(

dwitbp

M

F

rhasweltamme2

tee

est2tw

Dh

mttTm(Twenl(“

D

Ivowrei

H

ranby 58◦39′N, 17◦38′E 2300roksta 59◦56′N, 17◦27′E 2400

Given the known foraging behaviour of the predatorpecies studied in this work, we sought to evaluate the fol-owing questions:

Is the presence of hoverflies

1) negatively associated with the density of the less mobilemirid bugs?

2) not associated with the density of mobile anthocoridbugs?

3) affected by the density of prey (leaf beetle eggs) and thesize of leaf beetle egg clutches?

4) positively affected by occurrence of forest habitats,which provide shelter from wind and possibly floweringplants for the adults to feed from?

Additionally we asked:

5) Are the less mobile mirid bugs more likely to kill a poten-tial strong competitor, represented by a hoverfly egg ina cluster of leaf beetle eggs, than are the more mobileanthocorid bugs?

The first four questions were addressed by censusing theensity of the four predators and their main prey in plotsithin willow plantations. The fifth question was addressed

n a laboratory study and was complemented with an inves-igation of the size and some chemical properties of the leafeetle and hoverfly eggs as any difference could affect thereference of the bugs to feed on either type of the eggs.

aterials and methods

ield studies

To determine the relationships between hoverfly egg occur-ence and (1) the density of other natural enemies (i.e.eteropterans), (2) the density of leaf beetle eggs, (3) theverage size of beetle egg clutches and (4) the nature of theurrounding habitat, five willow plantations around Uppsalaere visited (see Table 1). These localities had been visited

arlier during the same season and had high densities of theeaf beetle P. vulgatissima. A number of 5 m × 5 m plots athe edges of the plantations, separated from one-another bydistance of 90 m, were sampled. This distance was used to

inimize the risk that an individual hoverfly would appear inore than one plot and is based on an investigation of hov-

rfly movements in different environments (Wratten et al.003). The other species have lower dispersal ranges than

Fpg

16.7 10 200715.0 13 2004

he hoverflies. Each plot was therefore treated as an isolatedxperimental unit, although we specify field as a randomffect (see Section “Statistical modeling of field data”).

The plantations (Table 1) differed in size. Consequently,ach had a different number of plots. The sizes of the plotsometimes had to be adjusted (8 were larger than 5 m × 5 m;he largest was 8.5 m × 5 m) since the goal was to find at least0 shoots with leaf beetle eggs in each plot. The samplingook place between 24/05/2008 and 26/05/2008. Each plotas censused once.

ensity of heteropterans and occurrence ofoverflies

The density of predators other than hoverflies was esti-ated by knockdown sampling (Björkman et al. 2003): the

op part (35 cm) of a single branch was shaken above a beatingray and the predators shaken off were identified and counted.he species counted in this study were the heteropterans O.arginalis (Om), C. fulvomaculatus (Cf) and A. nemorum

An). Other potential predators occurred in very low numbers.hirty samples were taken per plot. The density of hoverfliesas estimated by searching for hoverfly eggs in the leaf beetle

gg batches present in each plot (see below). Since the totalumber of hoverfly eggs per plot where they were found wasow, ranging between 1 and 3, we modeled their occurrenceabsence vs. presence) rather than their density (see SectionStatistical modeling of field data”).

ensity of leaf beetle egg clutches

All plots were systematically searched for leaf beetle eggs.n each plot, 5–10 leaf-carrying shoots per stem were sur-eyed for egg clutches 0.5–2 m above the ground. The numberf sampled shoots in each plot was recorded. The clutchesith hoverfly eggs were stored in a fridge for use in labo-

atory experiments. Additional clutches containing hoverflyggs were collected from other locations for use in the exper-mental study.

abitat effects

The habitats adjacent to each plot (100 m × 200 m; seeig. 1) were described and classified (on the basis of aerialhotographs and visual inspection) as being one of forest,rassland, arable land, or other. Area size was chosen on

C. Björkman et al. / Basic and Applied

Fig. 1. Illustration of a willow plantation, showing an inventory plot(h

thtasplehEaopa

S

etasstpti

l

wi

jmaeptrpmFaeid(

CinLfa

vfa(tSi1

aatpdDd(tatbmfpw

L

Intraguild predation between heteropterans and

small grey square) and the area adjacent to the plot studied in theabitat type analysis (dashed line).

