patch choice from a distance and use of habitat information during foraging by the parasitoid ibalia...

Ecological Entomology (2012), 37, 161–168 DOI: 10.1111/j.1365-2311.2012.01350.x

Patch choice from a distance and use of habitatinformation during foraging by the parasitoid Ibalialeucospoides

D E B O R A H F I S C H B E I N,1,2 J U L I E T A B E T T I N E L L I ,3 C A R L O SB E R N S T E I N2 and J U A N C . C O R L E Y1 1Grupo de Ecología de Insectos, Instituto Nacional de

Tecnología Agropecuaria, Estacion Experimental San Carlos de Bariloche, CC 277, Bariloche, Argentina, 2Laboratoire de

Biometrie et Biologie Evolutive, UMR 5558, Universite de Lyon, Villeurbanne, France and 3Department of Biology, University

of New Mexico, Albuquerque, New Mexico, U.S.A.

Abstract. 1. In environments in which resources are distributed heterogeneously,patch choice and the length of time spent on a patch by foragers are subject to strongselective pressures. This is particularly true for parasitoids because their host foragingsuccess translates directly into individual fitness.

2. The aim of this study was to test whether: (i) females of the parasitoid Ibalialeucospoides (Hymenoptera: Ibaliidae) can discriminate among patches according tohost numbers; (ii) the surrounding context affects the initial choice of patch, as wellas time spent on patch; and (iii) the perceived quality of a given patch is affected bythe quality of the surrounding patches.

3. Each female was randomly exposed to one of three different three-patchenvironments which differed in host number per patch, mean environment host numberand host distribution among patches. For each treatment level, the first patch chosenand the time allocated to each patch visited by the female were recorded.

4. Females of I. leucospoides were able to discriminate different levels of hostnumbers among patches from a distance. The patch bearing the highest number ofhosts was, predominantly, the first choice. Patch host number in association with meanhabitat profitability influenced the length of time spent on the first patch visited. Bycontrast, variance in habitat profitability did not influence time allocation decisions.Contrary to the study prediction, there were no significant habitat-dependent timeallocation differences among patches holding the same number of hosts.

5. The results indicate that, for I. leucospoides, patch exploitation decisions arepartially influenced by information obtained from the habitat as a whole, a behaviourthat may prove to indicate adaptive ability in highly patchy environments, as well assuggesting the presence of good cognitive abilities in this parasitoid species.

Key words. Foraging behaviour, marginal value theorem, parasitoid insects, patchdecision rules.

Introduction

Animals usually live in patchy environments in whichresources are heterogeneously distributed. In these conditions,mechanisms for resource patch choice and strategies for

Correspondence: Deborah Fischbein, Grupo de Ecología de Insec-tos, INTA EEA Bariloche, CC 277, San Carlos de Bariloche, 8400 RíoNegro, Argentina. E-mail: [email protected]

determining the length of time spent on a patch are subject tostrong selective pressures (Stephens & Krebs, 1986). This isparticularly true for parasitoids, which are insects that lay theireggs in or on other arthropods, because in these animals hostforaging success translates directly into offspring productionand thus into individual fitness. This behavioural trait makesparasitoids ideal subjects in which to study foraging decisions.As a consequence, foraging strategies, such as host patch

© 2012 The AuthorsEcological Entomology © 2012 The Royal Entomological Society 161

162 Deborah Fischbein et al.

choice and time spent on patch, and other factors influencingparasitoid foraging behaviour have been subject to significantresearch effort (see Wajnberg, 2006 for a review).

Parasitoid females frequently search for their hosts inhighly variable environments. In such settings, adaptiveforaging decisions depend on the accurate gathering anduse of information. Accordingly, parasitoids may samplepatches when searching in order to estimate the profitabilityof the current patch and of the surrounding habitat bycontinuously updating information. The use of informationfor patch exploitation has been studied vastly from boththeoretical (McNamara & Houston, 1985; Bernstein et al.,1988; Pierre et al., 2003) and experimental (Hubbard &Cook, 1978; Waage, 1979; Hemerik et al., 1993; Vos et al.,1998; Thiel & Hoffmeister, 2006; Tentelier et al., 2006;Tentelier & Fauvergue, 2007) viewpoints. Patch sampling, aninformation processing sequence, through which individualscompare a priori and a posteriori information, should helpnon-omniscient foragers to make better patch choices andusage decisions.

A great variety of environmental cues, such as chemical,visual and physical cues, are used by parasitoids as sources ofinformation for both locating and assessing host patches (Vet& Dicke, 1992; Godfray, 1994). These cues of various naturescan act as indicators of host presence, host species (Thiel &Hoffmeister, 2006) and host density (Waage, 1979; Li et al.,1997; Shaltiel & Ayal, 1998; Wang & Keller, 2004; Tentelieret al., 2005; Martínez et al., 2006, Corley et al., 2010), aswell as of the presence of competitors in the current patch(Janssen et al., 1995a,b; Bernstein & Driessen, 1996; Casteloet al., 2003). The use of such information is expected to reduceuncertainty and therefore improve foraging success.

