Effects of plant diversity and structural complexity on parasitoid behaviour in a field experiment

1. In natural ecosystems, plants containing hosts for parasitoids are often embedded within heterogeneous plant communities. These plant communities surrounding host‐infested plants may influence the host‐finding ability of parasitoids. 2. A release‐recapture‐approach was used to examine whether the diversity and structural complexity of the community surrounding a host‐infested plant influences the aggregation behaviour of the leaf‐miner parasitoid Dacnusa sibirica Telenga and naturally occurring local leaf‐miner parasitoids. Released and locally present parasitoids were collected on potted Jacobaea vulgaris Gaertn.plants infested with the generalist leaf‐miner Chromatomyia syngenesiae Hardy. The plants were placed in experimentally established plant communities differing in plant diversity (1–9 species) and habitat complexity (bare ground, mown vegetation, and tall vegetation). Additionally, parasitoids were reared out from host mines on the trap plants. 3. Plant diversity did not influence the mean number of recaptured D. sibirica or captures of other locally present parasitoids but the number of recaptured parasitoids was influenced by habitat complexity. No D. sibirica parasitoids were recaptured in the bare ground plots or plots with mown vegetation. The mean number of recaptured D. sibirica generally increased with increasing complexity of the plant community, whereas locally present parasitoids were captured more frequently in communities with more bare ground. There was a unimodal relationship between the number of reared out parasitoids and diversity of the surrounding vegetation with the highest density of emerged parasitoids at intermediate diversity levels. 4. The present study adds to the thus far limited body of literature examining the aggregation behaviour of parasitoids in the field and suggests that the preference of parasitoids to aggregate in complex versus simple vegetation is association specific and thus depends on the parasitoid species as well as the identity of the plant community.     

Density‐mediated indirect interactions alter host foraging behaviour of parasitoids without altering foraging efficiency

1. Foraging decisions of parasitoids are influenced by host density via density‐mediated indirect interactions. However, in the parasitoid's environment, non‐suitable herbivores are also present. These non‐hosts also occur in different densities, which can affect a parasitoid's foraging behaviour. 2. The influence of non‐host densities can be expressed during the first phase of the foraging process, when parasitoids use plant volatiles to locate plants infested by their host. They may also play a role during the second phase, when parasitoids use infochemicals from the host and plant to locate, recognise and accept the host. 3. By using laboratory and field setups, it was studied whether the density of non‐host herbivores influences these two phases of the foraging behaviour of the parasitoid Cotesia glomerata as well as the parasitoid's efficiency to find its host, Pieris brassicae caterpillars. 4. The findings show that a high non‐host density, regardless of the species used, negatively affected parasitoid preference for host‐infested plants, but that the behaviour on the plant and the total host‐finding efficiency of the parasitoids were not influenced by non‐host density. 5. These results are discussed in the context of density‐mediated indirect interactions.     

Plant‐mediated indirect effects and the persistence of parasitoid–herbivore communities

We have examined the effects of herbivore diversity on parasitoid community persistence and stability, mediated by nonspecific information from herbivore‐infested plants. First, we investigated host location and patch time allocation in the parasitoid Cotesia glomerata in environments where host and/or nonhost herbivores were present on Brassica oleracea leaves. Parasitoids were attracted by infochemicals from leaves containing nonhost herbivores. They spent considerable amounts of time on such leaves. Thus, when information from the plant is indistinct, herbivore diversity is likely to weaken interaction strengths between parasitoids and hosts. In four B. oleracea fields, all plants contained herbivores, often two or more species. We modelled parasitoid–herbivore communities increasing in complexity, based on our experiments and field data. Increasing herbivore diversity promoted the persistence of parasitoid communities. However, at a higher threshold of herbivore diversity, parasitoids became extinct due to insufficient parasitism rates. Thus, diversity can potentially drive both persistence and extinctions.     

