Non-host Herbivores Research Articles

Intraspecific plant variation and nonhost herbivores affect parasitoid host location behaviour

Parasitoids need to find their hosts in patchy environments that differ in profitability. To maximize foraging efficiency, parasitoids use volatile information of plants on which their hosts feed. The blend of plant volatiles emitted is affected by genetic variation in plants and by the herbivore species feeding on the plant. How parasitoids deal with variation in plant volatiles induced by host or nonhost herbivores on various plant genotypes in a plant stand is unclear. In a wind tunnel, we examined foraging behaviour of the parasitoid Cotesia glomerata in mixes of white cabbage cultivars with host ( Pieris brassicae ) and nonhost herbivores ( Mamestra brassicae or Delia radicum ). We specifically studied the efficiency of parasitoids in locating a host-infested plant when having to pass three other plants that varied in volatile emission by cultivar and herbivore identity. We show that foraging decisions of C. glomerata are affected by the apparency of volatile cues from upwind host-infested plants. We found that parasitoids flew over the first three plants more often when the last plant was a host-infested attractive cultivar and the first three plants were a less attractive cultivar, regardless of the presence of host or nonhost herbivores. Furthermore, parasitoids spent more time on the first three plants if these were infested with host or nonhost larvae, and this effect was stronger when the first three plants were of the attractive cultivar. Our results suggest that parasitoids may more easily locate host herbivores on plant genotypes with more apparent volatile information. However, host location efficiency is affected by the contrast with other plumes of plant volatiles derived from genotypic variation in plants and induction of volatiles by nonhost herbivores. Apparency of information on upwind patches influences patch residence time and patch choice and is an important component of optimal foraging in parasitoids. • Foraging decisions by Cotesia glomerata are affected by the apparency of information. • Profitability of upwind patches affects foraging decisions on the current patch. • Nonhost herbivores with traits similar to the host reduced host location efficiency. • Established parasitoid cultivar preferences are nuanced in complex plant mixtures.

Herbivore species identity rather than diversity of the non‐host community determines foraging behaviour of the parasitoid wasp C otesia 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 Hubner (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.

Feeding guild of non-host community members affects host-foraging efficiency of a parasitic wasp.

Interactions between predator and prey, or parasitoid and host, are shaped by trait- and density-mediated processes involving other community members. Parasitoids that lay their eggs in herbivorous insects locate their hosts through infochemicals such as herbivore-induced plant volatiles (HIPVs) and host-produced kairomones. Hosts are frequently accompanied by non-host herbivores that are unsuitable for the parasitoid. These non-hosts may interfere with host location primarily through trait-mediated processes, by their own infochemicals, and their induction of the emission of plant volatiles. Although it is known that single non-hosts can interfere with parasitoid host location, it is still unknown whether the observed effects are due to species specific characteristics or to the feeding habits of the non-host herbivores. Here we addressed whether the feeding guild of non-host herbivores differentially affects foraging of the parasitoid Cotesia glomerata for its common host, caterpillars of Pieris brassicae feeding on Brassica oleracea plants. We used different phloem-feeding and leaf-chewing non-hosts to study their effects on host location by the parasitoid when searching for host-infested plants based on HIPVs and when searching for hosts on the plant using infochemicals. To evaluate the ultimate effect of these two phases in host location, we studied parasitism efficiency of parasitoids in small plant communities under field-tent conditions. We show that leaf-chewing non-hosts primarily affected host location through trait-mediated effects via plant volatiles, whereas phloem-feeding non-hosts exerted trait-mediated effects by affecting foraging efficiency of the parasitoid on the plant. These trait-mediated effects resulted in associational susceptibility of hosts in environments with phloem feeders and associational resistance in environments with non-host leaf chewers.

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.