Making patch choice decisions on the basis of expected hostavailability (i.e. estimated through patch sampling or throughstimuli discrimination from a distance) might ultimately lead toan adaptive exploitation of resources. However, the accuracy ofsuch estimates depends on different factors, such as the numberof patches already visited and the development of learningabilities. The inborn ability to estimate host availability canbe highly inaccurate and lead to inefficient decisions at earlystages in the learning process. Alternatively, the quality of theestimate can rely on the ability to respond to cues to hostdensities prior to patch exploitation (Geervliet et al., 1998;Liu et al., 2009). In many host–parasitoid systems, differentcues, such as secondary chemical compounds released byplants, visual indications of plant consumption by herbivoresand volatile kairomones released by hosts, can provide arapid, albeit rough, estimate of host availability and representthe basis of an adaptive patch choice (Vet & Dicke, 1992;Turlings & Wackers, 2004; Tentelier et al., 2005; Tentelier &Fauvergue, 2007).

Once they are on a patch, parasitoids should be able to adjustthe length of time they allocate to it in order to maximise theirlifetime reproductive success. The marginal value theorem(MVT) (Charnov, 1976), the most influential rate maximisationmodel, predicts that an optimal forager should leave a resourcepatch when the instantaneous rate of fitness gain falls below theaverage rate of gain expected for the habitat. Therefore, optimal

residence time on a patch would increase with both increasingresource availability in the patch and decreasing availability inthe habitat as a whole (i.e. habitat profitability). However, theMVT model does not suggest patch exploitation mechanismsthat foragers should employ to achieve optimal residence time.Simple behavioural rules, such as the so-called rules of thumb(Iwasa et al., 1981; McNair, 1982; Green, 1984; Stephens &Krebs, 1986), and the more complex and dynamic incremen-tal and decremental patch-leaving rules have been proposed assuch mechanisms (Waage, 1979; Driessen et al., 1995; Wajn-berg et al., 2000; van Alphen et al., 2003; Wajnberg, 2006).

The parasitoid Ibalia leucospoides Hochenwarth (Hymen-optera: Ibaliidae) is a solitary, koinobiont and nearly pro-ovigenic parasitoid (i.e. with an ovigeny index of 0.77; D.Fischbein, unpublished data, 2011) that attacks eggs andfirst-instar larvae of the woodwasp Sirex noctilio Boidin(Hymenoptera: Siricidae) (Chrystal, 1930; Madden, 1968;Spradbery, 1974). Woodwasps are primitive xylophagousinsects that attack pine trees. Sirex noctilio is native to Mediter-ranean Europe, but over the last century has successfullyinvaded Australia, New Zealand, South Africa, South Amer-ica and, more recently, North America (Hoebeke et al., 2005).In most regions in which S. noctilio has established, it hasrapidly become an important pest of pine tree forestations,mainly as a result of its outbreak population dynamics, duringwhich tree mortality can be severe (Corley et al., 2007). Ibalialeucospoides is one of several biocontrol agents adopted forthe purposes of pest management of woodwasp populations(Hurley et al., 2007; Corley & Bruzzone, 2009). The para-sitoid, also native to Europe, was introduced into Australasiain the early 1960s, since when it has established throughoutthe invasion range of S. noctilio, mostly through accidentalintroductions together with its host (Madden, 1988). In fieldconditions, I. leucospoides may parasitise up to 40% of itshosts.

Because of its applied importance, there is a growingresearch effort on this parasitoid. Most studies have focusedon its host location and patch use behaviour. Together withits eggs, the host wasp injects spore of its symbiotic fungusAmylostereum areolatum into pine trees. Then, woodwasplarvae develop and grow inside these trees by feeding on wooddecomposed by the fungus (Madden, 1981). The chemicalinformation derived from the host fungal symbiont is used byparasitoids during host searching and may provide informationon host presence (Madden, 1968; Spradbery, 1974) and onthe relative densities of hosts on patches (Martínez et al.,2006). There is also evidence to suggest that I. leucospoideshas a type III functional response to host density in pinelogs (Fernandez-Arhex & Corley, 2005) and that interferencecan occur when two females forage for a host in the samepatch in simplified experimental conditions (Fernandez-Arhex& Corley, 2010). To date, not many attempts have been madeto evaluate host foraging behaviour by this parasitoid in a morenatural, multiple patch environment (Corley et al., 2010).

Whereas pine plantations are generally characterised bya regular spatial arrangement, trees attacked by S. noctilioare typically aggregated, especially during the longlast-ing, endemic population phase (Corley et al., 2007). The

© 2012 The AuthorsEcological Entomology © 2012 The Royal Entomological Society, Ecological Entomology, 37, 161–168

Host foraging behaviour of Ibalia leucospoides 163

distribution of attacks by S. noctilio within these clumps showsdifferent degrees of heterogeneity, whereby clusters of attackedtrees can show low or high degrees of variance in the num-ber of hosts per tree, which can range from a few individualsto several hundred woodwasp larvae. During outbreak peri-ods, overall infestation levels can be high, affecting mosttrees (≥80%) and rendering spatial distribution less hetero-geneous. Consequently, the abundance and spatial distributionof S. noctilio can vary not only among plantations, but withinstands, and in the course of a single flight season as well as insubsequent generations, resulting in varying levels of hetero-geneity. In this context, female I. leucospoides must deal withchanges in both mean and variance habitat profitability.

