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Basic and Applied Ecology 8 (2007) 66—74

1439-1791/$ - sdoi:10.1016/j.

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Spatial patterns of host exploitation in a larvalparasitoid of the predatory dusky large blueMaculinea nausithous

Christian Anton�, Martin Musche, Josef Settele

UFZ, Center for Environmental Research, Department of Community Ecology, Theodor-Lieser-Str. 4,06120 Halle, Germany

Received 9 November 2005; accepted 9 March 2006

KEYWORDSForaging behaviour;Host refuge;Neotypus melanoce-phalus;Patch size;Population density

ee front matter & 2006baae.2006.03.006

ing author. Tel.: +49 345ess: christian.anton@uf

SummaryThe foraging behaviour of the parasitoid wasp Neotypus melanocephalus and factorsaffecting parasitism at the population level were studied. This specialised parasitoidattacks caterpillars of the butterfly Maculinea nausithous, which sequentially feedon the plant Sanguisorba officinalis and specific red Myrmica ants. Among M.nausithous populations, there is considerable variation in caterpillar densities. Atlow M. nausithous densities, foraging might be time consuming for N. melanoce-phalus. High host densities may not always be advantageous to foraging parasitoidsdue to the caterpillars’ frequent overexploitation of ant resources and subsequentdensity-dependent mortality. In order to disperse progeny, we hypothesised that N.melanocephalus should search in a non-random way at the level of the micro-habitat, i.e., single flower heads of S. officinalis. Our analysis of 32 naturalpopulations in the Upper Rhine valley in Germany did not show a density-dependentrelationship between M. nausithous caterpillars and parasitism. Furthermore,habitat parameters like patch size and density of the host’s food plant did notaffect the parasitism rate. Foraging N. melanocephalus females preferred to searchon large flower heads. They probed host-occupied flower heads only, visiting non-host-exploited flower heads only briefly. Time spent on a flower head wasindependent of the number of caterpillars per flower head. This study indicatesthat N. melanocephalus increases its foraging efficiency by preferring large flowerheads that were previously shown to contain more host caterpillars than small flowerheads. Furthermore, oviposition increases the likelihood of continuing to search on aflower head, which is an adaptive strategy for parasitoids foraging for aggregatedhosts. However, many host-occupied flower heads were not probed byN. melanocephalus. We discuss the possibility that temporal host refuges of

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5585310; fax: +49 345 5585329.z.de (C. Anton).

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Patterns of parasitism in the predatory Maculinea nausithous 67

M. nausithous caterpillars might contribute to heterogeneity of parasitism, and whyspreading offspring might constitute a suitable strategy for a parasitoid of an ant-parasitic butterfly.& 2006 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.

ZusammenfassungIn dieser Studie untersuchten wir das Parasitierungsverhalten der Wespe Neotypusmelanocephalus sowie Parasitierungsmuster auf Populationsniveau. Neotypus mel-anocephalus parasitiert Raupen des Schmetterlings Maculinea nausithous, dessenLebenszyklus durch eine herbivore Phase in Blutenkopfen von Sanguisorba officinalisund eine rauberische Phase in Myrmica-Ameisennestern gekennzeichnet ist. DieDichte von M. nausithous schwankt stark zwischen Standorten. Wahrend inStandorten mit geringer Raupendichte die Wirtssuche fur N. melanocephalusmoglicherweise sehr ineffizient ist, sind Standorte mit hoher Dichte nichtzwangslaufig vorteilhaft fur die Wespen, da eine hohe Raupendichte oft zuUberausbeutung der Ameisennester fuhrt, die stark dichteabhangige Mortalitat zurFolge hat. Hierauf basiert unsere Hypothese, dass fur eine effiziente Wirtssuche einsystematisches, mindestens jedoch ein nicht-zufalliges Suchverhalten von N.melanocephalus notwendig ist. Die Untersuchung von 32 Populationen im sudwest-deutschen Oberrheintal zeigte, daß die Raupendichte, Grosse des Habitats und dieDichte der Wirtsfutterpflanze keinen Einfluss auf die Parasitierung haben. Wahrendder Wirtssuche bevorzugt N. melanocephalus grosse Blutenkopfe und beprobte nurBlutenkopfe, die auch tatsachlich Raupen enthielten; auf nicht-beprobten Kopfenhielten sich die Wespen nur kurz auf. Nach einer Eiablage wurde die Suche auf demselben Blutenkopf fortgesetzt. Die Zahl der Raupen pro Blutenkopf hatte keinenEinfluss auf die Suchzeit. Durch das Anfliegen von grossen Blutenkopfen, die oft mehrRaupen enthalten als kleine Blutenkopfe, optimiert N. melanocephalus seinSuchverhalten und investiert mehr Zeit in Blutenkopfe, auf denen schon ein Wirtparasitiert wurde. Trotzdem wurden viele Raupen nicht parasitiert. Es wirddiskutiert, wie ein Teil der Raupen der Parasitierung entgeht und welcheParasitierungsstrategie fur Gegenspieler von rauberischen Wirtsraupen geeignet ist.& 2006 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.