RETRACTED ARTICLE: Foraging of Host-Habitat and Superparasitism in <Emphasis Type="Italic">Cotesia glomerata</Emphasis>: A Gregarious Parasitoid of <Emphasis Type="Italic">Pieris brassicae</Emphasis>

The study investigates differences in the oviposition pattern of a braconid parasitoid, Cotesia glomerata (Linn.) in Pieris brassicae (Linn.) in relation to their use of different cruciferous food plants. The response of P. brassicae to superparasitism and consequences for the parasitoid were examined in order to elucidate the ecological significance of this behaviour. Female parasitoid located various crucifers and searched for host more frequently almost on all the host plants tested i.e. cabbage, cauliflower, Chinese cabbage, broccoli and radish. According to the estimated relative number of female locating hosts, cabbage was the most attractive plant for C. glomerata and total number of eggs laid in host larvae feeding on it was higher than in larvae feeding on other plants. Laboratory experiments demonstrated that superparasitism reduced survivorship of P. brassicae larvae. Superparasitism lengthened parasitoid development and prolonged the feeding period of host larvae. Sex ratio and the body weight of emergent wasps correlated negatively with brood size. Despite a trade-off between maximising brood size and optimising the fitness of individual offspring, two or three ovipositions on P. brassicae larvae resulted in a greater female dry mass than did a single oviposition on the host. Thus, superparasitism might be of adaptive significance under certain circumstances, especially when host density is low and unparasitized hosts are rare in a habitat.     

Host‐searching responses to herbivory‐associated chemical information and patch use depend on mating status of female solitary parasitoid wasps

1. In a tritrophic interaction system consisting of plants, herbivores, and their parasitoids, chemicals released from plants after herbivory are known to play important roles for many female parasitoids to find their hosts efficiently. On the plant side, chemical information associated with herbivory can act as an indirect defence by attracting the natural enemies of the host herbivores. 2. However, mated and virgin females of haplodiploid parasitoids might not necessarily respond to such chemical cues in the same way. Since virgin females can produce only sons, they might refrain from searching for hosts to invest eggs until copulation, in order to produce both sexes. 3. Here, we investigated differential host‐searching behaviours shown by mated and virgin females in the solitary parasitoid wasp, Cotesia vestalis, in response to herbivory‐associated chemical information from cruciferous plants infested by their host larvae, Plutella xylostella. 4. Mated females showed a significantly higher flight preference for host‐infested plants over intact plants, while no preference was observed with virgin females. Mated females also showed more intensive antennal searching and ovipositor probing behaviours to leaf squares with wounds caused by hosts than did virgin females. Furthermore, mated females stayed longer in host patches with higher parasitism rates than virgin females. 5. These results indicate that mating status of C. vestalis females clearly influences their host‐searching behaviour in response to herbivory‐associated chemical information and patch exploitation. Female parasitoids seem to forage for hosts depending on their own physiological condition in a tritrophic system.     

Interactions among three trophic levels: the influence of host plant on performance of Pieris brassicae and its parasitoid, Cotesia glomerata

The relative suitability of four host plants was determined both for unparasitized Pieris brassicae L. caterpillars and for Cotesia glomerata (L.) developing in P. brassicae. For unparasitized P. brassicae, growth rate and pupal weight were highest on Brussels sprouts and Swedish turnip, intermediate on rape, and lowest on nasturtium. In contrast, C. glomerata larval developmental rate and adult longevity were greatest for wasps from P. brassicae reared on nasturtium.On all four plants, the host-parasitoid complex attained a lower final weight than unparasitized P. brassicae, and it is argued that this difference is due primarily to reduced consumption by parasitized P. brassicae. Among parasitized caterpillars, however, complex weight was positively correlated with clutch size, suggesting that C. glomerata larvae are able to partially counteract the effect of parasitization per se on host consumption.The host plants of P. brassicae appear to face an evolutionary dilemma: in order to increase the total mass of parasitoids produced, they must suffer greater loss of foliage. This trade-off, if common in nature, may represent a formidable constraint on coevolution between host plants and parasitoids.     

