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Global climate change is resulting in a wide range of biotic responses, including changes in diel activity and seasonal phenology patterns, range shifts polewards in each hemisphere and/or to higher elevations, and altered intensity and frequency of interactions between species in ecosystems.Oak (Thaumetopoea processionea) and pine (T. pityocampa) processionary moths (hereafter OPM and PPM, respectively) are thermophilic species that are native to central and southern Europe. The larvae of both species are gregarious and produce large silken ‘nests’ that they use to congregate when not feeding. During outbreaks, processionary caterpillars are capable of stripping foliage from theirfood plants (oak and pine trees), generating considerable economic damage. Moreover, the third to last instar caterpillars of both species produce copious hairs as a means of defence against naturalenemies, including both vertebrate and invertebrate predators, and parasitoids. These hairs contain the toxin thaumetopoein that causes strong allergic reactions when it comes into contact with humanskin or other membranes. In response to a warming climate, PPM is expanding its range northwards, while OPM outbreaks are increasing in frequency and intensity, particularly in northern Germany,the Netherlands, and southern U.K., where it was either absent or rare previously. Here, we discuss how warming and escape from co-evolved natural enemies has benefitted both species, and suggest possible strategies for biological control.

1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free-living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed. 2. Honeydew, excreted by phloem-feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew-producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as hyperparasitoids, are not yet understood. 3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew-producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew-producing hosts. 4. Most honeydew types had a positive or neutral effect on life span and fecundity of hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types. 5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth-trophic-level organisms, not only those associated with honeydew-producing insects but also 'interlopers' without such a natural association.

To locate mating partners and essential resources such as food, oviposition sites and shelter, insects rely to a large extent on chemical cues. While most research has focused on cues derived from plants and insects, there is mounting evidence that indicates that micro‐organisms emit volatile compounds that may play an important role in insect behaviour. In this study, we assessed how volatile compounds emitted by phylogenetically diverse bacteria affected the olfactory response of the primary parasitoid Aphidius colemani and one of its secondary parasitoids, Dendrocerus aphidum. Olfactory responses were evaluated for volatile blends emitted by bacteria isolated from diverse sources from the parasitoid's habitat, including aphids, aphid mummies and honeydew, and from the parasitoids themselves. Results revealed that A. colemani showed a wide variation in response to bacterial volatiles, ranging from significant attraction over no response to significant repellence. Our results further showed that the olfactory response of A. colemani to bacterial volatile emissions was different from that of D. aphidum. Gas chromatography‐mass spectrometry analysis of the volatile blends revealed that bacterial strains repellent to A. colemani produced significantly higher amounts of esters, organic acids, aromatics and cycloalkanes than attractive strains. Strains repellent to D. aphidum produced significantly higher amounts of alcohols and ketones, whereas the strains attractive to D. aphidum produced higher amounts of the monoterpenes limonene, linalool and geraniol. Overall, our results indicate that bacterial volatiles can have an important impact on insect olfactory responses, and should therefore be considered as an additional, so far often overlooked factor in studying multitrophic interactions between plants and insects.

Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly decay. Little is known, however, on how they evolve when they confer a benefit to their host. Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to and colonized all the chromosomes. Moreover, large viral clusters are stably maintained suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed that this organization was already established ~53 mya. Transcriptomic analyses highlight temporal synchronization of viral gene expression, leading to particle production. Immune genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. This recognition suggests that no conflicts remain between symbiotic partners when benefits to them converge.

Insect hyperparasitoids are fourth trophic level organisms that commonly occur in terrestrial food webs, yet they are relatively understudied. These top-carnivores can disrupt biological pest control by suppressing the populations of their parasitoid hosts, leading to pest outbreaks, especially in confined environments such as greenhouses where augmentative biological control is used. There is no effective eco-friendly strategy that can be used to control hyperparasitoids. Recent advances in the chemical ecology of hyperparasitoid foraging behavior have opened opportunities for manipulating these top-carnivores in such a way that biological pest control becomes more efficient. We propose various infochemical-based strategies to manage hyperparasitoids. We suggest that a push-pull strategy could be a promising approach to ‘push’ hyperparasitoids away from their parasitoid hosts and ‘pull’ them into traps. Additionally, we discuss how infochemicals can be used to develop innovative tools improving biological pest control (i) to restrict accessibility of resources (e.g. sugars and alternative hosts) to primary parasitoid only or (ii) to monitor hyperparasitoid presence in the crop for early detection. We also identify important missing information in order to control hyperparasitoids and outline what research is needed to reach this goal. Testing the efficacy of synthetic infochemicals in confined environments is a crucial step towards the implementation of chemical ecology-based approaches targeting hyperparasitoids.

