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Adult parasitoids are well known to feed on sugar-rich resources such as floral nectar. Recently, an increasing body of evidence has shown that nectar is ubiquitously colonized by microorganisms and, as a consequence, microbial metabolic activity can affect several traits of floral nectar. Yet, how the fermentation of nectar by yeasts impacts the olfactory responses and performance of parasitoids is largely understudied, especially in the case of egg parasitoids. In this study, we investigated whether fermentation by the nectar yeasts Metschnikowia gruessii and M. reukaufii affects the olfactory responses of Trissolcus basalis and Ooencyrtus telenomicida, two egg parasitoid species associated with the southern green stink bug Nezara viridula. We also investigated how yeast fermentation affects the longevity and survival of the egg parasitoids. Results of static four-chamber olfactometer tests showed that nectar fermented by M. gruessii (but not by M. reukaufii) was attractive to both egg parasitoid species, whereas no significant yeast-mediated effects were found in terms of wasp longevity. Gas chromatography coupled with mass spectrometry (GC-MS) showed a clear separation of the volatile profiles among M. gruessii, M. reukaufii and non-fermented control nectar supporting the results of the insect bioassays. The results of our study highlight the need to consider the role of microbes when studying interactions between flower nectar and egg parasitoids and could have implications from a conservation biological control perspective. [ABSTRACT FROM AUTHOR]

Plants can respond to insect egg deposition by emitting oviposition‐induced plant volatiles (OIPVs) recruiting parasitoids. The recruitment of carnivore insects in response to egg deposition is considered an indirect defence strategy that is widespread in the plant kingdom. In recent years, there has been increasing evidence showing that microbial colonization can influence the strength of plant responses to insect herbivory, yet no information is available on how beneficial microbes modulate indirect defences induced by insect egg deposition.In this work, we evaluated the effects of inoculation with the beneficial soil fungus Trichoderma harzianum strain T22 on a tritrophic system consisting of tomato, the southern green stink bug Nezara viridula and its associated egg parasitoid Trissolcus basalis. We used Y‐tube olfactometer assays to evaluate the behavioural responses of the parasitoids to OIPVs emitted by plants colonized with beneficial soil microbes. We also used gas chromatography coupled with mass spectrometry (GC–MS) to investigate whether and how root inoculation with T. harzianum T22 affects the chemical composition of induced plant volatiles.In olfactometer assays, we found that root inoculation with T. harzianum T22 enhanced the attraction of the egg parasitoid towards tomato plants induced by N. viridula feeding and oviposition activities. In particular, the egg parasitoid preferred OIPVs emitted by tomato plants previously inoculated with T. harzianum T22 over OIPVs emitted by non‐inoculated plants. Furthermore, chemical analysis showed that root inoculation with T. harzianum T22 resulted in changes in the composition of OIPVs, which was consistent with the behavioural observations. Among the compounds that strongly contribute to the chemical differences between OIPVs from non‐inoculated and inoculated plants, chemical analysis identified green leaf volatiles ((Z)‐3‐hepten‐1‐ol, (E,E)‐2,4‐hexadienal), along with terpenoids (terpinen 4‐ol, α‐tujene and δ‐elemene).Taken together our results indicate that beneficial soil microbes enhance indirect plant defences induced by feeding and oviposition, broadening our understanding of plant responses to insect eggs. Our results underscore the importance of taking into account the role of microorganisms to fully comprehend the intricate interactions among plants, herbivore eggs and their associated egg parasitoids. Read the free Plain Language Summary for this article on the Journal blog. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Aims: Plant-beneficial fungi play an important role in enhancing plant growth and protecting plants from biotic and abiotic stresses. However, context-dependency of such effects and differences among fungi often lead to inconsistent results that hamper their widespread use. Here, we investigated the effect of plant-beneficial fungi on plant growth and herbivore resistance, and how effects are mediated by fertilization. Methods: Sweet pepper (Capsicum annuum L.) plants were root-inoculated with the plant-beneficial fungi Beauveria bassiana ARSEF 3097 and Trichoderma harzianum T22 and grown in a low-nutrient potting mix, with or without additional nutrients. Plant growth and herbivore resistance against the southern green stink bug (Nezara viridula L.) were compared between fungal treatments and fertilization levels by measuring several growth traits and quantifying feeding damage and plant defense-related gene expression. Results: Fertilization significantly increased plant growth, but at the same time made plants more susceptible to herbivory. Irrespective of fertilization, T. harzianum stimulated growth and reduced feeding damage (number of leaf punctures), while B. bassiana only enhanced growth. For both strains, fungal inoculation generally increased the expression of marker genes involved in salicylic acid- and jasmonic acid-dependent defense responses upon herbivory, but this was less pronounced for salicylic acid-dependent defense signaling under fertilization. Conclusions: We conclude that fungal inoculation improved plant growth and generally elicited a stronger defense response to stink bug feeding. Accordingly, plant damage was reduced by T. harzianum. Overall these results show that plant-beneficial fungi have the potential to promote plant growth and reduce feeding damage, irrespective of fertilization. [ABSTRACT FROM AUTHOR]