Introduction

Most species of the family Lycaenidae arecharacterised by an ant-associated life history(Pierce et al., 2002; Weeks, 2003). However, insome lycaenid species, the mutualistic relationshipwith ants has shifted to a predatory (Pierce, 1995;Thomas & Wardlaw, 1992) or parasitic relationshipleading to a severe exploitation of ant nests(Pierce, 1995; Thomas & Elmes, 1998). Parasiticand predacious lycaenids may benefit from thehighly defended and nutrient-rich ant nests (butsee Thomas & Elmes, 1993). However, during thefirst phase of development outside the ant nest,caterpillars are not protected against naturalenemies (Claassens, 1976, Thomas & Elmes,1993). In this study, we investigate the factorsinfluencing parasitism and host exploitation of theconcealed-feeding butterfly Maculinea nausithous(Bergstr.) by a specialised parasitoid wasp.

To forage efficiently, insect parasitoids should beable to search in a non-random pattern. Foragingefficiency depends on host traits (Weisser, 1994),

the density and/or distribution of the host (Iwasa,Higashi & Yamamura, 1981), and habitat character-istics such as patch size and plant density (Cappuc-cino, 1992; Doak, 2000; Segarra-Carmona &Barbosa, 1992). Plant architecture can affectparasitoid oviposition success either by modulatingthe searching behaviour (Andow & Prokrym, 1990;Weisser, 1995) or by providing refuges for the host(Price, 1988). These mechanisms, combined withbehavioural and morphological traits of the para-sitoid (Teder, Tanhuanpaa, Ruohomaki, Kaitamieni,& Henriksson, 2000) as well as interference byother parasitoids (Cronin & Strong, 1993), have ledto the evolution of specific parasitoid foragingbehaviours (van Alphen, Bernstein, & Driessen,2003). Patch-leaving decisions are of great impor-tance in determining parasitoid foraging success.Previous studies and models have shown that thebehaviour of parasitoids depends on the spatialdistribution of the host (Iwasa et al., 1981). Inparasitoid species foraging for aggregated hosts,oviposition increases the probability of staying in apatch (incremental mechanism), whereas in

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species foraging for more regularly distributedhosts, oviposition should increase the probabilityof leaving (decremental mechanism; van Alphen etal., 2003). Other factors affecting time allocationcomprise substances to mark the host habitat(Bernstein & Driessen, 1996), the ability to dis-criminate between parasitized hosts and un-para-sitized hosts (Rosenheim & Mangel, 1994), and theinternal state of the foraging female (Roitberg,Sircom, Roitberg, van Alphen, & Mangel, 1993).

The resulting relationship between parasitismand host density can be positive (e.g., Cappuccino,1992; Costamagna, Menalled, & Landis, 2004) ornegative (Strong, Antolin, & Rathbun, 1990; Taylor,1993). Density-independent heterogeneity of para-sitism can be due to several mechanisms (Hassell &Pacala, 1990; Hassell & Wilson, 1997). A particularform of heterogeneity of parasitism arises whenparasitoid attack is confined to some particular partof the host population. Refuges created in this waymay be spatial, i.e., if parasitism is confined tosome part of the habitat, or temporal, i.e., whenparasitism depends on the timing and overlap ofdifferent host and parasitoid stages (Hassell, 2000).

In this study, we investigate patterns of parasit-ism at the level of the microhabitat (single flowerheads), and at the level of habitat patches. On bothlevels, features of the host’s food plant mightinfluence patterns of parasitism. We ask thefollowing questions. What fraction of M. nausithouscaterillars are parasitized by Neotypus melanoce-phalus? Do N. melanocephalus parasitoids searchrandomly for host caterpillars? Do host density,patch size and the density of the host’s food plantinfluence parasitism rates?

