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There is increasing evidence that plant-associated microorganisms play important roles in defending plants against insect herbivores through both direct and indirect mechanisms. While previous research has shown that these microbes can modify the behaviour and performance of insect herbivores and their natural enemies, little is known about their effect on egg parasitoids which utilize oviposition-induced plant volatiles to locate their hosts. In this study, we investigated how root inoculation of sweet pepper (Capsicum annuum) with the plant-beneficial fungi Beauveria bassiana ARSEF 3097 or Trichoderma harzianum T22 influences the olfactory behaviour of the egg parasitoid Trissolcus basalis following egg deposition by its host Nezara viridula. Olfactometer assays showed that inoculation by T. harzianum significantly enhanced the attraction of the egg parasitoid, while B. bassiana had the opposite effect. However, no variation was observed in the chemical composition of plant volatiles. Additionally, fitness-related traits of the parasitoids (wasp body size) were not altered by any of the two fungi, suggesting that fungal inoculation did not indirectly affect host quality. Altogether, our results indicate that plant inoculation with T. harzianum T22 can be used to enhance attraction of egg parasitoids, which could be a promising strategy in manipulating early plant responses against pest species and improving sustainable crop protection. From a more fundamental point of view, our findings highlight the importance of taking into account the role of microorganisms when studying the intricate interactions between plants, herbivores and their associated egg parasitoids., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2024 Van Hee et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Conservation biological control aims to enhance populations of natural enemies of insect pests in crop habitats, typically by intentional provision of flowering plants as food resources. Ideally, these flowering plants should be inherently attractive to natural enemies to ensure that they are frequently visited. We review the chemical ecology of floral resources in a conservation biological control context, with a focus on insect parasitoids. We highlight the role of floral volatiles as semiochemicals that attract parasitoids to the food resources. The discovery that nectar-inhabiting microbes can be hidden players in mediating parasitoid responses to flowering plants has highlighted the complexity of the interactions between plants and parasitoids. Furthermore, because food webs in agroecosystems do not generally stop at the third trophic level, we also consider responses of hyperparasitoids to floral resources. We thus provide an overview of floral compounds as semiochemicals from a multitrophic perspective, and we focus on the remaining questions that need to be addressed to move the field forward.

Background: Interspecific competition in insect parasitoids is an important ecological phenomenon that has relevant implications for biological pest control. To date, interspecific intrinsic (=larval) competition has been intensively studied, while investigations on extrinsic (=adult) competition have often lagged behind. In this study we examined the role played by parasitoid reproductive traits and host clutch size on the outcome of extrinsic competition between Trissolcus basalis (Wollaston) and Ooencyrtus telenomicida (Vassiliev), two egg parasitoids of the pest Nezara viridula (L). Laboratory experiments were conducted by allowing both parasitoid species to exploit an egg mass made of 10, 20, 30, or 40 hosts through single or simultaneous releases. Furthermore, under field conditions, egg masses consisting of 10 or 40 hosts were exposed in a tomato crop in order to validate laboratory investigation., Results: The results show that the egg mass size is an important predictor of extrinsic competition in our study system as a higher proportion of T. basalis emerged from large egg masses, while O. telenomicida dominated in small egg masses. Analysis of reproductive traits of parasitoid species indicates that T. basalis has superior abilities in host exploitation compared with O. telenomicida., Conclusions: We found that contrasting reproductive traits of two competing egg parasitoid species facilitate coexistence on a shared stink bug host. This work also highlights the importance to consider extrinsic competitive interactions between parasitoid species in a biological control perspective. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry., (© 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.)