The parasitoidCotesia glomerata (Hymenoptera: Braconidae) discriminates between first and fifth larval instars of its hostPieris brassicae,on the basis of contact cues from frass,silk, and herbivore-damaged leaf tissue

Adult females of the larval parasitoidCotesia glomerata (L.) respond to chemical cues associated with feeding damage inflicted on cabbage plants by its host,Pieris brassicae (L.). The use of these infochemicals by the parasitoid during selection of the most suitable host instar was investigated. The parasitoid can successfully parasitize first-instar host larvae, while contacts with fifth-instar larvae are very risky since these caterpillars react to parasitization attempts by biting, spitting, and hitting, resulting in a high probability of the parasitoid being seriously injured or killed. Observations of the locomotor behavior of individual wasps on leaves with feeding damage inflicted by the first and the fifth larval instars and on host silk and frass showed that several cues affect the duration of searching by the parasitoids after reaching a leaf: cues on the margin of the feeding damage and cues in the host frass and silk. Whole frass, silk, and hexane extracts of frass obtained from first-instar elicited parasitoid's searching behavior significantly longer than frass, silk, and hexane extract of frass from the fifth instar. The results demonstrate thatC. glomerata can discriminate between first instars, which are more suitable hosts, and fifth instars ofP. brassicae without contacting the caterpillars, by exploiting instar-related cues.     

Varying degree of physiological integration among host instars and their endoparasitoid affects stress‐induced mortality

In natural populations of insect herbivores, genetic differentiation is likely to occur due to variation in host plant utilization and selection by the local community of organisms with which they interact. In parasitoids, engaging in intimate associations with their host during immature development, local variation may exist in host quality for parasitoid development. We compared the development of a gregarious endoparasitoid, Cotesia glomerata L. (Hymenoptera: Braconidae), collected in The Netherlands, in three strains and three caterpillar instars (L1–L3) of its main host, Pieris brassicae L. (Lepidoptera: Pieridae). Hosts had been collected in The Netherlands and France, and were reared in the laboratory for one generation. We also used an established Dutch laboratory strain that had not been exposed to parasitoids for at least 24 generations. Parasitoid survival to adulthood was inversely correlated with host instar at parasitism. Adult parasitoid body mass was largest when hosts were parasitized as L1 and smallest when hosts were parasitized as L3, whereas egg‐to‐adult development time was quickest on L3 hosts and slowest on L1 hosts. Higher survival and faster development of C. glomerata on French L2 hosts also showed that there is variation in host‐instar‐related suitability. Many L2 and most L3 caterpillars that were parasitized exhibited signs of pathogen infection and perished within a few days of parasitism, whereas this never happened when hosts were parasitized as L1 or in non‐parasitized control caterpillars. Our results reveal that, irrespective of the host strain, L1 hosts are optimally synchronized with C. glomerata development. By contrast, the high precocious mortality of L3 larvae may be due to stress‐induced regulation by the parasitoid in order to ‘force’ its developmental program into synchrony with the developing parasitoid larvae. Our results underscore a potentially important role played by pathogens in mediating herbivore–parasitoid interactions that are host‐instar‐dependent in their expression.     

Foraging for solitarily and gregariously feeding caterpillars: A comparison of two related parasitoid species (Hymenoptera: Braconidae)

In the present study we apply a comparative approach, in combination with experimentation, to study behavior of two parasitoid species that attack caterpillar hosts with different feeding strategies (gregarious or solitary). In a semifield setup, consisting of clean cabbage plants and plants infested with one of two host species, the foraging behavior of the specialistCotesia rubecula, on obligate parasitoid of solitarily feedingPieris rapae larvae, was compared to that of the generalistCotesia glomerata, a polyphagous parasitoid of several Pieridae species (mainly the gregariously feedingPieris brassicae).Cotesia glomerata displayed equal propensity to search for and parasitize larvae of both host species. AlthoughC. glomerata exhibited a relatively plastic foraging behavior in that it searched differently under different host distribution conditions, its behavior seems more adapted to search for gregariously feeding hosts. Females exhibited a clear area-restricted search pattern and were more successful in finding the gregariously feeding caterpillars.Cotesia rubecula showed a higher propensity to search forP. rapae than forP. brassicae, i.e., females left the foraging setup significantly earlier when their natural hostP. rapae was not present.C. rubecula showed a more fixed foraging behavior, which seems adapted to foraging for solitarily feeding host larvae. In a setup with onlyP. rapae larvae, the foraging strategies of the two parasitoid species were quite similar. In a choice situationC. glomerata did not show a preference for one of the host species, whileCotesia rubecula showed a clear preference for its natural host species. The latter was shown by several behavioral parameters such as the number of first landings, allocation of search time, and percentage parasitization.     