This study tested the hypothesis that parasitoids choosehost patches and adjust patch exploitation times accordingto different levels of host abundance and distribution amongattacked trees. This hypothesis leads to various accompanyingpredictions. Firstly, female parasitoids are likely to assesspatch profitability from a distance and, accordingly, to choosethe best patch within a local environment, whatever thesurrounding habitat characteristics may be. Secondly, a positiverelationship between patch residence time and host numbersshould emerge and the length of time allocated to patcheswill depend on the characteristics of the surrounding habitat.Therefore, parasitoids that experience local environments withdifferent mean host numbers but similar host distributionamong attacked trees (i.e. similar variance in host numbersper patch) will allocate more time to patches set in a poorerenvironment than to those in a richer one. In the samemanner, parasitoids that experience local environments withthe same mean host numbers but different host distributionamong attacked trees will allocate their time among patchesmore equally in line with the decreasing heterogeneity ofthe environment (i.e. more similar host numbers per patch).Finally, a given patch with an absolute abundance of hostswill have higher relative profitability for the parasitoid whenthis patch is placed in poor habitats than in richer ones and,hence, will be exploited more intensively in the former context.

This study was focused on individual decision making byfemale parasitoids that had arrived at an aggregate of host-attacked trees. Accordingly, predictions were tested in threedifferent three-patch environments characterised by differentcombinations of means and variances in habitat profitability.Host patches in the experimental set-up were recreated usingpine tree logs infested in a controlled manner; the first patchcontacted and the time allocated by parasitoids to each patchvisited were analysed. Thus, the aim of this study was totest whether: (i) I. leucospoides females are able to perceivedifferences in patch host numbers from a distance as indicatedby their selection of the best patch as their first choice; (ii)the surrounding context affects the choice of patch as wellas the time spent on patch; and (iii) the perceived quality(quality rating) of a given patch is affected by the quality ofthe surrounding patches.

Materials and methods

Host and parasitoid wasps used in this study were obtainedfrom pine (Pinus contorta) logs collected in the field, at severalheavily attacked plantations located in northwest Patagonia,Argentina (42◦02′S, 71◦56′W). Once felled, trees were cutinto 1-m logs and kept individually in locker-type cages underindoor conditions until insect emergence. Each morning, newlyemerged parasitoid females were collected from the cagesand immediately placed in individual plastic vials (251 cm3)

for 7 days in a common chamber, free from host odours(temperature 23 ± 1 ◦C, RH 53%, LD 16:8 h). This time spanwas chosen to combine practical purposes (i.e. the matching ofinsects with the experimental set-up) with the use of middle-aged, more representative individuals. All wasps were virginsand were given unlimited access to a diluted honey solution(30% honey in distilled water) from emergence. On the dayprior to the experiment, food was removed and replaced withdistilled water only.

Experimental design

The aims of the experiment were to assess the abilityof I. leucospoides females to detect the best patch of threeoffered from a distance and to establish whether patchresidence time is proportional to host availability. The studyalso sought to establish whether mean host abundance inthe local environment and host distribution among patchesinfluence patch exploitation behaviour. For this purpose,female parasitoids were individually assigned at random toone of three different three-patch environments. The settingsdiffered in host numbers at the individual log level (i.e. patch),in mean environment host numbers (the three logs), as wellas in host distribution among patches (i.e. variance in hostnumbers per log). The settings are hereafter referred to ashabitats LM-HV (low mean host numbers, high variance inhost numbers), HM-LV (high mean host numbers, low variancein host numbers) and HM-HV (high mean host numbers, highvariance in host numbers) (Table 1). The first host patch chosen(i.e. the first patch contacted by a parasitoid), subsequentpatch visits and the time allocated to each patch visited wererecorded as response variables. Therefore, if parasitoids areable to assess patch profitability without making direct contactwith host patches, the patch with higher host numbers shouldbe selected as their first choice, regardless of surroundinghabitat characteristics. Additionally, if parasitoids are ableto adapt their residence time in patches according to thesurrounding patches, residence time should be longer in thepoorer (LM-HV) than in the richer (HM-HV) habitat. Inaddition, if parasitoids can adjust their current patch timeallocation to neighbouring patches, the time spent on patchesshould increase in similarity as the distribution of hosts amongpatches decreases in heterogeneity (e.g. HM-LV vs. HM-HV).Moreover, if parasitoids use the relative profitability of patchesto adjust patch exploitation times, patches with similar absolutehost numbers should be visited for less time when they arelocated in rich (HM-LV and HM-HV) than in poor (LM-HV)habitats.



Table 1. Females of the parasitoid Ibalia leucospoides were individually assigned to one of three different three-patch environments (habitatsLM-HV, HM-LV and HM-HV).

Patch host numbers

n Low Medium HighMean environmenthost number

Host distributionamong patches (vc∗)

Habitat LM-HV 12 1 8 15 8 0.87Habitat HM-LV 11 10 15 20 15 0.33Habitat HM-HV 13 2 15 28 15 0.87

∗vc, the variation coefficient, was used as a relative measure of variance in host distribution among patches (i.e. the ratio between the standarddeviation of the mean environment host number and mean environment host number).The environments differed in individual patch host numbers, mean environment host number and host distribution among patches (vc).LM-HV, low mean host numbers, high variance in host numbers; HM-LV, high mean host numbers, low variance in host numbers; HM-HV, highmean host numbers, high variance in host numbers.