Many species of parasitoid wasps use plant volatiles to locate their herbivorous hosts. These volatiles are reliable indicators of host presence when their emission in plants is induced by herbivory. Hyperparasitoids may also use information from lower trophic levels to locate their parasitoid hosts but little is known about the role of volatiles from the plant–host complex in the foraging behavior of hyperparasitoids. Here, we studied how Dendrocerus aphidum (Megaspilidae) responds to plant and host volatiles in a series of experiments. This hyperparasitoid uses aphid mummies as its host and hampers biological control of aphids by parasitoids in greenhouse horticulture. We found that D. aphidum females were strongly attracted to volatiles from mummy-infested sweet pepper plants, but only when clean air was offered as an alternative odor source in the Y-tube olfactometer. Hyperparasitoid females did not have a preference for mummy-infested plants when volatiles from aphid-infested or healthy pepper plants were presented as an alternative. These olfactory responses of D. aphidum were mostly independent of prior experience. Volatiles from the host itself were also highly attractive to D. aphidum, but again hyperparasitoid females only had a preference in the absence of plant volatiles. Our findings suggest that plant volatiles may confuse, rather than guide the foraging behavior of D. aphidum. Mummy hyperparasitoids, such as D. aphidum, can use a wide variety of mummies and are thus extreme generalists at the lower trophic levels, which may explain the limited role of (induced) plant volatiles in their host searching behavior.

Climate warming is considered to be among the most serious of anthropogenic stresses to the environment, because it not only has direct effects on biodiversity, but it also exacerbates the harmful effects of other human-mediated threats. The associated consequences are potentially severe, particularly in terms of threats to species preservation, as well as in the preservation of an array of ecosystem services provided by biodiversity. Among the most affected groups of animals are insects—central components of many ecosystems—for which climate change has pervasive effects from individuals to communities. In this contribution to the scientists' warning series, we summarize the effect of the gradual global surface temperature increase on insects, in terms of physiology, behavior, phenology, distribution, and species interactions, as well as the effect of increased frequency and duration of extreme events such as hot and cold spells, fires, droughts, and floods on these parameters. We warn that, if no action is taken to better understand and reduce the action of climate change on insects, we will drastically reduce our ability to build a sustainable future based on healthy, functional ecosystems. We discuss perspectives on relevant ways to conserve insects in the face of climate change, and we offer several key recommendations on management approaches that can be adopted, on policies that should be pursued, and on the involvement of the general public in the protection effort.

Draagt rewilding bij aan biodiversiteitsherstel? Om die vraag te beantwoorden monitoren vmbo-leerlingen en mbo- en hbo-studenten planten en insecten op een afgebakend stukje schoolterrein waar beheer wordt losgelaten. Over het Rewilding project van Lectoraat Ecologisch Wijs van Aeres Hogeschool, met Jetske de Boer en Marlies Beukenkamp.

In deze webinar vertellen Jetske de Boer en Marlies Beukenkamp meer over het project 'Biodiveristeitsherstel op schoolterreinen'.

1. Dynamic conditions in nature have led to the evolution of behavioural traits that allow animals to use information on local circumstances and adjust their behaviour accordingly, for example through learning. Although learning can improve foraging efficiency, the learned information can become unreliable as the environment continues to change. This could lead to potential fitness costs when memories holding such unreliable information persist. Indeed, persistent unreliable memory was found to reduce the foraging efficiency of the parasitoid Cotesia glomerata under laboratory conditions. 2. Here, we evaluated the effect of such persistent unreliable memory on the foraging behaviour of C. glomerata in the field. This is a critical step in studies of foraging theory, since animal behaviour evolved under the complex conditions present in nature. 3. Existing methods provide little detail on how parasitoids interact with their environment in the field, therefore we developed a novel multi-camera system that allowed us to trace parasitoid foraging behaviour in detail. With this multi-camera system, we studied how persistent unreliable memory affected the foraging behaviour of C. glomerata when these memories led parasitoids to plants infested with non-host caterpillars in a semi-field set-up. 4. Our results demonstrate that persistent unreliable memory can lead to maladaptive foraging behaviour in C. glomerata under field conditions and increased the likelihood of oviposition in the non-host caterpillar Mamestra brassica. Furthermore, these time- and egg-related costs can be context dependent, since they rely on the plant species used. 5. These results provide us with new insight on how animals use previously obtained information in naturally complex and dynamic foraging situations and confirm that costs and benefits of learning depend on the environment animals forage in. Although behavioural studies of small animals in natural habitats remain challenging, novel methods such as our multi-camera system contribute to understanding the nuances of animal foraging behaviour.

