Understanding insect foraging in complex habitats by comparing trophic levels : insights from specialist host-parasitoid-hyperparasitoid systems

Insects typically forage in complex habitats in which their resources are surrounded by non-resources. For herbivores, pollinators, parasitoids, and higher level predators research has focused on how specific trophic levels filter and integrate information from cues in their habitat to locate resources. However, these insights frequently build specific theory per trophic level and seldom across trophic levels. Here, we synthesize advances in understanding of insect foraging behavior in complex habitats by comparing trophic levels in specialist host-parasitoid-hyperparasitoid systems. We argue that resources may become less apparent to foraging insects when they are member of higher trophic levels and hypothesize that higher trophic level organisms require a larger number of steps in their foraging decisions. We identify important knowledge gaps of information integration strategies by insects that belong to higher trophic levels.</p

Vosteen et al. 2016_R Skript_Fig. 3 honeydew attractivity

Fig. 3 – hoverfly oviposition experiment: To test which cues elicit hoverfly oviposition under field conditions, eggs were counted on plants that were previously aphid infested, non-infested plants treated with aphid honeydew and non-treated control plants in the presence and absence of pea aphids. Plants were left for 30 h in the field and hoverfly eggs were counted afterwards. A randomized block design was used in this experiments. Each block consisted of all six treatments. Number of hoverfly eggs was analyzed with a generalized linear mixed effects model with a poisson error distribution, using blocks as random effects (random intercept) and treatments as fixed effects. P-values for explanatory variables were obtained by sequentially deleting explanatory variables and comparison of the more complex model with the simpler model with a likelihood ratio test (Zuur et al. 2009). Factor level reductions were used to reveal differences between levels of a treatment (Crawley 2013)

data_Vosteen et al. 2016_Journal of Animal Ecology

data_Vosteen et al. 2016_Journal of Animal Ecolog

Gone with the wind : low availability of volatile information limits foraging efficiency in downwind-flying parasitoids

Parasitoids need to find their plant-feeding hosts in complex environments that contain multiple other plant and insect species. They usually rely on herbivore-induced plant volatiles to locate herbivore-infested plants from a distance and their foraging efficiency may be reduced when volatile information is not available. Downwind foraging during times when high wind speeds prevent odour-guided upwind flights may create foraging situations with limited accessibiliy to volatile information. We hypothesized that parasitoids forage less efficiently by landing on nonhost-damaged or undamaged plants when they are forced to fly downwind and tested this in a wind tunnel experiment. We released the parasitoid Cotesia glomerata (Hymenoptera, Braconidae) either upwind or downwind of a plant stand and observed their foraging behaviour. During downwind foraging, parasitoids were less successful in host finding and needed more time until they managed to oviposit in a host caterpillar compared to the upwind foraging situation. The observed increase in foraging time was caused by prolonged foraging on nonhost-infested and undamaged plants in the downwind situation, indicating that parasitoids leave an unprofitable patch that does not contain host caterpillars earlier, when they perceive volatiles from other herbivore-infested plants located upwind. Volatile information on the availability of herbivore-infested plants within a plant stand seems to be crucial for efficient foraging in plant stands that contain a mixture of host-infested, nonhost-infested and undamaged plants. Parasitoid foraging efficiency may thus be strongly reduced when high wind speed prevents odour-guided upwind flight.</p

Vosteen et al. 2016_R Data_Fig. 5 less suitable plant 2014

file used for statistical analysis in

Ecological functions of fungal sesquiterpenes in the food preference and fitness of soil Collembola

Volatile organic compounds (VOCs) emitted by fungi play a key role in locating and selecting hosts for fungivorous arthropods. However, the ecological functions of many common VOC classes, such as sesquiterpenes, remain unknown. Mutants of Trichoderma virens, defective in the emission of most sesquiterpenes owing to the deletion of the terpene cyclase vir4, were used to evaluate the role of this compound class in the food preference and fitness of the soil Collembola Folsomia candida. Choice experiments with and without direct contact with fungal mycelium revealed that Collembola were preferentially attracted to Δvir4 mutants impaired in sesquiterpene synthesis compared to wild-type T. virens. Grazing by F. candida on the sesquiterpene deficient T. virens strain had no effect on Collembola survival, reproduction and growth compared to wild-type T. virens. The results suggest that sesquiterpenes play an important role in fungal defence as repellents, but not as deterrents or toxins, against fungivorous Collembola. Our research contributes to the understanding of ecological interactions between fungi and fungivorous arthropods, providing insights into the specific ecological functions of sesquiterpenes. The study has implications for chemical ecology and the dynamics of multitrophic interactions in soil ecosystems

Vosteen et al. 2016_R Data_Fig. 4a honeydew quality

file used for statistical analysis in

Vosteen et al. 2016_R Skript_Fig. 4b honeydew quantity

Fig. 4b – honeydew quantity: Six, 12 or 18 droplets of this honeydew collected from Pisum race aphids feeding on Vicia faba were applied to uninfested Vicia faba. Plants were left for 30 h in the field and hoverfly eggs were counted afterwards. A randomized block design was used in this experiments. Each block consisted of all three treatments. Number of hoverfly eggs was analyzed with a generalized linear mixed effect model

Getting confused: learning reduces parasitoid foraging efficiency in some environments with non-host-infested plants

Foraging animals face the difficult task to find resources in complex environments that contain conflicting information. The presence of a non-suitable resource that provides attractive cues can be expected to confuse foraging animals and to reduce their foraging efficiency. We used the parasitoid Cotesia glomerata to study the effect of non-host-infested plants and associative learning on parasitoid foraging efficiency. Inexperienced C. glomerata did not prefer volatiles emitted from host (Pieris brassicae)-infested plants over volatiles from non-host (Mamestra brassicae)-infested plants and parasitoids that had to pass non-host-infested plants needed eight times longer to reach the host-infested plant compared to parasitoids that had to pass undamaged plants. Contrary to our expectations, oviposition experience on a host-infested leaf decreased foraging efficiency due to more frequent visits of non-host-infested plants. Oviposition experience did not only increase the responsiveness of C. glomerata to the host-infested plants, but also the attraction towards herbivore-induced plant volatiles in general. Experience with non-host-infested leaves on the contrary resulted in a reduced attraction towards non-host-infested plants, but did not increase foraging efficiency. Our study shows that HIPVs emitted by non-host-infested plants can confuse foraging parasitoids and reduce their foraging efficiency when non-host-infested plants are abundant. Our results further suggest that the effect of experience on foraging efficiency in the presence of non-host-infested plants depends on the similarity between the rewarding and the non-rewarding cue as well as on the completeness of information that parasitoids have acquired about the rewarding and non-rewarding cues.</p