Flexible parasitoid behaviour overcomes constraint resulting from position of host and nonhost herbivores

Parasitoids face several hurdles and distractions while foraging for their hosts, one of which is the presence of nonhost herbivores. Nonhost herbivores may interfere with plant volatile-mediated location of host-infested plants and reduce encounter rates with hosts on the plant. This results in a lower foraging efficiency. In this study, we tested whether the feeding position of a host and nonhost herbivore on the same plant influences foraging decisions and parasitism efficiency of parasitoids. We confined host and nonhost herbivores to either higher positions, i.e. younger leaves (preferred by the host) or lower positions on the plant, i.e. older leaves (preferred by the nonhost). Host and nonhost herbivores fed either on separate leaves or on the same leaf. Results from laboratory experiments show that during the first phase of foraging when plant volatiles are used to locate a host-infested plant, parasitoids were misled when host and nonhost were positioned in an unnatural way on the individual plant (host on the older leaves). The positions of host and nonhost partly influenced parasitoids during the second phase of foraging, when the host is located on the plant by using host cues. Total host-finding efficiency, as tested in a semifield set-up, was not affected by herbivore position. We conclude that parasitoid foraging behaviour has enough flexibility to overcome constraints resulting from an unexpected distribution of herbivores over a plant.

Floral volatiles interfere with plant attraction of parasitoids: ontogeny-dependent infochemical dynamics in Brassica rapa.

BackgroundThe role of plant ontogeny on investment in direct defense against herbivores is well accepted, but the transition from the vegetative to the reproductive stage can also affect indirect resistance traits (i.e. attraction of the natural enemies of plant attackers). Here, we conducted behavioral bioassays in olfactometers to determine whether the developmental stage (vegetative, pre-flowering, and flowering) of Brassica rapa plants affects attraction of Cotesiaglomerata, a parasitoid of the herbivore Pieris brassicae, and examined the blends of volatile compounds emitted by plants at each developmental stage.ResultsPieris-infested plants were always more attractive to parasitoids than control plants and plants infested by a non-host herbivore, independently of plant developmental stage. On the other hand, the relative attractiveness of Pieris-infested plants was ontogeny dependent: Pieris-infested plants were more attractive at the pre-flowering stage than at the vegetative stage, and more attractive at the vegetative stage than at the flowering stage. Chemical analyses revealed that the induction of leaf volatiles after herbivory is strongly reduced in flowering plants. The addition of synthetic floral volatiles to infested vegetative plants decreased their attractiveness to parasitoids, suggesting a trade-off between signaling to pollinators and parasitoids.ConclusionOur results show that putative indirect resistance traits are affected by plant development, and are reduced during B. rapa reproductive stage. The effects of ontogenetic shifts in resource allocation on the behavior of members of the third trophic level may have important implications for the evolution of plant defense strategies against herbivores.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-015-0047-7) contains supplementary material, which is available to authorized users.

Egg parasitoid attraction toward induced plant volatiles is disrupted by a non-host herbivore attacking above or belowground plant organs.

Plants respond to insect oviposition by emission of oviposition-induced plant volatiles (OIPVs) which can recruit egg parasitoids of the attacking herbivore. To date, studies demonstrating egg parasitoid attraction to OIPVs have been carried out in tritrophic systems consisting of one species each of plant, herbivore host, and the associated egg parasitoid. Less attention has been given to plants experiencing multiple attacks by host and non-host herbivores that potentially could interfere with the recruitment of egg parasitoids as a result of modifications to the OIPV blend. Egg parasitoid attraction could also be influenced by the temporal dynamics of multiple infestations, when the same non-host herbivore damages different organs of the same plant species. In this scenario we investigated the responses of egg parasitoids to feeding and oviposition damage using a model system consisting of Vicia faba, the above-ground insect herbivore Nezara viridula, the above- and below-ground insect herbivore Sitona lineatus, and Trissolcus basalis, a natural enemy of N. viridula. We demonstrated that the non-host S. lineatus disrupts wasp attraction toward plant volatiles induced by the host N. viridula. Interestingly, V. faba damage inflicted by either adults (i.e., leaf-feeding) or larvae (i.e., root-feeding) of S. lineatus, had a similar disruptive effect on T. basalis host location, suggesting that a common interference mechanism might be involved. Neither naïve wasps or wasps with previous oviposition experience were attracted to plant volatiles induced by N. viridula when V. faba plants were concurrently infested with S. lineatus adults or larvae. Analysis of the volatile blends among healthy plants and above-ground treatments show significant differences in terms of whole volatile emissions. Our results demonstrate that induced plant responses caused by a non-host herbivore can disrupt the attraction of an egg parasitoid to a plant that is also infested with its hosts.