he basis of estimates of the distance travelled by individualoverflies (cf. above and Wratten et al. (2003). Willow planta-ions were classified as arable land; streams, lakes, buildings,nd roads were classified as ‘other’. Previous studies havehown that forests and grasslands with tall vegetation haveositive effects on the abundance of hoverflies, while arableand is expected to have the opposite effect as many hov-rfly species seem to avoid flying longer distances in openabitats with no or low vegetation (Sjödin, Bengtsson, &kbom 2008). The classification of willow plantations asrable land was somewhat arbitrary. However, because allf the plots were surrounded by similar amounts of willowlantation, their precise classification did not significantlyffect the results or conclusions of the study.

tatistical modeling of field data

We modeled the probability of occurrence of hoverflyggs using a Bayesian hierarchical (random effects) logis-ic regression model. The reason for choosing the Bayesianpproach was that it is convenient for modeling hierarchicallytructured data (Gelman & Hill 2007). An additional morepecific reason was the sparse data, which made it impossibleo fit the model using frequentist statistics. The reason wasrobably lack of information about the standard deviation ofhe random effect (see below and Section “Results”). Plots,, were nested within fields, F. Specifically,

ogit(pi) = α +∑

βjXij + δF (i),

j

here p is the probability of hoverfly egg occurrence in plot, α is an “intercept” parameter, Xij is the ith value of the

h

A

Ecology 12 (2011) 516–522 519

th standardized (divided by its standard deviation) and nor-alized (subtracted by its mean) explanatory variable with

ssociated regression parameter βj (effect size). The param-ter δF(i) represents field-specific random effects. For eachlot, i, there is a field-specific random effect, F. F(i) meanshat plot i gets the field-specific random effect F. Although theesponse variable is not normally distributed, several of thearameters are. The prior distributions for α and β were nor-al with a mean of 0 and a precision (1/variance) of 0.001.or δF(i), we used a normal prior distribution with mean 0nd precision τδ. For the standard deviation of this randomffect (

√1/τδ) we assumed a uniform prior distribution rang-

ng from >0 to 100. Note that we use an uninformative prioristribution (it is uniform), and allow a wide range of valuesthe upper limit is as high as 100).

Models were evaluated using the Deviance Informationriterion (DIC), which measures the fit of the model penal-

zed for an increased model complexity, i.e. increasingumber of parameters (Spiegelhalter, Best, Carlin, & van derinde 2002, Snäll, O’Hara, & Arjas 2007). DIC is appropriate

or choosing between nested as well as non-nested models,nd is an analogue to Akaike’s Information Criterion (AIC).

We present the 95% and 50% Bayesian confidence inter-als for the effect size parameters (βj). These correspond torequentist confidence intervals. We also present the prob-bilities that the parameters are greater than or less than 0one type of Bayesian p-values). The models were fitted usinghe OpenBUGS 3.0.8 software (Thomas, O’Hara, Ligges, &turtz 2006). We ran two chains: after a ‘burn-in’ of 10,000

terations, every 10th iteration was taken from a total of00,000 iterations.

The densities of A. nemorum (An), C. fulvomaculatus (Cf),nd O. marginalis (Om) in individual plots ranged between 0nd 9, 0 and 29 and 0 and 38, respectively. The full model forhe probability of occurrence of hoverfly eggs (Dbar = 2.3,D = 1.9, DIC = 4.2) was effectively no better than one thatid not account for the density of An (Dbar = 2.4, pD = 1.9,IC = 4.3). Moreover, models that did not account for theensity of either Cf (Dbar = 2.5, pD = 2.0, DIC = 4.5) or OmDbar = 3.2, pD = 2.3, DIC = 5.6) were only somewhat worsehan the full model. However, a model that did not account forny of these predators had a DIC that was 2.6 units higher thanhe full model. We therefore make the biological inferencesased on the parameter estimates of the full model. In thisodel, we only include the habitat variable “proportion of

orest” since this habitat variable had highest explanatoryower. Also, including the other habitat variables resulted inorse models (higher DIC).