Effect of belowground herbivory on parasitoid associative learning of plant odours

Root herbivores can influence both the performance and the behaviour of parasitoids of aboveground insect herbivores through changes in aboveground plant quality and in the composition of the plant's odour blend. Here we show that root herbivory by Delia radicum larvae did not influence the innate preferences for plant odours of the two closely related parasitoid species Cotesia glomerata and C. rubecula, but did affect their learned preferences, and did so in an opposite direction. While C. glomerata learned to prefer the odour of plants with intact roots, C. rubecula learned to prefer the odour of root‐infested plants. The learned preference of C. glomerata for the odour of plants with intact roots matches our previously published result of its better performance when developing in P. brassicae hosts feeding on this plant type. In contrast, the relatively stronger learned preference of C. rubecula for the odour of root‐infested plants cannot be merely explained by its performance, as the results of our present study indicate that D. radicum root herbivory did not influence the performance of C. rubecula nor of its host P. rapae. Our results stress the importance of assessing the influence of root herbivores on both innate and learned responses of parasitoids to plant odours.     

Associative learning of host presence in non‐host environments influences parasitoid foraging

1. Parasitoids are known to utilise learning of herbivore‐induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non‐suitable herbivores (non‐hosts). Simultaneous infestation of plants by hosts and non‐hosts has been found to result in induction of HIPVs that differ from host‐infested plants. Each non‐host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non‐host herbivore also contain the host. 2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non‐hosts in the laboratory and in semi‐field experiments. 3. In two‐choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant–host–non‐host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non‐host caterpillar Mamestra brassicae or the non‐host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non‐host caterpillars or aphids in a semi‐field situation. 4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.     

The influence of plant species on attraction and host acceptance inCotesia glomerata (Hymenoptera: Braconidae)

Females of the larval parasitoidCotesia glomerata (L.) use plant-associated cues to locate their lepidopteran host,Pieris rapae L. In this study we investigated the influence of four host plant species,Brassica oleracea var.acephala (‘Vates’ kale),Tropaeolum majus (nasturtium),Lunaria annua (honesty), andCleome spinosa (spider flower), on two components of the host selection process inC. glomerata, namely, attraction and host acceptance. Choice tests in a flight tunnel showed that parasitoids were attracted to some host plant species more than to others in the absence of host larvae.B. oleracea was the most attractive plant species, followed byL. annua, T. majus, andC. spinosa. In previous studies it was shown thatB. oleracea carries highly suitable hosts forC. glomerata and that, in the field, parasitization rates on this plant were the highest. When host larvae were reared on the four host plant species and then transferred to a common substrate (B. oleracea var.capitata, cabbage), plant species that had served as diet for the hosts did not have a significant effect on acceptance for parasitization. Thus, parasitoids were attracted to host plant species differentially, but they did not discriminate among host larvae based on the dietary history of their hosts. ForC. glomerata, it appears that phytochemistry mediates host selection more by influencing parasitoid attraction than it does by affecting host acceptance.     

Females of Cotesia vestalis,a parasitoid of diamondback moth larvae,learn to recognise cues from aphid‐infested plants to exploit honeydew

1. To maximise their reproductive success, the females of most parasitoids must not only forage for hosts but must also find suitable food sources. These may be nectar and pollen from plants, heamolymph from hosts and/or honeydew from homopterous insects such as aphids. 2. Under laboratory conditions, females of Cotesia vestalis, a larval parasitoid of the diamondback moth (Plutella xylostella) which does not feed on host blood, survived significantly longer when held with cruciferous plants infested with non‐host green peach aphids (Myzus persicae) than when held with only uninfested plants. 3. Naïve parasitoids exhibited no preference between aphid‐infested and uninfested plants in a dual‐choice test, but those that had been previously fed aphid honeydew significantly preferred aphid‐infested plants to uninfested ones. 4. These results suggest that parasitoids that do not use aphids as hosts have the potential ability to learn cues from aphid‐infested plants when foraging for food. This flexible foraging behaviour could allow them to increase their lifetime reproductive success.     