Because of the short duration of the insect emergenceseason (2 months approximately), and the time-consuminglogistics associated with the experimental set-up (see below),completion of the research in a single season was unfeasible.The experiments were thus carried out in two different years,during daytime hours (11.00–20.00 hours) and at 23 ± 1 ◦C.During the first year, five, five and six replicates of the LM-HV, HM-LV and HM-HV habitat set-ups, respectively, werecarried out. A further seven, six and seven replicates wereadded for each habitat scenario, respectively, during the secondexperimental year.

In order to create a symmetrical environment, three logswere placed in the corners of an imaginary isosceles triangle(30 cm on each side) inside a wire mesh cage (1 m3). Toprovide host patches, ‘clean’ (i.e. free from woodwasp attacks)pine logs, 0.8 m in length, were cut and allowed to dry atambient temperatures for 10 days to ensure appropriate woodmoisture conditions for woodwasp oviposition. Logs were thenexposed to woodwasp females until the desired number ofovipositions had been achieved. Logs were then stored foranother 10 days before the experiments to ensure that hostdevelopment and fungal growth were suitable and attractiveto I. leucospoides females. Data on the number of hosts perlog (Table 1) were obtained by observing female woodwaspscontinuously and tallying each insertion of the ovipositor intothe log. The number of host eggs laid was estimated accordingto Madden (1974). The position of a given log within the arraywas set at random.

A female wasp was introduced at the exact centre ofthe arrangement. After a 5-min adaptation period duringwhich the wasp was kept inside a perforated plastic vial,the wasp was gently released and the trial initiated. In eachreplicate of the experiment, both the parasitoids and logs usedwere replaced. Wasps were observed continuously during anexperiment. Patch residence times were recorded using a hand-held stopwatch. Although off-patch short excursions duringhost patch visits are not common in I. leucospoides, the endof a patch visit was arbitrarily defined as the point at whicha wasp left the patch and remained off it for 20 min. Theexperiment was considered to have ended when, having left apatch and landed elsewhere, the wasp remained off any patchfor ≥30 min.

Data analysis

A multinomial logit model was fitted to analyse the effectsof the surrounding context on the first patch chosen. Theinitial model considered patch chosen (a qualitative three-level factor: high, medium, low) as the response variable, andhabitat (a qualitative three-level factor: LM-HV, HM-LV, HM-HV) and year as explanatory variables. Starting with the mostcomplex model, patch chosen = habitat |year (the latter termrepresents the sum of the effects of the two-way interaction andthe two single variables), the non-significant factors and theinteraction between factors were progressively removed untila minimal appropriate model was obtained. Model comparisonswere computed using the standard likelihood method (Faraway,2006). To test the hypothesis that the females chose logs atrandom, a G test for goodness of fit was carried out (Sokal &Rohlf, 1981).

The effects of host numbers in a patch and the habitatas a whole on time allocated to the patch visited wereanalysed using a generalised linear model assuming a gammadistribution of residuals and an inverse link function. The patchhost number (a quantitative variable in this case, representingthe number of hosts within the patch), the habitats (LM-HV,HM-LV and HM-HV) and year were introduced in the modelas explanatory variables. A backward procedure was used toremove non-significant factors and interactions between factorsin order to select the final model. Model comparisons werecomputed using the standard likelihood method. Residualswere examined to confirm that the final model accurately fittedthe data. To test the effect of habitats on time assigned to apatch holding 15 hosts, when this patch was selected as afirst choice, a generalised linear model based on an inverselink function and a gamma distribution was used. All dataanalyses were performed using the R statistical environment(R Development Core Team, 2011).

Results

Patch choice

The analysis of the first patch chosen out of the threeoffered showed no significant interaction between habitat and



year (χ2 = 8.49, d.f. = 4, P = 0.07). Additionally, and aspredicted, the first patch chosen by I. leucospoides femaleswas selected independently of habitat (χ2 = 6.84, d.f. = 4,P = 0.14) and year (χ2 = 2.12, d.f. = 2, P = 0.34).However, the results show that parasitoids were able to assesspatch profitability without requiring direct contact with hostpatches by showing a propensity to alight on and exploitthe patch bearing the highest number of hosts (χ2 = 17.96,d.f. = 2, P < 0.001) (Fig. 1).

The influence of patch host number and habitat on patchresidence time

Only six of a total of 36 wasps visited more than one patch,irrespective of the local environment. Half of these waspsoriented directly to the best patch, exploited it and then movedto a subsequent patch. The time allocated to each patch visitedtended to be positively related to host numbers on the patch.The remaining three wasps made a first, short visit to poorerpatches and then moved to the patch with the highest number ofhosts, in which they stayed and which they exploited. As onlya limited number of wasps visited more than one patch, it wasdifficult to analyse data adequately in terms of patch residencetime on all patches and therefore all statistical analysis wasfocused on patch residence time on the first host patch chosen.