Insect herbivores interact via plant-mediated interactions in which one herbivore species induces changes in plant quality that affects the performance of a second phytophagous insect that shares the food plant. These interactions are often asymmetric due to specificity in induced plant responses to herbivore attack, amount of plant damage, elicitors in herbivore saliva and plant organ damaged by herbivores. Parasitoids and their symbiotic polydnaviruses alter herbivore physiology and behaviour and may influence how plants respond to parasitized herbivores. We argue that these phenomena affect plant-mediated interactions between herbivores. We identify that the extended phenotype of parasitoid polydnaviruses is an important knowledge gap in interaction networks of insect communities., (Copyright © 2021 Elsevier Inc. All rights reserved.)

Hyperparasitoids are some of the most diverse members of insect food webs. True hyperparasitoids parasitize the larvae of other parasitoids, reaching these larvae with their ovipositor through the herbivore that hosts the parasitoid larva. During pupation, primary parasitoids also may be attacked by pseudohyperparasitoids that lay their eggs on the parasitoid (pre)pupae. By attacking primary parasitoids, hyperparasitoids may affect herbivore population dynamics, and they have been identified as a major challenge in biological control. Over the past decades, research, especially on aphid- and caterpillar-associated hyperparasitoids, has revealed that hyperparasitoids challenge rules on nutrient use efficiency in trophic chains, account for herbivore outbreaks, or stabilize competitive interactions in lower trophic levels, and they may use cues derived from complex interaction networks to locate their hosts. This review focuses on the fascinating ecology of hyperparasitoids related to how they exploit and locate their often inconspicuous hosts and the insect community processes in which hyperparasitoids are prominent players.

The quality of hosts for a parasitoid wasp may be influenced by attributes such as host size or species, with high quality for successful development usually coincident with high quality for larger offspring. This is not always the case: for the Scelionid wasp Trissolcus basalis, oviposition in eggs of the Brown Marmorated Stink Bug, Halyomorpha halys, rather than of the normal host, the Southern Green Stink Bug, Nezara viridula, leads to lower offspring survival, but survivors can be unusually large. Adult female T. basalis engage in contests for host access. As larger contestants are typically favoured in contests between parasitoids, the larger size of surviving offspring may compensate for the mortality of others. We construct a general game-theoretic model to explore whether size advantage can sustain a maternal preference to utilize a more deadly host species. We find that size advantage alone is unlikely to sustain a shift in host preference, yet such an outcome is possible when size asymmetries act simultaneously with advantages in host possession (ownership effect). Halyomorpha halys is an invasive pest of major agro-economic importance in Europe and the Americas, and use of its eggs as hosts by native parasitoids such as T. basalis has been seen as an evolutionary trap due to their high developmental mortality. Our model suggests that the recently discovered effect of host choice on offspring size may provide an escape from the trap via effects on contest biology of T. basalis which could foster a more stable association with H. halys. An evolutionary shift in the reproductive value of H. halys could increase the efficiency of T. basalis as a biological control agent of this invasive stink bug pest., (Copyright © 2021 Elsevier Ltd. All rights reserved.)