DNA-based confirmation that the parasitic wasp <Emphasis Type="Italic">Cotesia glomerata</Emphasis> (Braconidae,Hymenoptera) is a new threat to endemic butterflies of the Canary Islands

Island-endemic species can be particularly vulnerable to alien invasion. There are many examples of introduced insect parasitoids having a serious impact on endemic butterflies and moths. In 2006, a population of parasitic wasps was reared from larvae of the Canary Island Large White butterfly (Pieris cheiranthi), an endemic inhabitant of laurel forests unique to the Canary Islands of Macaronesia. Parasitoids were tentatively identified as Cotesia glomerata (Braconidae, Hymenoptera), a widely introduced agricultural bioagent. To corroborate this finding we sequenced 632 bp of mitochondrial cox1 from parasitoids and hosts from La Palma and from the native range of C. glomerata in continental Europe. These were combined with GenBank sequences and a character-based, phylogenetic approach was used to assess the species status of parasites and hosts. The La Palma parasitoid could unambiguously be assigned to C. glomerata under the criterion of diagnosibility with corroboration from multiple lines of evidence (DNA, morphology). We suggest that this opportunistic, non-native parasitoid wasp will be a threat to P. cheiranthi and other endemic Canarian butterflies. Parasitoid populations were recorded from P. cheiranthi in marginal forest habitats but not in central forest areas, suggesting that comprehensive habitat conservation of the Canarian laurel forests could prevent penetration of the alien parasitoid wasps and subsequent mortality of endemic butterfly populations.     

Food plant and herbivore host species affect the outcome of intrinsic competition among parasitoid larvae

1. In nature, several parasitoid species often exploit the same stages of a common herbivore host species and are able to coexist despite competitive interactions amongst them. Less is known about the direct effects of resource quality on intrinsic interactions between immature parasitoid stages. The present study is based on the hypothesis that variation in the quality or type of plant resources on which the parasitoids indirectly develop may be complementary and thus facilitate niche segregation favouring different parasitoids in intrinsic competition under different dietary regimes. 2. The present study investigated whether two herbivore species, the cabbage butterflies Pieris brassicae and Pieris rapae (Pieridae), and the quality of two important food plants, Brassica oleracea and Brassica nigra (Brassicaceae), affect the outcome of intrinsic competition between their primary larval endoparasitoids, the gregarious Cotesia glomerata (Braconidae) and the solitary Hyposoter ebeninus (Ichneumonidae). 3. Hyposoter ebeninus is generally an intrinsically superior competitor over C. glomerata. However, C. glomerata survived more antagonistic encounters with H. ebeninus when both developed in P. brassicae rather than in P. rapae caterpillars, and while its host was feeding on B. nigra rather than B. oleracea. Moreover, H. ebeninus benefitted from competition by its higher survival in multiparasitised hosts. 4. These results show that both plant and herbivore species mediate the battleground on which competitive interactions between parasitoids are played out and may affect the outcomes of these interactions in ways that enable parasitoids to segregate their niches. This in turn may promote coexistence among parasitoid species that are associated with the same herbivore host.     