A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores

BackgroundVolatiles emitted by herbivore-infested plants are highly attractive to parasitoids and therefore have been proposed to be part of an indirect plant defense strategy. However, this proposed function of the plant-provided signals remains controversial, and it is unclear how specific and reliable the signals are under natural conditions with simultaneous feeding by multiple herbivores. Phloem feeders in particular are assumed to interfere with plant defense responses. Therefore, we investigated how attack by the piercing-sucking cicadellid Euscelidius variegatus influences signaling by maize plants in response to the chewing herbivore Spodoptera littoralis.ResultsThe parasitoid Cotesia marginiventris strongly preferred volatiles of plants infested with its host S. littoralis. Overall, the volatile emissions induced by S. littoralis and E. variegatus were similar, but higher levels of certain wound-released compounds may have allowed the wasps to specifically recognize plants infested by hosts. Expression levels of defense marker genes and further behavioral bioassays with the parasitoid showed that neither the physiological defense responses nor the attractiveness of S. littoralis infested plants were altered by simultaneous E. variegatus attack.ConclusionsOur findings imply that plant defense responses to herbivory can be more robust than generally assumed and that ensuing volatiles convey specific information about the type of herbivore that is attacking a plant, even in complex situations with multiple herbivores. Hence, the results of this study support the notion that herbivore-induced plant volatiles may be part of a plant's indirect defense stratagem.

Effect of the Presence of a Nonhost Herbivore on the Response of the Aphid Parasitoid Diaeretiella rapae to Host-infested Cabbage Plants

The vast majority of studies of plant indirect defense strategies have considered simple tritrophic systems that involve plant responses to attack by a single herbivore species. However, responses by predators and parasitoids to specific, herbivore-induced, volatile blends could be compromised when two or more different herbivores are feeding on the same plant. In Y-tube olfactometer studies, we investigated the responses of an aphid parasitoid, Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae), to odors from cabbage plants infested with the peach-potato aphid Myzus persicae (Sulzer) (Homoptera: Aphididae), in both the presence and absence of a lepidopteran caterpillar, Plutella xylostella L. (Lepidoptera: Plutellidae). Female parasitoids chose aphid-infested plants over uninfested plants but did not distinguish between caterpillar-infested and uninfested plants. When given a choice between odors from an aphid-infested plant and those from a plant infested with diamondback moth larvae, they significantly chose the former. Furthermore, the parasitoids responded equally to odors from a plant infested with aphids only and those from a plant infested with both aphids and caterpillars. The results support the hypothesis that the aphid and the caterpillar induce different changes in the volatile profile of cabbage plants and that D. rapae females readily distinguish between the two. Furthermore, the changes to the plant volatile profile induced by the caterpillar damage did not hinder the responses of the parasitoid to aphid-induced signals.

Foraging efficiency of a parasitoid of a leaf herbivore is influenced by root herbivory on neighbouring plants

1 Root feeding insects can influence foliar quality of the host plant, which can affect the development and behaviour of leaf herbivores and parasitoids. Thus far, such interactions have been reported in situations where root and leaf associated organisms share a host-plant. We tested whether root herbivory influences searching behaviour of an above-ground parasitoid when the foliar feeding host of the parasitoid and the root herbivore are feeding on different plants. 2 We manipulated the proportion of 25 plants (ranging from 0 to 1) exposed to root herbivory by Delia radicum (neighbouring-plants). Five additional plants were infested above-ground with Pieris brassicae larvae (host-infested plants) and were placed in-between the neighbouring plants. We then released females of the parasitoid Cotesia glomerata which attacks P. brassicae and studied foraging efficiency of the parasitoid. 3 Overall, parasitoids located more host-infested plants during the maximum allowed searching time, and found their hosts about three times faster when neighbouring plants were exposed to root herbivory, than when neighbouring plants were not infested with D. radicum. Similar results were found when the host-infested plants were also exposed to root herbivory. 4 Our results show that the interaction between an above-ground foliar feeding insect and its parasitoid can be influenced by the presence of non-host herbivores feeding on the roots of neighbouring conspecific plants.

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.