Consistent with the study predictions, the time allocatedto the exploitation of the first host patch visited increasedwith increasing patch host numbers (χ2 = 12.61, d.f. = 1,P < 0.0001). In addition, patch residence time was signif-icantly affected by the interaction between host number in apatch and habitat (LM-HV, HM-HV, HM-LV; χ2 = 7.79,d.f. = 2, P < 0.0001). We attempted to understand this sta-tistically significant interaction by comparing habitats accord-ing to their mean and variance in profitability (see below).

When habitat LM-HV was compared with habitat HM-HV,results suggested that parasitoids may use the relative prof-itability of patches to adjust their patch exploitation times.

patch host number

High Medium Low

Num

ber

of fe

mal

e w

asps

0

5

10

15

20

25

Fig. 1. Number of female wasps of Ibalia leucospoides that chosea given host patch for the first time, among the three patchessimultaneously offered, as a function of patch host number (high,medium, low).

Patch residence time was significantly affected by the interac-tion between host number in a patch and habitat (χ2 = 2.60,d.f. = 1, P = 0.01). Therefore, female wasps were able tostay longer on patches (specifically, see patch containing 15hosts; Fig. 2) in LM-HV conditions than in HM-HV condi-tions. Patches with different absolute numbers of hosts, butwith the same relative profitability in habitat LM-HV andHM-HV, were assigned exploitation times according to theirrelative value (i.e. quality rating) (Fig. 2). However, patch res-idence time increased with the number of hosts on the patch(χ2 = 13.06, d.f. = 1, P < 0.0001).

When habitat HM-LV was compared with habitat HM-HV,the interaction between host number in a patch and habitatwas significant (χ2 = 3.80, d.f. = 1, P < 0.01). However,this probably occurred as a consequence of the fact thatonly a single wasp (that in habitat HM-LV) visited the patchcontaining 10 hosts and allocated a disproportionate amountof time to it compared with the time allocated by the otherwasps to patches of comparable richness. When the individualthat had visited the patch bearing 10 hosts was removedfrom the analysis, the interaction between host number inthe patch and habitat was no longer significant for habitatsHM-LV and HM-HV (χ2 = 0.39, d.f. = 1, P = 0.38), and,contrary to the study prediction, habitat (i.e. variance inhost numbers per patch) did not affect patch residence time(χ2 = 0.29, d.f. = 1, P = 0.52). Nonetheless, time spent onthe first patch visited increased with host numbers in that patch(χ2 = 11.98, d.f. = 1, P < 0.0001).

To further study the use of patch relative profitability toadjust patch exploitation times, differences in the time assignedto patches holding 15 hosts when these patches were selectedas first choice were analysed (these patches were included inthe LM-HV, HM-LV and HM-HV habitats). In a manner thatis partially consistent with the study prediction, females tended

patch host number

1 2 8 10 15 20 28

Pat

ch r

esid

ence

tim

e (m

in)

0

100

200

300

400

500

Fig. 2. Patch residence times (mean ± standard error) on the firstpatch visited as a function of patch host number, for Ibalialeucospoides females exposed to different environmental conditions.

, habitat LM-HV (low mean host numbers, high variance in hostnumbers); , habitat HM-LV (high mean host numbers, low variancein host numbers); , habitat HM-HV (high mean host numbers, highvariance in host numbers).



Habitat

LM-HV HM-LV HM-HVPat

ch r

esid

ence

tim

e on

pat

ches

of f

iftee

n ho

sts

(min

)

0

20

40

60

80

100

120

140

Fig. 3. Patch residence times (mean ± standard error) on patches of15 hosts chosen as first options in habitats LM-HV, HM-LV or HM-HV. LM-HV, low mean host numbers, high variance in host numbers;HM-LV, high mean host numbers, low variance in host numbers; HM-HV, high mean host numbers, high variance in host numbers.

to stay on the patch containing 15 hosts longer when thispatch was located in the poorer habitat [mean ± standard error(SE) in habitat LM-HV: 114.10 ± 14.63 min (n = 10)] thanwhen it was placed in the richer habitat [mean ± SE in habitatHM-LV: 89.00 ± 36.35 min (n = 6); mean ± SE in habitatHM-HV: 61.33 ± 18.47 min (n = 3)] (Fig. 3). However, thedifferences among habitats were not significant (χ2 = 0.86,d.f. = 2, P = 0.37). The years in which the experimentswere performed had no significant effect on any responsevariable analysed.

Discussion

Results show that I. leucospoides females may alight on andexploit, firstly, logs holding the highest number of hosts. Thisis particularly remarkable given that the first selection occursfrom a distance. Once on the patch, the time allocated to theexploitation of the first host patch visited depended on hostnumber in the patch in association with habitat profitability.This finding suggests that exploitation decisions may beinfluenced by information obtained from the surroundingpatches.

Patch choice decisions

The most striking finding in this study is that I. leucospoideswas capable of responding to differences in host patchquality without needing to make direct contact with logsin order to assess their profitability. Ibalia leucospoidesseems to do this using chemical cues derived from the hostfungal symbiont (Madden, 1968; Martínez et al., 2006). Asovipositing woodwasps may disturb tree growth during theirattacks, through a phytotoxic substance and fungus associatedwith oviposition, it is likely that tree location by foraging

parasitoids follows volatile cues emitted by stressed trees, suchas monoterpenes (α- and β-pinene) (Madden, 1988). Odourcues derived mainly from the host symbiotic fungus probablyhelp foraging wasps to optimise patch choice decisions evenbefore they reach the patch (Martínez et al., 2006; Corleyet al., 2010). However, we cannot discard the role played byvolatiles derived from live but stressed trees in the field inparasitoid attraction and patch choice.