There is increasing awareness that interactions between plants and insects can be mediated by microbial symbionts. Nonetheless, evidence showing that symbionts associated with organisms beyond the second trophic level affect plant-insect interactions are restricted to a few cases belonging to parasitoid-associated bracoviruses. Insect parasitoids harbour a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behaviour. Yet, the function of these symbionts in plant-based trophic webs remains largely overlooked. Here, we provide the first evidence of a parasitoid-associated symbiont belonging to the group of ichnoviruses which affects the strength of plant-insect interactions. A comparative proteomic analysis shows that, upon parasitoid injection of calyx fluid containing ichnovirus particles, the composition of salivary glands of caterpillars changes both qualitatively (presence of two viral-encoded proteins) and quantitatively (abundance of several caterpillar-resident enzymes, including elicitors such as glucose oxidase). In turn, plant phenotypic changes triggered by the altered composition of caterpillar oral secretions affect the performance of herbivores. Ichnovirus manipulation of plant responses to herbivory leads to benefits for their parasitoid partners in terms of reduced developmental time within the parasitized caterpillar. Interestingly, plant-mediated ichnovirus-induced effects also enhance the performances of unparasitized herbivores which in natural conditions may feed alongside parasitized ones. We discuss these findings in the context of ecological costs imposed to the plant by the viral symbiont of the parasitoid. Our results provide intriguing novel findings about the role played by carnivore-associated symbionts on plant-insect-parasitoid systems and underline the importance of placing mutualistic associations in an ecological perspective., (© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Although consumers often rely on chemical information to optimize their foraging strategies, it is poorly understood how top carnivores above the third trophic level find resources in heterogeneous environments. Hyperparasitoids are a common group of organisms in the fourth trophic level that lay their eggs in or on the body of other parasitoid hosts. Such top carnivores use herbivore-induced plant volatiles (HIPVs) to find caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of different quality may be present alongside non-host parasitoid species, each of which can develop in multiple herbivore species. Because both the identity of the herbivore species and its parasitization status can affect the composition of HIPV emission, hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and field experiments to investigate the role of HIPVs in host selection of hyperparasitoids that search for hosts in a multi-parasitoid multi-herbivore context. In a wild Brassica oleracea-based food web, the hyperparasitoid Lysibia nana preferred HIPVs emitted in response to caterpillars parasitized by the gregarious host Cotesia glomerata over the non-host Hyposoter ebeninus. However, no plant-mediated discrimination occurred between the solitary host C. rubecula and the non-host H. ebeninus. Under both laboratory and field conditions, hyperparasitoid responses were not affected by the herbivore species (Pieris brassicae or P. rapae) in which the three primary parasitoid species developed. Our study shows that HIPVs are an important source of information within multitrophic interaction networks allowing hyperparasitoids to find their preferred hosts in heterogeneous environments.

Microbial mutualistic symbiosis is increasingly recognised as a hidden driving force in the ecology of plant-insect interactions. Although plant-associated and herbivore-associated symbionts clearly affect interactions between plants and herbivores, the effects of symbionts associated with higher trophic levels has been largely overlooked. At the third-trophic level, parasitic wasps are a common group of insects that can inject symbiotic viruses (polydnaviruses) and venom into their herbivorous hosts to support parasitoid offspring development. Here, we show that such third-trophic level symbionts act in combination with venom to affect plant-mediated interactions by reducing colonisation of subsequent herbivore species. This ecological effect correlated with changes induced by polydnaviruses and venom in caterpillar salivary glands and in plant defence responses to herbivory. Because thousands of parasitoid species are associated with mutualistic symbiotic viruses in an intimate, specific relationship, our findings may represent a novel and widespread ecological phenomenon in plant-insect interactions., (© 2018 The Authors Ecology Letters published by CNRS and John Wiley & Sons Ltd.)

Symbiotic relationships may provide organisms with key innovations that aid in the establishment of new niches. For example, during oviposition, some species of parasitoid wasps, whose larvae develop inside the bodies of other insects, inject polydnaviruses into their hosts. These symbiotic viruses disrupt host immune responses, allowing the parasitoid's progeny to survive. Here we show that symbiotic polydnaviruses also have a downside to the parasitoid's progeny by initiating a multitrophic chain of interactions that reveals the parasitoid larvae to their enemies. These enemies are hyperparasitoids that use the parasitoid progeny as host for their own offspring. We found that the virus and venom injected by the parasitoid during oviposition, but not the parasitoid progeny itself, affected hyperparasitoid attraction toward plant volatiles induced by feeding of parasitized caterpillars. We identified activity of virus-related genes in the caterpillar salivary gland. Moreover, the virus affected the activity of elicitors of salivary origin that induce plant responses to caterpillar feeding. The changes in caterpillar saliva were critical in inducing plant volatiles that are used by hyperparasitoids to locate parasitized caterpillars. Our results show that symbiotic organisms may be key drivers of multitrophic ecological interactions. We anticipate that this phenomenon is widespread in nature, because of the abundance of symbiotic microorganisms across trophic levels in ecological communities. Their role should be more prominently integrated in community ecology to understand organization of natural and managed ecosystems, as well as adaptations of individual organisms that are part of these communities., Competing Interests: The authors declare no conflict of interest.