Adults of many mosquito species feed on plants to obtain metabolic energy and to enhance reproduction. Mosquitoes primarily rely on olfaction to locate plants and are known to respond to a range of plant volatiles. We studied the olfactory response of the yellow fever mosquito Aedes aegypti to methyl jasmonate (MeJA) and cis-jasmone (CiJA), volatile compounds originating from the octadecanoid signaling pathway that plays a key role in plant defense against herbivores. Specifcally, we investigated how Ae. aegypti of diferent ages responded to elevated levels of CiJA in two attractive odor contexts, either derived from Lima bean plants or human skin. Aedes aegypti females landed signifcantly less often on a surface with CiJA and MeJA compared to the solvent control, CiJA exerting a stronger reduction in landing than MeJA. Odor context (plant or human) had no signifcant main efect on the olfactory responses of Ae. aegypti females to CiJA. Mosquito age signifcantly afected the olfactory response, older females (7–9 d) responding more strongly to elevated levels of CiJA than young females (1–3 d) in either odor context. Our results show that avoidance of CiJA by Ae. aegypti is independent of odor background, suggesting that jasmonates are inherently aversive cues to these mosquitoes. We propose that avoidance of plants with elevated levels of jasmonates is adaptive to mosquitoes to reduce the risk of encountering predators that is higher on these plants, i.e. by avoiding ‘enemy-dense-space’.

Animals can alter their foraging behavior through associative learning, where an encounter with an essential resource (e.g., food or a reproductive opportunity) is associated with nearby environmental cues (e.g., volatiles). This can subsequently improve the animal’s foraging efficiency. However, when these associated cues are encountered again, the anticipated resource is not always present. Such an unrewarding experience, also called a memory-extinction experience, can change an animal’s response to the associated cues. Although some studies are available on the mechanisms of this process, they rarely focus on cues and rewards that are relevant in an animal’s natural habitat. In this study, we tested the effect of different types of ecologically relevant memory-extinction experiences on the conditioned plant volatile preferences of the parasitic wasp Cotesia glomerata that uses these cues to locate its caterpillar hosts. These extinction experiences consisted of contact with only host traces (frass and silk), contact with nonhost traces, or oviposition in a nonhost near host traces, on the conditioned plant species. Our results show that the lack of oviposition, after contacting host traces, led to the temporary alteration of the conditioned plant volatile preference in C. glomerata, but this effect was plant species-specific. These results provide novel insights into how ecologically relevant memory-extinction experiences can fine-tune an animal’s foraging behavior. This fine-tuning of learned behavior can be beneficial when the lack of finding a resource accurately predicts current, but not future foraging opportunities. Such continuous reevaluation of obtained information helps animals to prevent maladaptive foraging behavior.

Eikenprocessierups, buxusmot en mug: er zijn genoeg plagen die ons de kriebels bezorgen. Maar veel meer insectensoorten zijn juist onmisbaar en verdienen aandacht omdat het slecht met ze gaat. Het nieuwe lectoraat ‘Ecologisch Wijs: Insecten & Maatschappij’ is bedoeld om ecologische oplossingen te ontwikkelen met bedrijfsleven en natuurorganisaties, stevig verankerd in het groene beroepsonderwijs.

De overlast van de eikenprocessierups (EPR) voor de gezondheid van mens en dier vraagt om aandacht en aanpakken. Op veel plekken gebeurt dat al. In de praktijk zijn verschillende middelen en maatregelen in zwang. Daarbij ontstaan vragen over de werkzaamheid, effectiviteit, (schadelijke) neveneffecten en gevaren van de verschillende instrumenten. De Informatiebladen Beheersing eikenprocessierups bevatten kernachtige informatie over gangbare, kansarme en kansrijke instrumenten om de overlast aan te pakken. Het Kennisplatform Processierups heeft de gepresenteerde informatie beoordeeld op relevantie en betrouwbaarheid.

To locate mating partners and essential resources such as food, oviposition sites and shelter, insects rely to a large extent on chemical cues. While most research has focused on cues derived from plants and insects, there is mounting evidence that indicates that micro‐organisms emit volatile compounds that may play an important role in insect behaviour. In this study, we assessed how volatile compounds emitted by phylogenetically diverse bacteria affected the olfactory response of the primary parasitoid Aphidius colemani and one of its secondary parasitoids, Dendrocerus aphidum. Olfactory responses were evaluated for volatile blends emitted by bacteria isolated from diverse sources from the parasitoid's habitat, including aphids, aphid mummies and honeydew, and from the parasitoids themselves. Results revealed that A. colemani showed a wide variation in response to bacterial volatiles, ranging from significant attraction over no response to significant repellence. Our results further showed that the olfactory response of A. colemani to bacterial volatile emissions was different from that of D. aphidum. Gas chromatography‐mass spectrometry analysis of the volatile blends revealed that bacterial strains repellent to A. colemani produced significantly higher amounts of esters, organic acids, aromatics and cycloalkanes than attractive strains. Strains repellent to D. aphidum produced significantly higher amounts of alcohols and ketones, whereas the strains attractive to D. aphidum produced higher amounts of the monoterpenes limonene, linalool and geraniol. Overall, our results indicate that bacterial volatiles can have an important impact on insect olfactory responses, and should therefore be considered as an additional, so far often overlooked factor in studying multitrophic interactions between plants and insects.