Choosing the best of three nearby patches suggests, fromone perspective, proportionality between odour concentrationand host number. Moreover, it requires at least a given abilityto appraise several patches in the local environment and thecapability to detect differences in volatile cues. It is generallyassumed that parasitoids need to sample their environmentfirst, mostly by making contact with host patches, in orderto assess its profitability and make decisions (Hubbard &Cook, 1978; Waage, 1979; Driessen et al., 1995). However,the present results suggest that I. leucospoides is able to makehost-searching decisions by assessing initial host availabilityin patches, without the need for direct contact. In addition,assessment ability and patch choice in this parasitoid did notdiffer among habitats (i.e. independently of the characteristicsof the habitat into which they were released, wasps tended toselect the best log first), although at this stage we cannot ruleout the possibility that this apparent lack of difference maybe the consequence of a lack of power of our tests caused bysmall sample sizes.

In I. leucospoides, the strategy of choosing and stayinglonger in the best patch may result in a better outcomethan a strategy of engaging in a process of sampling andcontinuous updating. A hypothetical explanation of the strategyof choosing a single patch must involve a highly variableenvironment. In pine plantations, S. noctilio densities and theirspatial distribution among trees are known to vary, even duringpopulation outbreaks (Corley et al., 2007). In these conditions,it is possible that a host-infested tree, within the aggregationof attacked trees, bears several to hundreds of host larvae,hence surpassing the parasitoid egg complement. Thus, forparasitoids, the ability to assess patch quality from a distanceand respond accordingly by moving towards the best patchwould be valuable: firstly, it may result in a time-savingstrategy, and, secondly, making an appropriate choice givesthe female parasitoid the chance to lay more eggs in a singletree with a high density of hosts. By making accurate choicesand thoroughly exploiting a patch, I. leucospoides may protectitself against failure to find another good host patch, mortalityduring travel, and losses in terms of energy budget. It isalso true that individual offspring production per patch canbe independent of the number of hosts per patch (Tentelieret al., 2008). In the wild, a low number of eggs laid by afemale per patch in relation to the number of hosts availablemay occur as a result of either strong predation pressure orparasitoid redistribution among patches.

Patch residence time

Under the experimental conditions considered here, thefirst patch chosen by I . leucospoides was probably exploited



according to mean habitat profitability. Parasitoids may usethe relative profitability of patches to adjust their patchexploitation times, but patch residence time also increaseswith the number of hosts in the patch. By contrast, variancein habitat profitability seems to have no influence on timeallocation decisions. In accordance with the predictions ofsome theoretical studies (McNamara & Houston, 1985, 1987;Vos & Hemerik, 2003), the present results suggest that waspsmay use the information available from nearby patches to makepatch-leaving decisions. Additionally, the results qualitativelyagreed with the general MVT predictions in that patchresidence times by parasitoids increased with increasing hostnumber. The increase in patch residence time may occur inconsequence to a response of I. leucospoides to concentrationsof host chemical cues.

Foraging theory predicts that the time allocated to a patchwith a given host density depends upon the particular hostenvironment. Thus, as habitat profitability increases, residencetimes on a patch of particular host availability should decrease(Charnov, 1976). Although we found that the number of hostsin the patch determined the time allocated to the first patchchosen in association with mean habitat profitability, we didnot observe a statistically significant habitat-dependent timeallocation difference with those patches bearing 15 hosts. Thisapparent mismatch is probably a consequence of the low powerof the statistical test (low sample size) and not of parasitoidbehaviour. Note that female wasps tended to spend more timeon the patch with 15 hosts when this patch was within thepoorer habitat (LM-HV) than when it was in the richest habitat(HM-HV).

In this study, the inclusion of an environment with lowmean habitat profitability and low variance in host numbersper patch would have facilitated a factorial design. However,an environment that strictly follows these characteristics isdifficult to design. Such an environment would have required amean host number (for the environment) of eight with patchesbearing different host numbers whilst conserving a variationcoefficient of 0.33. An example of such a setting would includepatches with six, eight and ten hosts. It is very unlikely that,in this or similar scenarios, these patches would be perceivedas different by I. leucospoides females.

This study shows the relevance of quantitative differencesin volatile-based cues and the roles they play in the processof patch selection. Once on a patch, animals may well useor overlook information about habitat characteristics. In thisstudy, I. leucospoides showed a strong response to patch hostabundance and the probable use of habitat information, butwhether this leads to an increase in reproductive successrequires further investigation. In any case, the ability to respondto differences in host numbers on patches is of great importancebecause it may indicate how well I. leucospoides individualsmatch their foraging effort to host availability.

Acknowledgements

We acknowledge financial support from the Agencia Nacionalde Promocion Científica y Tecnologica (ANPCyT), Argentina

(PICT 0-1200/06 and PICT 2010-1775), Centre National dela Recherche Scientifique (CNRS), France (PICS 4144) andInstituto Nacional de Tecnología Agropecuaria, Argentina, andwe thank two anonymous reviewers for their helpful commentson the manuscript.