Methods

Study species

Female M. nausithous oviposit on the closedinflorescences of Sanguisorba officinalis L. (Rosa-ceae) flower heads. After a few days, the flor-escences open and cover the eggs. Caterpillarshatch and bore into the flower cup of single florets.Later, they feed on the immature seeds. Thecaterpillars then move within the inflorescences.Large flower heads can support several larvae(Musche, Anton, Worgan, & Settele, unpublished).After 3–4 weeks, fourth-instar caterpillars leavethe food plant and drop to the ground where theyare carried off by workers of any Myrmica species(Thomas, Elmes, Wardlaw, & Woyciechowski,1989), but successful development of M. nausithous

has only been observed in Myrmica rubra L. nests,where overexploitation of ant nests often leads toscramble competition among caterpillars (Stankie-wicz & Sielezniew, 2004; Thomas & Elmes, 1998).

During the short period of phytophagy, M.nausithous caterpillars are attacked by the para-sitoid wasp N. melanocephalus. The larvae of thissolitary parasitoid develop in the haemocoel of thecaterpillar and feed on the haemolymph. Develop-ment of N. melanocephalus larvae is synchronisedwith the development of their host: Immediatelyafter pupation of the caterpillars, N. melanoce-phalus leaves the host and pupates inside the pupalcase of M. nausithous. While N. melanocephalusoviposits M. teleius in Hungarian populations(Tartally, 2005) dissections of M. teleius caterpillarsfrom two populations in the study area could notreveal parasitism (Anton, unpublished).

Behavioural study

Behavioural studies were carried out between 4August and 6 August 2002 in Eußertal (SW Germany,49113055.000N, 7159057.000E). This N. melanocephaluspopulation is one of the largest in the study areadescribed below.

Five behavioural components were identified andtimed: (1) searching, (2) probing, (3) ovipositing,(4) grooming and (5) resting. Searching femalesdrum the flower heads with their antennae. Theyprobe the flower heads with their abdomen toreach host caterpillars. Oviposition is characterisedby a specific posture of females while standing still.Resting is defined as inactivity. When ovipositionwas observed, flower heads were termed exploited.Foraging by N. melanocephalus is often interruptedby periods of resting and grooming in the vegeta-tion. Female behaviour from landing on a flowerhead until leaving was observed and recorded usinga dictaphone. Based on this protocol, the timebudget of wasps was calculated. The developmentof M. nausithous caterpillars is synchronised withthe phenological change in the flower heads. Whileonly a small proportion of florets are open atbutterfly oviposition, the flower head is completelywilted by the time the caterpillars leave the plant.The size and phenological stage of 67 flower headsvisited by wasps were measured in the laboratory.To quantify the status of the flower phenology, wedefined categories describing the proportion ofopen or wilted flowers (1, 0% flowering; 2, 1–50%open; 3, 51–100% open; 4, 100% open; 5, 1–50%wilted; 6, 51–100% wilted). In order to find outwhether foraging wasps land on specific flowerheads, these measures were repeated with a

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control group comprising 70 randomly selectedflower heads. After recording parasitoid behaviour,we removed 24 flower heads and checked them forcaterpillars in the laboratory. The behaviour of thefemales was compared to the incidence andnumber of hosts per flower head. The density ofcaterpillars in non-visited flower heads was calcu-lated from a random sample of 156 flower heads.

Population density study

The population study was conducted in the UpperRhine valley in south-western Germany between theRhine River and the Palatinate forest between 1 Julyand 10 August 2003. Thirty-four patches in the studyarea (20� 45km) were checked for parasitism. Weexcluded two sites where the closely related M.teleius occurred, because young instar caterpillarsare difficult to tell apart. The fraction of parasitizedM. nausithous caterpillars was determined by dissec-tion. Depending on the estimated population size ofthe host butterfly, we dissected between 20 and 150M. nausithous caterpillars. Caterpillar density wascalculated from a collection of S. officinalis flowerheads from 20 randomly selected shoots. The flowerheads were collected 1 week after the phenologicalpeak of the parasitoid and brought into the labora-tory. We put the flower heads into Petri dishes andcounted emerging M. nausithous caterpillars for 1week. The size of the habitat patches was defined bythe area that was covered by the food-plant S.officinalis and ranged from 361 to 11191m2.

Statistical analysis

Student’s t-test was used to compare the meansize of visited flower heads with a random controlgroup and a w2 test to compare the phenologicalstages of visited flower heads with a randomcontrol group. We used Wilcoxon test to comparethe time wasps spent searching, probing, groomingand resting on exploited versus non-exploitedflower heads. The total time wasps spent onexploited and non-exploited flower heads wasanalysed with Student’s t-test.