The venom gland is a ubiquitous organ in Hymenoptera. In insect parasitoids, the venom gland has been shown to have multiple functions including regulation of host immune response, host paralysis, host castration and developmental alteration. However, the role played by the venom gland has been mainly studied in parasitoids developing in larval or pupal hosts while little is known for parasitoids developing in insect eggs. We conducted the first extensive characterization of the venom of the endoparasitoid Ooencyrtus telenomicida (Vassiliev), a species that develops in eggs of the stink bug Nezara viridula (L.). In particular we investigated the structure of the venom apparatus, its functional role and conducted a transcriptomic analysis of the venom gland. We found that injection of O. telenomicida venom induces: 1) a melanized-like process in N. viridula host eggs (host-parasitoid interaction), 2) impairment of the larval development of the competitor Trissolcus basalis (Wollaston) (parasitoid-parasitoid interaction). The O. telenomicida venom gland transcriptome reveals a majority of digestive enzymes (peptidases and glycosylases) and oxidoreductases (laccases) among the most expressed genes. The former enzymes are likely to be involved in degradation of the host resources for the specific benefit of the O. telenomicida offspring. In turn, alteration of host resources caused by these enzymes may negatively affect the larval development of the competitor T. basalis. We hypothesize that the melanization process induced by venom injection could be related to the presence of laccases, which are multicopper oxidases that belong to the phenoloxidases group. This work contributed to a better understanding of the venom in insect parasitoids and allowed to identify candidate genes whose functional role can be investigated in future studies., (Copyright © 2018 Elsevier Ltd. All rights reserved.)

Taste allows insects to detect palatable or toxic foods, identify a mate, and select appropriate oviposition sites. The gustatory system strongly contributes to the survival and reproductive success of many species, yet it is rarely studied in insect parasitoids. In order to locate and assess a host in which they will lay their eggs, female wasps actively search for chemical cues using their sensory organs present mainly on the antennae. In this paper, we studied the role of antennal taste sensilla chaetica in the perception of contact semiochemicals in Trissolcus brochymenae (Hymenoptera: Platygastridae), an egg parasitoid of the brassicaceae pest Murgantia histrionica (Heteroptera: Pentatomidae). Methanolic extracts obtained from male and female hosts elicited action potentials in taste neurons housed in antennal sensilla chaetica, indicating that these sensilla are involved in the perception of non volatile host kairomones. In behavioural assays, wasp females displayed an intense searching behaviour in open arenas treated with host extracts, thus confirming that these kairomones are soluble in polar solvents. We further investigated the extracts by Gas Chromatography-Mass Spectrometry (GC-MS) and found that they contain several compounds which are good candidates for these contact kairomones. This study contributes to better understanding contact chemoreception in egg parasitoids and identifying gustatory receptor neurons involved in the host location process., (Copyright © 2016 Elsevier Ltd. All rights reserved.)

Animals can adjust their behaviour according to previous experience gained during foraging. In parasitoids, experience plays a key role in host location, a hierarchical process in which air-borne and substrate-borne semiochemicals are used to find hosts. In nature, chemical traces deposited by herbivore hosts when walking on the plant are adsorbed by leaf surfaces and perceived as substrate-borne semiochemicals by parasitoids. Chemical traces left on cabbage leaves by adults of the harlequin bug (Murgantia histrionica) induce an innate arrestment response in the egg parasitoid Trissolcus brochymenae characterized by an intense searching behaviour on host-contaminated areas. Here we investigated whether the T. brochymenae response to host walking traces left on leaf surfaces is affected by previous experience in the context of parasitoid foraging behaviour. We found that: 1) an unrewarded experience (successive encounters with host-contaminated areas without successful oviposition) decreased the intensity of the parasitoid response; 2) a rewarded experience (successful oviposition) acted as a reinforcing stimulus; 3) the elapsed time between two consecutive unrewarded events affected the parasitoid response in a host-gender specific manner. The ecological role of these results to the host location process of egg parasitoids is discussed.