A comparison of the host-searching efficiency of two larval parasitoids of Plutella xylostella

1. A host specialist parasitoid is thought to have greater efficiency in locating hosts or greater ability to overcome host defence than a generalist species. This leads to the prediction that a specialist should locate and parasitise more hosts than a generalist in a given arena. The work reported here tested these predictions by comparing the host‐searching behaviour of Diadegma semiclausum (a specialist) and Cotesia plutellae (an oligophagous species), two parasitoids of larval Plutella xylostella. 2. Both parasitoids employed antennal search and ovipositor search when seeking hosts but D. semiclausum also seemed to use visual perception in the immediate vicinity of hosts. 3. Larvae of P. xylostella avoided detection by parasitoids by moving away from damaged plant parts after short feeding bouts. When they encountered parasitoids, the larvae wriggled vigorously as they retreated and often hung from silk threads after dropping from a plant. 4. These two parasitoids differed in their responses to host defences. Diadegma semiclausum displayed a wide‐area search around feeding damage and waited near the silk thread for a suspended host to climb up to the leaf, then attacked it again. Cotesia plutellae displayed an area‐restricted search and usually pursued the host down the silk thread onto the ground. 5. Diadegma semiclausum showed a relatively fixed behavioural pattern leading to oviposition but C. plutellae exhibited a more plastic behavioural pattern. 6. The time spent by the two parasitoids on different plants increased with increasing host density, but the time spent either on all plants or a single plant by D. semiclausum was longer than that of C. plutellae. Diadegma semiclausum visited individual plants more frequently than C. plutellae before it left the patch, and stung hosts at more than twice the rate of C. plutellae. 7. The results indicated that the host‐location strategies employed by D. semiclausum were adapted better to the host's defensive behaviour, and thus it was more effective at detecting and parasitising the host than was C. plutellae.     

Combined use of herbivore‐induced plant volatiles and sex pheromones for mate location in braconid parasitoids

Herbivore‐induced plant volatiles (HIPVs) are important cues for female parasitic wasps to find hosts. Here, we investigated the possibility that HIPVs may also serve parasitoids as cues to locate mates. To test this, the odour preferences of four braconid wasps – the gregarious parasitoid Cotesia glomerata (L.) and the solitary parasitoids Cotesia marginiventris (Cresson), Microplitis rufiventris Kokujev and Microplitis mediator (Haliday) – were studied in olfactometers. Each species showed attraction to pheromones but in somewhat different ways. Males of the two Cotesia species were attracted to virgin females, whereas females of M. rufiventris were attracted to virgin males. Male and female M. mediator exhibited attraction to both sexes. Importantly, female and male wasps of all four species were strongly attracted by HIPVs, independent of mating status. In most cases, male wasps were also attracted to intact plants. The wasps preferred the combination of HIPVs and pheromones over plant odours alone, except M. mediator, which appears to mainly use HIPVs for mate location. We discuss the ecological contexts in which the combined use of pheromones and HIPVs by parasitoids can be expected. To our knowledge, this is the first study to show that braconid parasitoids use HIPVs and pheromones in combination to locate mates.     

Behavioral manipulation of host caterpillars by the primary parasitoid wasp Cotesia glomerata (L.) to construct defensive webs against hyperparasitism

Many parasitoids control the behavior of their hosts to achieve more preferable conditions. Decreasing predation pressure is a main aim of host manipulation. Some parasitoids control host behavior to escape from their enemies, whereas others manipulate hosts into constructing defensive structures as barriers against hyperparasitism. Larvae of the parasitoid wasp Cotesia glomerata form cocoon clusters after egression from the parasitized host caterpillar of the butterfly Pieris brassicae. After the egression of parasitoids, the perforated host caterpillar lives for a short period and constructs a silk web that covers the cocoon cluster. We examined whether these silk webs protect C. glomerata cocoons against the hyperparasitoid wasp Trichomalopsis apanteroctena. In cocoon clusters that were not covered by silk webs (bare clusters), only cocoons hidden beneath others avoided hyperparasitism. In covered cocoon clusters, both cocoons hidden beneath others and those with a space between them and the silk web avoided hyperparasitism, whereas cocoons that contacted the silk webs were parasitized. The frequency of cocoons that were hidden beneath others increased with the increasing number of cocoons in a cluster, but the defensive effect of cluster size was thought to be lower than that of silk webs. However, the rate of hyperparasitism did not differ between covered and bare clusters when we allowed the hyperparasitoids to attack the cocoon clusters in an experimental arena. This result was thought to have been caused by low oviposition frequency by these hyperparasitoids. As a result, silk webs did not guard the cocoons from hyperparasitoids in our experiments, but would protect cocoons under high hyperparasitism pressure by forming a space through which the ovipositors could not reach the cocoons.     