In order to take into account the possibility thatsome observations might not be independent due tomultiple observations on the same individual, thedegree of freedom was reduced by 10% to deter-mine the level of significance in the behaviouralanalysis. A Poisson distribution was generated andcompared with the observed frequency of super-parasitized caterpillars using w2 test. We performeda simple linear regression analysis to examine therelationship between the time parasitoids spent on

the flower head and the number of caterpillars perflower head.

Parasitism rates at the patch level were analysedusing a generalised linear model (GLM) withquasibinomial error structure and a logit linkfunction ðlnðp=1� pÞÞ as linear predictor. In thefull model, the influence of caterpillar density,plant density and patch size on the proportion ofparasitised caterpillars was analysed. A simple GLMwith quasibinomial error was performed to analysethe relationship between the proportion of super-parasitised caterpillars and parasitism rate. Weused w2 test to compare the distribution ofparasitoid larvae per host caterpillar with a randomPoisson distribution. All analyses were performedwith the software package R V. 2.0.1 (http://cran.r-project.org/).

Results

Behavioural study

Large-sized flower heads and flower heads with ahigh proportion of open flowers were more oftenvisited than expected assuming random landings(Fig. 1). Since large flower heads are more likely tobe in a later phenological stage, both effects arenot independent (GLM; F1;68 ¼ 2:6, Po0.05). Onexploited flower heads, wasps spent 12.8% of thetotal time on the flower head for oviposition.Parasitoid behaviour did significantly differ be-tween host-exploited ðN ¼ 12Þ and non-exploitedflower heads ðN ¼ 45Þ. They searched, probed andgroomed longer on exploited flower heads(Table 1). Furthermore, females spent 78.2% oftime probing the flower head to reach caterpillars.The total time N. melanocephalus spent onexploited flower heads was on average six timeslonger than that spent on non-exploited flowerheads (Table 1). After the first oviposition, femalescontinued searching for 90.7723.9 s before theyeither oviposited again or left the flower head.That is, the additional time wasps spent on a flowerhead after the first oviposition was significantlylonger than that spent on non-exploited flowerheads (t-test; t ¼ �2:4; p ¼ 0:04). Twenty-four ofthe visited flower heads were dissected andchecked for caterpillars.

Eighty per cent of flower heads that were visitedby female wasps contained caterpillars. On aver-age, visited flower heads contained 3.370.5caterpillars. The control group of non-visited flowerheads ðN ¼ 156Þ contained 2.2 M. nausithouscaterpillars per flower head. Since the individual

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number of caterpillars per flower head in thecontrol group was not known, we did not statisti-cally compare it to the number of caterpillars pervisited flower head. Oviposition was observed inonly 16% of flower heads. All M. nausithous

Table 1. Behaviour of N. melanocephalus on exploited and

Behaviour of N. melanocephalus71SE (s)

Searching Probing Oviposition

Exploitedflower heads

75.3722.9 99.8726.2 26.376.5

Non-exploitedflower heads

19.972.8 2.371.2

W-/t-value W ¼ 43:5 W ¼ 5:0Significance Po0.001 Po0.05

aFor means of comparability, the time wasps spent for oviposition w

Figure 1. Comparison of flower heads that were visitedby N. melanocephalus females with a control group ofrandomly selected flower heads. (A) Median phenologicalstage of flower heads (71SE); categories describe theflowering status of florets from 1 (all florets closed) to 6(all florets wilted; see text); w2 ¼ 263:0, N ¼ 137,***Po0.001. (B) Mean size of flower heads (71SE),t ¼ �3:96, N ¼ 137, ***Po0.001.

caterpillars gained from the sampled flower headswere in the first or second larval stage. M. nausithouscaterpillars were stored in alcohol several hours afterparasitoid oviposition. Since the caterpillars couldhave moved during that time, we did not analyse therelation between parasitoid behaviour and the spatialposition ofM. nausithous caterpillars. Inside occupiedflower heads, 89% of caterpillars fed inside the flowercups. There was no significant correlation betweenthe time wasps spent on the flower head and thenumber of caterpillars per flower head (simple linearregression; t ¼ 1:5, N ¼ 24, P ¼ 0:14). Forty per centof flower heads that contained caterpillars were notprobed by wasps.