aboratory experiments

over fliesNymphs of the mirids Om and Cf and the anthocorid

n were collected in the field and starved in a fridge

5 Applied Ecology 12 (2011) 516–522

(thn(

wmTimaebriwntc

C

wVnDl

R

otoacfa(oWavmpiab2eswl

Fig. 2. Estimated parameters (standardized effect sizes) of a hierar-chical logistic regression model of the probability of occurrence ofpredatory hoverfly eggs in prey egg batches. Pv = Phratora vulgatis-sima (prey: leaf beetle), Cf = Closterotomus fulvomaculatus (lessmobile competitor: predatory mirid), Om = Orthotylus marginalis(less mobile competitor: predatory mirid), An = Anthocoris nemo-rum (mobile competitor: predatory anthocorid. The thick and thetd

7osor(tCtA(t(

tvle(Nv

D

p

20 C. Björkman et al. / Basic and

T = 6.5–7.2 ◦C) for 24 h before the experiments to increaseheir motivation to predate. To maximize their feeding rate,eteropterans in their fourth or fifth nymphal stage were used;ymphs in these stages are known to be particularly voraciousBjörkman et al. 2003).

Predation on hoverfly eggs was studied to determinehether the tendency to predate was higher in the less mobileirids Om and Cf than in the more mobile anthocorid An.he leaf beetle egg clutches with hoverfly eggs were kept

ndividually in Petri dishes (Ø 8.5 cm) containing a piece ofoist filter paper. A single predator was introduced to this

rena. The leaf beetle egg clutches differed in size (6–131ggs); the clutch sizes were evenly distributed across the threeug species. The number of eggs (leaf beetle and hoverfly)emaining after 7 h and after 24 h was recorded. The exper-ments were finished when the hoverfly egg was consumed,hen it hatched, or after 72 h, whichever occurred first. Theumber of replicates per bug species was 20. Likelihood ratioests were used to assess differences in the numbers of eggsonsumed by the different predators.

hemical analyses and weight of eggsIndividual eggs were, after being dried at 70 ◦C for 24 h,

eighed and later analyzed in an Elemental Analyzer (seeerardo, Froehlich, & McIntyre 1990) to determine their totalitrogen and carbon content as a fraction of their dry weight.ifferences between the values measured for hoverfly and

eaf beetle eggs were analyzed using t-tests.

esults

The field study showed that the probability of occurrencef hoverfly eggs clearly increased with increasing propor-ion of forest near the plot, and with increasing numbersf Pv eggs (Fig. 2). The final model also gave support forn effect of predator density, although the 95% Bayesianonfidence limits overlapped zero. There was 92% supportor a negative effect of increasing Cf (Pr(β4 < 0) = 92%),nd 94% support for a negative effect of increasing OmPr(β5 < 0) = 94%). The estimated 95% confidence intervalf the An density parameter (β6) clearly overlapped zero.e cannot differentiate between the relative importances

mong these explanatory variables since the confidence inter-als of the parameters (effect sizes) overlaps. The estimatedode and 95% Bayesian confidence limits of the intercept

arameter α were −29.7 and −77.9–26.4, respectively. Thenformation in the dataset for estimating the standard devi-tion of the random effect (

√1/τδ) was low, as reflected

y a wide confidence interval for its posterior distribution,0.3–100 with a mode of 77.6. Our conclusions about the

ffect of the explanatory variables were not sensitive to thepecified width of the prior distribution. In fact, in a modelith a narrower prior distribution (>0–10) the confidence

imits of the β-parameters were narrower.

dtah

hin horizontal lines represent the 50% and 95% Bayesian confi-ence, respectively.

The laboratory experiment showed that, after seven hours,5% of the Cf nymphs had consumed the hoverfly egg, whilenly 5% of the An and none of the Om nymphs had doneo (df = 2, χ2 = 40.6, p < 0.001). After 24 h, most of the bugsf all three species had consumed the hoverfly egg; the cor-esponding values were 95%, 71%, and 86%, respectivelydf = 2, χ2 = 4.6, p = 0.10). Put another way (albeit in a wayhat does not admit statistical analysis), the average time untilf had consumed the hoverfly egg was 7.5 h. The average

imes for Om and An were 22.0 h and 27.3 h, respectively.fter 24 h, Cf had consumed 4.0 (SE = 0.8) Pv eggs, Om 4.5

SE = 0.7) Pv eggs and An 2.2 (SE = 0.5) Pv eggs; the specieshus exhibited minor differences in their consumption ratesKruskal–Wallis test; H = 6.26, df = 2, p = 0.044).