Herbivore species identity rather than diversity of the non‐host community determines foraging behaviour of the parasitoid wasp Cotesia glomerata

Extensive research has been conducted to reveal how species diversity affects ecosystem functions and services. Yet, consequences of diversity loss for ecosystems as a whole as well as for single community members are still difficult to predict. Arthropod communities typically are species‐rich, and their species interactions, such as those between herbivores and their predators or parasitoids, may be particularly sensitive to changes in community composition. Parasitoids forage for herbivorous hosts by using herbivore‐induced plant volatiles (indirect cues) and cues produced by their host (direct cues). However, in addition to hosts, non‐suitable herbivores are present in a parasitoid's environment which may complicate the foraging process for the parasitoid. Therefore, ecosystem changes in the diversity of herbivores may affect the foraging efficiency of parasitoids. The effect of herbivore diversity may be mediated by either species numbers per se, by specific species traits, or by both. To investigate how diversity and identity of non‐host herbivores influence the behaviour of parasitoids, we created environments with different levels of non‐host diversity. On individual plants in these environments, we complemented host herbivores with 1–4 non‐host herbivore species. We subsequently studied the behaviour of the gregarious endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) while foraging for its gregarious host Pieris brassicae L. (Lepidoptera: Pieridae). Neither non‐host species diversity nor non‐host identity influenced the preference of the parasitoid for herbivore‐infested plants. However, after landing on the plant, non‐host species identity did affect parasitoid behaviour, whereas non‐host diversity did not. One of the non‐host species, Trichoplusia ni Hübner (Lepidoptera: Noctuidae), reduced the time the parasitoid spent on the plant as well as the number of hosts it parasitized. We conclude that non‐host herbivore species identity has a larger influence on C. glomerata foraging behaviour than non‐host species diversity. Our study shows the importance of species identity over species diversity in a multitrophic interaction of plants, herbivores, and parasitoids.     

Effects of quantitative and qualitative differences in volatiles from host‐ and non‐host‐infested maize on the attraction of the larval parasitoid Cotesia kariyai

Cotesia kariyai Watanabe (Hymenoptera: Braconidae) is a specialist larval parasitoid of Mythimna separata Walker (Lepidoptera: Noctuidae). Cotesia kariyai wasps use herbivore‐induced plant volatiles (HIPVs) to locate hosts. However, complex natural habitats are full of volatiles released by both herbivorous host‐ and non‐host‐infested plants at various levels of intensity. Therefore, the presence of non‐hosts may affect parasitoid decisions while foraging. Here, the host‐finding efficiency of naive C. kariyai from HIPVs influenced by host‐ and non‐host‐infested maize [Zea mays L. (Poaceae)] plants was investigated with a four‐arm olfactometer. Ostrinia furnacalis Guenée (Lepidoptera: Crambidae) was selected as a non‐host species. One unit (1 U) of host‐ or non‐host‐infested plant was prepared by infesting a potted plant with five host or seven non‐host larvae. In two‐choice bioassays, host‐infested plants fed upon by different numbers of larvae, and various units of host‐ and non‐host‐infested plants (infestation units; 1 U, 2 U, and 3 U) were arranged to examine the effects of differences in volatile quantity and quality on the olfactory responses of C. kariyai with the assumption that volatile quantity and quality changes with differences in numbers of insects and plants. Cotesia kariyai was found to perceive quantitative differences in volatiles from host‐infested plants, preferring larger quantities of volatiles from larger numbers of larvae or plants. Also, the parasitoids discriminated between healthy plants, host‐infested plants, and non‐host‐infested plants by recognising volatiles released from those plants. Cotesia kariyai showed a reduced preference for host‐induced volatiles, when larger numbers of non‐host‐infested plants were present. Therefore, quantitative and qualitative differences in volatiles from host‐ and non‐host‐infested plants appear to affect the decision of C. kariyai during host‐habitat searching in multiple tritrophic systems.