Population density study

N. melanocephalus was present in 24 out of 32screened butterfly occupied patches. The densityof host caterpillars did not influence the proportionof parasitized caterpillars (Fig. 2). Also, the densityof the host plant S. officinalis and the size of thehabitat patch did not affect parasitism rates(Table 2). Although N. melanocephalus is a solitaryparasitoid, 24% of parasitized caterpillarsðNparasitized ¼ 638Þ hosted more than one parasitoidlarva. The distribution of parasitoid larvae amongM. nausithous caterpillars did not significantlydiffer from a Poisson distribution (Fig. 3). Therewas no significant relationship between the propor-tion of superparasitized caterpillars and parasitismrate (deviance ¼ 46.2, F1;23 ¼ 0:8, P ¼ 0:4; meanresidual deviance ¼ 2.0).

Discussion

Parasitoid foraging behaviour

The searching behaviour of N. melanocephalus isinfluenced by the size of the flower head and its

non-exploited flower heads of S. officinalis

Time spent onflower71SE (s)

N

Grooming Resting

13.175.8 0.370.3 186.7737.8a 12

2.770.7 0.770.5 24.674.4 45

W ¼ 126 W ¼ 206 t ¼ �3:6Po0.05 P ¼ 0:51 P ¼ 0:002

as not included.

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Table 2. Analysis of deviance for the proportion ofparasitized M. nausithous caterpillars

Term d.f. Mean residualdeviance

F P

Densitycaterpillars

30 11.2 0.9 0.35

Density hostplants

29 2.8 0.2 0.63

Patch size 28 34.5 2.8 0.11Null 31 2.2

Terms were added sequentially.

Figure 2. Relationship between the proportion of para-sitized M. nausithous caterpillars and the density of M.nausithous (for statistical results, see Table 2).

Figure 3. Distribution of N. melanocephalus larvaeamong M. nausithous caterpillars (observed), comparedwith a Poisson distribution (expected); w2 ¼ 20:0,d.f. ¼ 16, P ¼ 0:22.

Patterns of parasitism in the predatory Maculinea nausithous 71

phenological stage. Large flower heads with manyopen florets are preferred. Previous studies haveshown that large flower heads are also predomi-

nantly selected by ovipositing M. nausithous fe-males (Figurny & Woyciechowski, 1998). Inaddition, only 80% of visited flower heads containedcaterpillars, suggesting that N. melanocephalusfemales may not be able to discriminate occupiedfrom unoccupied flower heads before landing onthem. However, the mean number of caterpillarsper flower head was 30% higher in visited flowerheads than in the non-visited control group. Thus,the selection of large and conspicuous flower headsby N. melanocephalus increases the likelihood ofhost encounters.

All flower heads probed by N. melanocephalusfemales contained caterpillars. The selective prob-ing suggests that N. melanocephalus femalesdiscriminate occupied from un-occupied flowerheads once they have landed, which could be byolfactorial or vibrational cues, as reported for otherparasitoid species (Djemai, Casas, & Magal, 2001).However, a large number of flower heads were notprobed although they contained caterpillars. Someparasitoid species mark hosts or the ovipositionsites after oviposition (Hoffmeister, 2000). Since wenever observed any marking behaviour, it appearsthat M. nausithous caterpillars feeding insiderejected flower heads might not be detectable forsearching females. A large fraction of caterpillarswas superparasitized, suggesting that female waspsrarely encounter unparasitized hosts at high para-sitism rates. The distribution of parasitoid larvaesuggests that N. melanocephalus randomly ovipo-sits on caterpillars. In a comparison among patches,superparasitism did not increase with overallparasitism rate. If N. melanocephalus was not ableto discriminate parasitized from unparasitized hostcaterpillars, we would expect that superparasitismshould increase as the encounter rate with unpar-asitized hosts decreases (Outreman, Le Ralec,Wajnberg, & Pierre, 2001; van Lenteren, 1981).Since we did not find such a relationship, wesuggest that N. melanocephalus might be able todiscriminate parasitized hosts and might acceptsuboptimal (parasitized) hosts (van Alphen & Visser,1990). Probing flower heads and caterpillar hand-ling is very time consuming. N. melanocephalusspent 80% of the time on the host-occupied flowerheads for probing, but 40% of the flower heads werenot probed. Dissections of flower heads revealedthe vast majority of caterpillars to be hidden byplant tissue in the flower cups. Perhaps N.melanocephalus is not able to detect caterpillarswithin the flower cups, so a fraction of caterpillarsescape parasitism. Even if N. melanocephalus iscapable of detecting M. nausithous caterpillarsinside the flower cup, the caterpillars may beinaccessible (Edwards & Hopper, 1999; Price, 1988;

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but see Hausmann, Matiacci, & Dorn, 2005). Thoughour study cannot directly show that caterpillarsfeeding inside flower cups are unsuitable for N.melanocephalus, it may affect parasitism.