The mean dry weight of the leaf beetle eggs was higherhan that of hoverfly eggs; mean(±SE) was 0.0496(±0.001)s. 0.0172(±0.0006) mg (t = 25.3, p < 0.001, df = 13). Theeaf beetle eggs had a higher C content than the hoverflyggs; mean(±SE) was 492.9(±8.4) vs. 403.8(±15.0) mg/gt = 5.31, p < 0.001, df = 12). The leaf beetle eggs had a higher

content than the hoverfly eggs; mean(±SE) was 85.2(±1.2)s. 79.2(±2.2) mg/g (t = 2.39, p = 0.034, df = 12).

iscussion

The results of the field study indicate that intraguildredation may be an important factor in determining the

istribution and abundance of generalist natural enemies ofhe willow leaf beetle P. vulgatissima. However, the negativessociations observed in the field may also be due to femaleoverflies being reluctant to oviposit in places with high den-

Applied

sstppot2awsosb

bvtRnoCobtiehetdoTwttcLafarbta

tnnfpthtts

daotbic

oS2cs2wioot2afl

pnflihEuedvaep

imcrbfbesnfimf

C. Björkman et al. / Basic and

ities of predatory bugs. Irrespective of the cause, the datauggest a negative interaction between hoverflies and preda-ory bugs. The laboratory experiment showed that mirids arearticularly quick to consume the eggs of potential com-etitors (i.e. hoverfly larvae), highlighting the importancef intraguild predation. The results also showed that preda-or foraging behaviour matters (cf. Rosenheim & Corbett003). Less mobile mirids that consume entire egg clutchesre stronger intraguild predators, interacting more negativelyith hoverflies, than the more mobile anthocorids that con-

ume a few eggs and move on. The probability of occurrencef hoverflies increased with both increasing proportion ofurrounding nearby forest and with increasing density of leafeetle eggs.

As expected on the basis of their different foragingehaviours, the less mobile mirids (O. marginalis and C. ful-omaculatus) were more likely to feed on the hoverfly egghan was the more active anthocorid (A. nemorum). Fréchette,ojo, Alomar, & Lucas (2007) observed a similarly strong,egative interaction between mirids and hoverflies in a studyf aphid predation. However, An is smaller than Om andf and would thus be expected to consume less than eitherf them; this may have exaggerated the observed differenceetween the species. The relatively small differences betweenhe mirids and the anthocorid observed in our study might bemportant in a theoretical or evolutionary sense if the differ-nces are consistent. From the perspective of applied ecology,owever, such small differences are less significant. Hoverflyggs are unlikely to escape consumption by any of the preda-ors; all three typically consumed the hoverfly egg within 24 hespite the surplus of alternative prey (the average numberf leaf beetle eggs presented to individual predators was 35).he experiments were conducted in Petri dishes; in the realorld, predators are not so confined and it is thus possible that

he more mobile anthocorids would be less likely to consumehe hoverfly egg than would the mirids. Furthermore, antho-orids are normally less common than mirids (Björkman &iman 2005; Dalin 2006). Thus, in the field situation it ist present not possible to quantify the relative importance oforaging behaviour and predator density on the importance ofparticular predator in intraguild predation. Ultimately, our

esults suggest that attempts to increase hoverfly numbers,y e.g. adding flowering plants or placing plantations closeo forests, may be most likely to succeed in areas with a lowbundance of mirids.

The fact that most of the specimens of all three preda-ory bug species consumed the hoverfly egg within 24 h isot necessarily indicative of an evolved behaviour to elimi-ate a potentially strong competitor; the apparent preferenceor hoverfly eggs may be due to their chemical content, thehysical properties of the egg shell, or their size. However,he smaller size and lower carbon and nitrogen contents of

overfly eggs compared to leaf beetle eggs are not consis-ent with this alternative hypothesis; these differences implyhat bugs should prefer leaf beetle eggs. We did not mea-ure the levels of defensive compounds present in the eggs;

A

E

Ecology 12 (2011) 516–522 521

ifferences in this variable can therefore not be ruled out asn explanatory factor. Although we did not measure softnessf the eggshells, we did not observe any difference betweenhe hoverfly and beetle eggs in terms of the effort exertedy the predators when penetrating the eggshells, and so its unlikely that this is the cause of the observed preferentialonsumption.