References

van Alphen, J.J.M., Bernstein, C. & Driessen, G. (2003) Informationacquisition and time allocation in insect parasitoids. Trends inEcology & Evolution, 18, 81–87.

Bernstein, C. & Driessen, G. (1996) Patch-marking and optimal searchpatterns in the parasitoid Venturia canescens. Journal of AnimalEcology, 65, 211–219.

Bernstein, C., Kacelnik, A. & Krebs, J.R. (1988) Individual decisionsand the distribution of predators in a patchy environment. Journalof Animal Ecology, 57, 1007–1026.

Castelo, M.K., Corley, J.C. & Desouhant, E. (2003) Conspecificavoidance during foraging in Venturia canescens (Hymenoptera:Ichneumonidae): the roles of host presence and conspecific densities.Journal of Insect Behavior, 16, 307–318.

Charnov, E.L. (1976) Optimal foraging: the marginal value theorem.Theoretical Population Biology, 9, 129–136.

Chrystal, R.N. (1930) Studies of the Sirex Parasites, Oxford ForestryMemories No. 11. Oxford University Press, London, U.K.

Corley, J.C. & Bruzzone, O.A. (2009) Delayed emergence and thesuccess of parasitoids in biological control. Biological Control, 51,471–474.

Corley, J.C., Villacide, J.M. & Bruzzone, O.A. (2007) Spatial dynam-ics of a Sirex noctilio woodwasp population within a pine plan-tation in Patagonia. Entomología Experimentalis et Applicata, 125,231–236.

Corley, J.C., Villacide, J.M. & van Nouhuys, S. (2010) Patch timeallocation by the parasitoid Ibalia leucospoides (Hymenoptera:Iballidea): the influence of conspecifics, host abundance and distanceto the patch. Journal of Insect Behaviour, 23, 431–440.

Driessen, G., Bernstein, C., van Alphen, J.J.M. & Kacelnik, A. (1995)A count-down mechanism for host search in the parasitoid Venturiacanescens. Journal of Animal Ecology, 64, 117–125.

Faraway, J.J. (2006) Extending the Linear Model with R. Chapman &Hall, Boca Raton, Florida; London, U.K.

Fernandez-Arhex, V. & Corley, J.C. (2005) The functional responseof Ibalia leucospoides (Hymenoptera: Ibaliidae), a parasitoid ofSirex noctilio (Hymenoptera: Siricidae). Biocontrol Science andTechnology, 15, 207–212.

Fernandez-Arhex, V. & Corley, J.C. (2010) The effects of patchrichness on con-specific interference in the parasitoid Ibalia leu-cospoides (Hymenoptera: Ibaliidae). Insect Science, 17, 379–385.

Geervliet, J.B.F., Ariens, S., Dicke, M. & Vet, L.E.M. (1998) Long-distance assessment of patch profitability through volatile info-chemicals by the parasitoids Cotesia glomerata and C. rubecula(Hymenoptera: Braconidae). Biological Control, 11, 113–121.

Godfray, H.C.J. (1994) Parasitoids. Behaviour and EvolutionaryEcology. Princeton University Press, Princeton, New Jersey.

Green, R.F. (1984) Stopping rules for optimal foragers. AmericanNaturalist, 123, 30–40.

Hemerik, L., Driessen, G. & Haccou, P. (1993) Effects of intra-patchexperiences on patch time, search time and searching efficiency ofthe parasitoid Leptopilina clavipes. Journal of Animal Ecology, 62,33–44.

Hoebeke, E.R., Haugen, D.A. & Haack, R.A. (2005) Sirex noctilio:discovery of a Palearctic siricid woodwasp in New York. Newsletterof the Michigan Entomological Society, 50, 24–25.



Hubbard, S.F. & Cook, R.M. (1978) Optimal foraging by parasitoidwasps. Journal of Animal Ecology, 47, 593–604.

Hurley, B.P., Slippers, B. & Wingfield, M.J. (2007) A comparison ofcontrol results for the alien invasive woodwasp, Sirex noctilio, inthe southern hemisphere. Agricultural and Forest Entomology, 9,159–171.

Iwasa, Y., Higashi, M. & Yamamura, N. (1981) Prey distribution as afactor determining the choice of optimal foraging strategy. AmericanNaturalist, 117, 710–723.

Janssen, A., Van Alphen, J.J.M., Sabelis, M.W. & Bakker, K. (1995a)Odour-mediated avoidance of competition in Drosophila para-sitoids: the ghost of competition. Oikos, 73, 356–366.

Janssen, A., Van Alphen, J.J.M., Sabelis, M.W. & Bakker, K. (1995b)Specificity of odour-mediated avoidance of competition in Dro-sophila parasitoids. Behavioral Ecology and Sociobiology, 36,229–235.

Li, C., Roitberg, B.D. & Mackauer, M. (1997) Effect of contactkairomone and experience on initial giving-up time. EntomologiaExperimentalis et Applicata, 84, 101–104.

Liu, Q.Y., Thiel, A. & Hoffmeister, T.S. (2009) Odour-mediated patchchoice in the parasitoid Venturia canescens: temporal decisiondynamics. Entomologia Experimentalis et Applicata, 132, 110–117.