Many species of parasitoid wasps use plant volatiles to locate their herbivorous hosts. These volatiles are reliable indicators of host presence when their emission in plants is induced by herbivory. Hyperparasitoids may also use information from lower trophic levels to locate their parasitoid hosts but little is known about the role of volatiles from the plant–host complex in the foraging behavior of hyperparasitoids. Here, we studied how Dendrocerus aphidum (Megaspilidae) responds to plant and host volatiles in a series of experiments. This hyperparasitoid uses aphid mummies as its host and hampers biological control of aphids by parasitoids in greenhouse horticulture. We found that D. aphidum females were strongly attracted to volatiles from mummy-infested sweet pepper plants, but only when clean air was offered as an alternative odor source in the Y-tube olfactometer. Hyperparasitoid females did not have a preference for mummy-infested plants when volatiles from aphid-infested or healthy pepper plants were presented as an alternative. These olfactory responses of D. aphidum were mostly independent of prior experience. Volatiles from the host itself were also highly attractive to D. aphidum, but again hyperparasitoid females only had a preference in the absence of plant volatiles. Our findings suggest that plant volatiles may confuse, rather than guide the foraging behavior of D. aphidum. Mummy hyperparasitoids, such as D. aphidum, can use a wide variety of mummies and are thus extreme generalists at the lower trophic levels, which may explain the limited role of (induced) plant volatiles in their host searching behavior.

Insect hyperparasitoids are fourth trophic level organisms that commonly occur in terrestrial food webs, yet they are relatively understudied. These top-carnivores can disrupt biological pest control by suppressing the populations of their parasitoid hosts, leading to pest outbreaks, especially in confined environments such as greenhouses where augmentative biological control is used. There is no effective eco-friendly strategy that can be used to control hyperparasitoids. Recent advances in the chemical ecology of hyperparasitoid foraging behavior have opened opportunities for manipulating these top-carnivores in such a way that biological pest control becomes more efficient. We propose various infochemical-based strategies to manage hyperparasitoids. We suggest that a push-pull strategy could be a promising approach to ‘push’ hyperparasitoids away from their parasitoid hosts and ‘pull’ them into traps. Additionally, we discuss how infochemicals can be used to develop innovative tools improving biological pest control (i) to restrict accessibility of resources (e.g. sugars and alternative hosts) to primary parasitoid only or (ii) to monitor hyperparasitoid presence in the crop for early detection. We also identify important missing information in order to control hyperparasitoids and outline what research is needed to reach this goal. Testing the efficacy of synthetic infochemicals in confined environments is a crucial step towards the implementation of chemical ecology-based approaches targeting hyperparasitoids.

Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly decay. Little is known, however, on how they evolve when they confer a benefit to their host. Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to and colonized all the chromosomes. Moreover, large viral clusters are stably maintained suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed that this organization was already established ~53 mya. Transcriptomic analyses highlight temporal synchronization of viral gene expression, leading to particle production. Immune genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. This recognition suggests that no conflicts remain between symbiotic partners when benefits to them converge.

1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free-living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed. 2. Honeydew, excreted by phloem-feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew-producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as hyperparasitoids, are not yet understood. 3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew-producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew-producing hosts. 4. Most honeydew types had a positive or neutral effect on life span and fecundity of hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types. 5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth-trophic-level organisms, not only those associated with honeydew-producing insects but also 'interlopers' without such a natural association.

Global climate change is resulting in a wide range of biotic responses, including changes in diel activity and seasonal phenology patterns, range shifts polewards in each hemisphere and/or to higher elevations, and altered intensity and frequency of interactions between species in ecosystems.Oak (Thaumetopoea processionea) and pine (T. pityocampa) processionary moths (hereafter OPM and PPM, respectively) are thermophilic species that are native to central and southern Europe. The larvae of both species are gregarious and produce large silken ‘nests’ that they use to congregate when not feeding. During outbreaks, processionary caterpillars are capable of stripping foliage from theirfood plants (oak and pine trees), generating considerable economic damage. Moreover, the third to last instar caterpillars of both species produce copious hairs as a means of defence against naturalenemies, including both vertebrate and invertebrate predators, and parasitoids. These hairs contain the toxin thaumetopoein that causes strong allergic reactions when it comes into contact with humanskin or other membranes. In response to a warming climate, PPM is expanding its range northwards, while OPM outbreaks are increasing in frequency and intensity, particularly in northern Germany,the Netherlands, and southern U.K., where it was either absent or rare previously. Here, we discuss how warming and escape from co-evolved natural enemies has benefitted both species, and suggest possible strategies for biological control.