Intrinsic competition in insect parasitoids occurs when supernumerary larvae develop in the same host as consequence of multiple ovipositions by females of the same species (intra-specific competition) or by females of different species (inter-specific competition). Studies on intrinsic competition have mainly focused on understanding the factors that play a role in the outcome of competition, while fitness-related effects for the parasitoid surviving the competition have been poorly investigated, especially in egg parasitoids. Interestingly, even the winning parasitoid can experience fitness costs due to larval development in a host in which multiple factors have been injected by the ovipositing females or released by their larvae. In this paper we studied fitness-related traits associated with intra- and inter-specific competition between Trissolcus basalis (Wollaston) and Ooencyrtus telenomicida (Vassiliev), the main egg parasitoids associated with the southern green stink bug Nezara viridula (L.) in Italy. We investigated the impact of intrinsic competition for the surviving parasitoid in terms of body size, developmental time, number and size of oocytes. Our results indicated that T. basalis adults did not experience fitness-related costs when surviving intra-specific competition; however, adults were smaller, took longer to develop and females produced fewer oocytes after surviving inter-specific competition. A different outcome was found for O. telenomicida where the emerging females were smaller, produced fewer and smaller oocytes when suffering intra-specific competition whereas no fitness costs were found when adults survived inter-specific competition. These results support the hypothesis that the impact of intrinsic competition in egg parasitoids depends on the severity of the competitive interaction, as fitness costs were more pronounced when the surviving parasitoid interacted with the most detrimental competitor., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

In response to insect herbivory, plants emit volatile organic compounds which may act as indirect plant defenses by attracting natural enemies of the attacking herbivore. In nature, plants are often attacked by multiple herbivores, but the majority of studies which have investigated indirect plant defenses to date have focused on the recruitment of different parasitoid species in a single-herbivore context. Here, we report our investigation on the attraction of egg parasitoids of lepidopteran hosts (Trichogramma brassicae and T. evanescens) toward plant volatiles induced by different insect herbivores in olfactometer bioassays. We used a system consisting of a native crucifer, Brassica nigra, two naturally associated herbivores [the butterfly Pieris brassicae (eggs and caterpillars) and the aphid Brevicoryne brassicae] and an alien invasive herbivore (eggs and caterpillars of the moth Spodoptera exigua). We found that Trichogramma wasps were attracted by volatiles induced in the plants by P. brassicae eggs, but not by those induced in the plants by S. exigua eggs, indicating the specificity of the plant responses toward lepidopteran herbivores. The results of the chemical analysis revealed significant differences between the volatile blends emitted by plants in response to attack by P. brassicae and S. exigua eggs which were in agreement with the behavioural observations. We investigated the attraction of Trichogramma wasps toward P. brassicae egg-induced volatiles in plants simultaneously attacked by larvae and nymphs of different non-hosts. The two chewing caterpillars P. brassicae and S. exigua, but not the phloem-feeding aphid B. brassicae, can disrupt the attraction of Trichogramma species toward P. brassicae egg-induced volatiles. Indirect plant defenses are discussed in the context of multiple herbivory by evaluating the importance of origin, dietary specialization and feeding guild of different attackers on the recruitment of egg-killing parasitoids.