Madden, J.L. (1968) Behavioural responses of parasites to thesymbiotic fungus associated with Sirex noctilio F. Nature, 218,189–190.

Madden, J.L. (1974) Oviposition behaviour of the woodwasp Sirexnoctilio F. Australian Journal of Zoology, 22, 341–351.

Madden, J.L. (1981) Egg and larval development in the woodwaspSirex noctilio. Australian Journal of Zoology, 29, 493–506.

Madden, J.L. (1988) Sirex in Australasia. Dynamics of ForestInsect Populations: Patterns, Causes and Implications (ed. byA. A. Berryman), pp. 407–429. Plenum Press, New York, NewYork.

Martínez, A., Fernandez-Arhex, V. & Corley, J.C. (2006) Chemicalinformation from the fungus Amylostereum aerolatum and host for-aging behaviour in the parasitoid Ibalia leucospoides. PhysiologicalEntomology, 31, 336–340.

McNair, J.M. (1982) Optimal giving-up time and the marginal valuetheorem. American Naturalist, 119, 511–529.

McNamara, J.M. & Houston, A.I. (1985) Optimal foraging andlearning. Journal of Theoretical Biology, 117, 231–249.

McNamara, J.M. & Houston, A.I. (1987) Memory and the efficient useof information. Journal of Theoretical Biology, 125, 385–395.

Pierre, J.S., van Baaren, J. & Boivin, G. (2003) Patch leaving decisionrules in parasitoids: do they use sequential decisional sampling?Behavioral Ecology and Sociobiology, 54, 147–155.

R Development Core Team (2011). R: A language and environmentfor statistical computing. R Foundation for Statistical Computing,Vienna, Austria [WWW document]. URL http://www.R-project.org/[accessed on 4 September 2011].

Shaltiel, L. & Ayal, Y. (1998) The use of kairomones for foragingdecisions by an aphid parasitoid in small host aggregations.Ecological Entomology, 23, 319–329.

Stephens, D.W. & Krebs, J.R. (1986) Foraging Theory. PrincetonUniversity Press, Princeton, New Jersey.

Sokal, R.R. & Rohlf, F.J. (1981) Biometry: The Principles andPractices of Statistics in Biological Research. W.H. Freeman, NewYork, New York.

Spradbery, J.P. (1974) The responses of Ibalia species (Hymenoptera:Ibaliidae) to the fungal symbiontes of siricid woodwasp hosts.Journal of Entomology, 48, 217–222.

Tentelier, C. & Fauvergue, X. (2007) Herbivore-induced plant volatilesas cues for habitat assessment by a foraging parasitoid. Journal ofAnimal Ecology, 76, 1–8.

Tentelier, C., Wajnberg, E. & Fauvergue, X. (2005) Parasitoids useherbivore-induced information to adapt patch exploitation behaviour.Ecological Entomology, 30, 739–744.

Tentelier, C., Desouhant, E. & Fauvergue, X. (2006) Habitat assess-ment by parasitoids: mechanisms for patch use behaviour. Behav-ioral Ecology, 17, 515–521.

Tentelier, C., Guillemaud, T., Ferry, F. & Fauvergue, X. (2008)Microsatellite-based parentage analysis reveals non-ideal free dis-tribution in a parasitoid population. Molecular Ecology, 17,2300–2309.

Thiel, A. & Hoffmeister, T.S. (2006) Selective information use inparasitoid wasps. Animal Biology, 56, 233–245.

Turlings, T.C.J. & Wackers, F.L. (2004) Recruitment of predatorsand parasitoids by herbivore-injured plants. Advances in InsectChemical Ecology (ed. by R. T. Carde and J. G. Millar), pp. 21–75.Cambridge University Press, Cambridge, U.K.

Vet, L.E.M. & Dicke, M. (1992) Ecology of infochemical useby natural enemies in a tritrophic context. Annual Review ofEntomology, 37, 141–172.

Vos, M. & Hemerik, L. (2003) Linking foraging behaviour to lifetimereproductive success for an insect parasitoid: adaptation to hostdistributions. Behavioral Ecology, 14, 236–245.

Vos, M., Hemerik, L. & Vet, L.E.M. (1998) Patch exploitation by theparasitoids Cotesia rubecula and Cotesia glomerata in multi-patchenvironments with different host distributions. Journal of AnimalEcology, 67, 774–783.

Waage, J.K. (1979) Foraging for patchily distributed hosts by theparasitoid, Nemeritis canescens. Journal of Animal Ecology, 48,353–371.

Wajnberg, E. (2006) Time allocation strategies in insect parasitoids:from ultimate predictions to proximate behavioural mechanisms.Behavioral Ecology and Sociobiology, 60, 589–611.

Wajnberg, E., Fauvergue, X. & Pons, O. (2000) Patch leaving decisionrules and the marginal value theorem: an experimental analysis anda simulation model. Behavioral Ecology, 6, 577–586.

Wang, X.G. & Keller, M.A. (2004) Patch-time allocation by theparasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae).III. Effects of kairomone sources and previous parasitism. Journalof Insect Behavior, 17, 761–776.

Accepted 19 February 2012


patch choice from a distance and use of habitat information during foraging by the parasitoid ibalia...

Documents