The factors that limit the distribution and abundancef hoverflies are not always well known (e.g. Sutherland,ullivan, & Poppy 2001; Meyer, Jauker, & Steffan-Dewenter009), but it has been shown that different kinds of obsta-les (e.g. hedges and long distances between patches ofuitable habitats) may limit their dispersal (Wratten et al.003). The proportion of forest in the vicinity of the plotsas positively associated with hoverfly occurrence, possibly

ndicating that the adult hoverflies avoid flying long distancesver open areas (cf. Sjödin et al. 2008). Adult hoverflies feedn flowering plants, and are responsible for the dispersal ofheir species (Haenke, Scheid, Schaefer, Tscharntke, & Thies009). The positive association between hoverfly numbersnd proximal forests may partly be due to the abundance ofowering plants in these habitats.In order to achieve effective biological control using multi-

le predators, it is important to select predator species that doot interact negatively with one-another. It seems that hover-ies have the potential to be particularly important predators

n recently harvested willow plantations, which typicallyave low densities of heteropterans (Björkman, Bommarco,klund, & Höglund 2004). The population of mirids in partic-lar is often low after harvesting because they overwinter asggs under the bark of the willows, and harvesting takes placeuring winter. The hoverflies, by contrast, overwinter as lar-ae or pupae in the ground. Thus, the hoverflies should not beffected negatively by the harvesting and mobile adult hov-rflies, which reach recently established or newly harvestedlantations, should be less exposed to intraguild predation.

In conclusion, negative interactions that probably involventraguild predation between enemies which share a com-

on prey seem to be important in willow plantations; thisonclusion is supported by both field observations and labo-atory experiments. These findings may have practical utilityecause perennials are of growing interest, especially as bio-uel crops. The findings are also particularly well-suited toiological control methods that aim at using several differ-nt predator species because their growth does not cause theort of seasonal variation in ecological processes (such asumerical responses) that is observed with annual crops. Ourndings suggest that such multi-species strategies will beost effective if they use enemy species with complementary

eeding behaviours.

cknowledgments

We thank Richard Hopkins for valuable comments, Karinklund for assistance and Tomas Grönqvist for conducting

5 Applied

tTA2

R

A

B

B

B

C

D

D

F

F

F

G

H

L

L

M

P

P

R

R

R

S

S

S

S

S

S

S

T

V

W

22 C. Björkman et al. / Basic and

he chemical analysis. The study was financially supported byhe Oscar and Lili Lamm Foundation, The Swedish Energygency and The Swedish Research Council Formas (grants005-933 to TS and 2005-1326 to CB).

eferences

rim, M., & Marquet, P. A. (2004). Intraguild predation: Awidespread interaction related to species biology. Ecology Let-ters, 7, 557–564.

jörkman, C., Bommarco, R., Eklund, K., & Höglund, S. (2004).Harvesting disrupts biological control of herbivores in ashort-rotation coppice system. Ecological Applications, 14,1624–1633.

jörkman, C., Dalin, P., & Eklund, K. (2003). Generalist natural ene-mies of a willow leaf beetle (Phratora vulgatissima): Abundanceand feeding habits. Journal of Insect Behavior, 16, 747–764.

jörkman, C., & Liman, A.-S. (2005). Foraging behaviour influ-ences the outcome of predator–predator interactions. EcologicalEntomology, 30, 164–169.

arey, M. P., & Wahl, D. H. (2010). Interactions of multiple preda-tors with different foraging modes in an aquatic food web.Oecologia, 162, 443–452.

alin, P. (2006). Habitat difference in abundance of willow leaf bee-tle Phratora vulgatissima (Coleoptera: Chrysomelidae): Plantquality or natural enemies? Bulletin of Entomological Research,96, 629–635.

alin, P., Kindvall, O., & Björkman, C. (2006). Predator forag-ing strategy influences prey population dynamics: Arthropodspredating a gregarious leaf beetle. Animal Behaviour, 72,1025–1034.

inke, D. L., & Denno, R. F. (2002). Intraguild predation dimin-ished in complex-structured vegetation: Implications for preysuppression. Ecology, 83, 643–652.

inke, D. L., & Denno, R. F. (2004). Predator diversity dampenstrophic cascades. Nature, 429, 407–410.

réchette, B., Rojo, S., Alomar, O., & Lucas, E. (2007). Intraguildpredation between syrphids and mirids: Who is the prey? Whois the predator? BioControl, 52, 175–191.