N. melanocephalus females were observed tostay six times longer on exploited flower headscompared to non-exploited ones (Table 1). Similarresults were found by Cronin and Strong (1993) forAnagrus delicates (Dozier), a parasitoid of planthoppers. If N. melanocephalus does not receivehost cues after a certain time and if travel costs arelow, it might be the best strategy to leave the plant(Rosenheim & Mangel, 1994). Unlike in our study,the parasitoid Agathis sp. (Hymenoptera: Braconi-dae), which attacks the moth Greya subalba(Braun), is not able to detect concealed hostcaterpillars feeding within immature seeds ofLomatium without probing (Thompson, 1986).Females were observed to probe all immatureseeds irrespective of the presence of caterpillarsand spent the same amount of time on exploitedand non-exploited seeds. The number of G. subalbahosts per seed did not differ significantly betweenprobed and non-probed seeds. After oviposition,N. melanocephalus females continued searching.This motivation to continue host search suggeststhat N. melanocephalus expects multiplehosts within flower heads. Since large flower headsof S. officinalis contain higher numbers of cater-pillars than small ones (Musche et al., unpub-lished), an incremental mechanism of decisionmaking might be adaptive for N. melanocephalus(van Alphen et al., 2003). The rapid decision to stopor to continue searching after landing on a largeflower head may enable N. melanocephalus toexploit patches with low host density caterpillars.The fact that the number of caterpillars per flowerhead did not influence the time parasitoids spenton the flower head might be due to the lowdetectability of some caterpillars in the flowercup (Price, 1988).

Population density study

At the patch level, parasitism was not correlatedwith the density of M. nausithous caterpillars,although N. melanocephalus shows host-dependentforaging behaviour on the flower heads. Density-dependent foraging might not result in density-dependent parasitism if (1) patch arrival andleaving behaviour is density-dependent (Casas,1989; Umbanhowar, Maron, & Harrison, 2003), (2)handling time is long (Hassell, 1978; Rosenheim,Meade, Powch, & Schoenig, 1989), (3) the para-sitiod is egg limited (Hassell, 1982), (4) the host

experiences density-dependent mortality (Connor& Cargain, 1994; Tscharntke, 1992) or (5) hostsemploy defence behaviour (Rosenheim, 1990). Thehigh proportion of superparasitised caterpillarssuggests that N. melanocephalus might be moretime limited than egg limited. Only 16% of visits toflower heads lead to parasitism, although 80% ofvisited flower heads contained caterpillars. Somecaterpillars might have been rejected because theywere already parasitized. In addition, caterpillarsfeeding in the flower cup were probably unsuitable.Predatory Maculinea like M. nausithous experiencecontest competition on the host plant andstrong scramble competition inside ant nests(Mouquet, Thomas, Elmes, Clarke, & Hochberg,2005). The density-dependent mortality on thesequential resources could lead N. melanocephalusto spread offspring independent of host density(Hopper, 1999; but see Hopper & Rosenheim,2003). This conclusion is supported by the absenceof correlations between habitat characters likepatch size and parasitism. The density of the foodplant S. officinalis did not influence parasitism,either. Since the density of M. nausithous is limitedby the density of the host ant Myrmica rubra(Anton, Musche, Hula, & Settele, unpublished),plant density is an unsuitable indicator for hostdensity.

Feeding inside flower cups may create temporalrefuges for M. nausithous. It is not clear why N.melanocephalus does not attack later instars thatcan be more easily reached. In a 3-year study, itwas shown that the phenological peak of N.melanocephalus is 2–3 weeks after the phenologi-cal peak of M. nausithous (Loritz, unpublisheddata). At that time, a large fraction of caterpillarsis hidden by the flower cup. Competition amongforaging parasitoids for healthy hosts or immuno-logical reactions of later host stages to parasitoideggs might shift parasitism to young caterpillarstages (Brodeur and Boivin 2004).

Acknowledgements

Many thanks to Karsten Schonrogge and twoanonymous referees for helpful comments on themanuscript. We thank Klaus Horstmann for identi-fying Neotypus specimens , Vicky Temperton forimproving the English, and the authorities ofRhineland Palatinate (Struktur-und Genehmigungs-direktion Sud, Neustadt an der Weinstraße) for thepermission to work on M. nausithous. The researchwas funded by the EC within the RTD project‘‘MacMan’’ (EVK2-CT-2001-00126).

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