Contact kairomones from the host mud dauber wasp Trypoxylon politum Say (Hymenoptera: Crabronidae) that mediate behavioral responses of its ectoparasitoid Melittobia digitata Dahms (Hymenoptera: Eulophidae) were investigated. Chemical residues from host by-products, the cocoon, and the meconium, induced arrestment behavior of macropterous female parasitoids, while those from the host stage attacked, i.e., the prepupa, did not. Melittobia digitata response to polar and apolar extracts of host by-products indicated kairomone(s) solubility mainly in hexane. GC and GC/MS analysis of cocoon and meconium apolar extracts revealed a mixture of linear carboxylic acids from C(6) to C(18), and both extracts contained almost identical compounds. When a reconstructed blend of host by-product carboxylic acids was tested, M. digitata females showed only a weak response, thus suggesting that other unidentified compounds present in small quantities also may be involved. Melittobia digitata's response to contact kairomones was innate and not affected by previous host exposure experience. Our results provide evidence of contact kairomone exploitation in the genus Melittobia. The ecological significance of these findings in the host selection process of M. digitata is discussed.

Learning and memory allow animals to adjust their foraging strategies through experience. Despite the known impact of temperature on many aspects of the behavioral ecology of animals, memory retention in the face of realistic thermal stress has seldom been assessed. In the laboratory, we studied the behavioral expression of an egg parasitoid's (Trissolcus basalis) memory when exposed to thermal stress that could be encountered in nature. We hypothesized that thermal stress would disrupt memory consolidation and/ or modify the optimality of memory retention, thus affecting patch time allocation strategies. Memory consolidation was resilient to 1 h of thermal stress following an unrewarded experience (learning) on a patch of host-associated infochemicals. Neither high (40 °C) or low (10 °C) thermal stress changed the intensity of the experienced wasps' behavioral response relative to those held at a moderate temperature (25 °C). Next, we investigated how temperature stress could affect the parasitoids' memory retention ("forgetting"). When kept at a constant moderate temperature after learning, residence times of wasps retested on host cues increased relative to controls (naïve wasps) over a period of 4 days as they presumably "forgot." However, both hot and cool daily temperature cycles prevented forgetting; the residence times of retested experienced wasps in these treatments did not change relative to controls over time. We discuss to what extent this may be an adaptive response by the parasitoids versus a physiological constraint imposed by temperature. Our findings contribute to an understanding of the impact of thermal stress on foraging strategies that involve learning and memory. [ABSTRACT FROM AUTHOR]

Melittobia acasta and M. australica are newly recorded from Sicily, Italy, and the second species is reported in Europe for the first time. A short historical background about Melittobia parasitoid wasps, their hosts, and distribution, with emphasis in those two species is presented together with illustrations to facilitate their identification. Brief discussion about the presence and possible distribution of the species in Sicily is also included. [ABSTRACT FROM AUTHOR]

Responses of macropterous females of the ectoparasitoid Melittobia digitata Dahms (Hymenoptera: Eulophidae) to direct and indirect cues emitted by its natural hosts as well as laboratory hosts were investigated using a Y-tube olfactometer. To locate the nest of mud dauber wasps, Trypoxylon politum Say (Hymenoptera: Crabronidae), and one of their inquilines, Anthrax spec., parasitoids exploit volatiles from the freshly built nest mud and the empty cocoon constructed by the wasps, as well as their meconium. However, the parasitoids did not respond to odors emitted by older nest mud or by the host stages that are attacked ( T. politum prepupae and Anthrax spec. larvae). Melittobia digitata was not attracted to direct volatiles released by the dipteran hosts Anastrepha ludens Loew (Diptera: Tephritidae) (a natural host) and Sarcophaga bullata (Parker) (Diptera: Sarcophagidae) (a laboratory host). Based on our results, we suggest that M. digitata adopts a ‘sit and wait’ strategy to locate mud dauber wasps, relying mainly on indirect host-related cues: females search for nests that are under construction and once found, they wait inside the cell until the host completes its cocoon and releases meconium, an indicator that is associated with host suitability. No attraction was found to dipteran hosts, suggesting that parasitization of these hosts may be incidental, due to the broad host plasticity of Melittobia wasps. [ABSTRACT FROM AUTHOR]