elman, A., & Hill, J. (2007). Data analysis using regressionand multilevel/hierarchical models. UK: Cambridge UniversityPress.

aenke, S., Scheid, B., Schaefer, M., Tscharntke, T., & Thies, C.(2009). Increasing syrphid fly diversity and density in sownflower strips within simple vs. complex landscapes. Journal ofApplied Ecology, 4, 1106–1114.

etourneau, D. K., Jedlicka, J. A., Bothwell, S. G., & Moreno, C. R.(2009). Effects of natural enemy biodiversity on the suppressionof arthropod herbivores in terrestrial ecosystems. Annual Review

of Ecology, Evolution and Systematics, 40, 573–592.

osey, J. E., & Denno, R. F. (1998). Positive predator–predator inter-actions: Enhanced predation rates and synergistic suppression ofaphid populations. Ecology, 79, 2143–2152.

Ecology 12 (2011) 516–522

eyer, B., Jauker, F., & Steffan-Dewenter, I. (2009). Contrastingresource-dependent responses of hoverfly richness and densityto landscape structure. Basic Applied Ecology, 10, 178–186.

olis, G. A. (1984). Age structure component of niche width andintraspecific resource partitioning – Can age-groups function asecological species? The American Naturalist, 123, 541–564.

olis, G. A., & Myers, C. A. (1989). The ecology and evolution ofintraguild predation: Potential competitors that eat each other.Annual Review of Ecology and Systematics, 20, 297–330.

ickers, S., Langek, R., & Scheu, S. (2006). Stable isotope anal-yses document intraguild predation in wolf spiders (Araneae:Lycosidae) and underline beneficial effects of alternative preyand microhabitat structure on intraguild prey survival. Oikos,114, 471–478.

osenheim, J. A., & Corbett, A. (2003). Omnivory and the inde-terminacy of predator function: Can a knowledge of foragingbehavior help? Ecology, 84, 2538–2548.

osenheim, J. A., Wilhoit, L. R., & Armer, C. A. (1993). Influ-ence of intraguild predation among generalist insect predatorson the suppression of an herbivore population. Oecologia, 96,439–449.

age, R. B., & Tucker, K. (1998). The distribution of Phratora vul-gatissima (Coleoptera: Chrysomelidae) on cultivated willows inBritain and Ireland. European Journal of Forest Pathology, 4,289–296.

jödin, N. E., Bengtsson, J., & Ekbom, B. (2008). The influenceof grazing intensity and landscape composition on the diver-sity and abundance of flower-visiting insects. Journal of AppliedEcology, 45, 763–772.

näll, T., O’Hara, R. B., & Arjas, E. (2007). A mathematical and sta-tistical framework for modelling dispersal. Oikos, 116, 966–974.

nyder, W. E., Snyder, G. B., Finke, D. B., & Straub, C. S. (2006).Predator biodiversity strengthens herbivore suppression. Ecol-ogy Letters, 9, 789–796.

piegelhalter, D. J., Best, N. G., Carlin, B. P., & van der Linde,A. (2002). Bayesian measures of model complexity and fit (withdiscussion). Journal of the Royal Statistical Society Series B, 64,583–616.

utherland, J. P., Sullivan, M. S., & Poppy, G. M. (2001). Dis-tribution and abundance of aphidophagous hoverflies (Diptera:Syrphidae) in wildflower patches and field margin habitats. Agri-cultural and Forest Entomology, 3, 57–64.

ymondson, W. O. C., Sunderland, K. D., & Greenstone, M. H.(2002). Can generalist predators be effective biocontrol agents?Annual Review of Entomology, 47, 561–594.

homas, A., O’Hara, R. B., Ligges, U., & Sturtz, S. (2006). MakingBUGS open. R News, 6, 12–17.

erardo, D. J., Froehlich, P. N., & McIntyre, A. (1990). Determina-tion of organic carbon and nitrogen in marine sediments using theCarlo Erba NA-1500 analyzer. Deep-Sea Research, 37, 157–165.

ratten, S. D., Bowie, M. H., Hickman, J. M., Evans, A. M.,

Sedcole, J. R., & Tylianakis, J. M. (2003). Field boundariesas barriers to movement of hover flies (Diptera: Syrphidae) incultivated land. Oecologia, 134, 605–611.