Concurrent releases of several species of natural enemies for pest control have been studied in various crops with either positive, neutral, or negative results. To control the pest Tuta absoluta (Meyrick) (Lepidoptera Gelechiidae), only the egg parasitoid Trichogramma pretiosum Riley (Hymenoptera Trichogrammatidae) is applied on many hectares with tomatoes in South America. Use of the mirid predator Macrolophus basicornis Stal (Hemiptera Miridae) is considered either alone or in combination with the parasitoid T. pretiosum. To determine if intraguild relationships between the two natural enemies negatively affect concurrent releases, unparasitized eggs and eggs parasitized by T. pretiosum were exposed to the predator. Knowing which stages of parasitized eggs are consumed or rejected by the predator is important for development of a release strategy resulting in highest pest mortality. M. basicornis consumed 1-2 day old parasitized eggs as well as unparasitized eggs, and, consequently, expressed strong intraguild predation (IGP). Five and 9-day old parasitized eggs were often not consumed, and, therefore, exerted the phenomenon of competitive exclusion (CE). Predation rates of old parasitized eggs were very low and similar in no-choice and choice tests, and in experiments with a large (100), medium (50) and very limited (10) number of preys offered, demonstrating a strong CE effect. Interestingly, in choice experiments with unparasitized and old parasitized eggs, predators started to consume unparasitized eggs significantly later than when only unparasitized or young parasitized eggs were offered. This suggests that old, parasitized eggs in some way reduce the foraging activity of M. basicornis. We expect that stronger pest reduction by concurrent releases of both natural enemies will only occur at the start of the tomato production season and when the egg parasitoid is introduced seven days before the mirid predator in order to reduce intraguild predation of parasitized eggs by the predator. [ABSTRACT FROM AUTHOR]

Polyphagous mirid predators are increasingly used in commercial, augmentative biological control. Information about their foraging behaviour is essential, especially if one intends to use several natural enemies to control one or more pests in a crop, to detect if negative intraguild effects occur. We studied a case of intraguild predation (IGP) involving the predator Macrolophus basicornis (Stal) (Hemiptera Miridae) of the worldwide invasive South American tomato leaf miner Tuta absoluta (Meyrick) (Lepidoptera Gelechiidae) and explored how this predator deals with prey parasitized by Trichogramma pretiosum (Riley) (Hymenoptera Trichogrammatidae). Behavioural observations show that M. basicornis predators contacted significantly fewer old, parasitized eggs of T. absoluta than recently parasitized eggs. Olfactometer tests revealed that predators could smell differences between volatiles of tomato leaves infested with eggs of different qualities to locate suitable prey. They preferred volatiles from leaflets with unparasitized eggs above control leaflets and, moreover, preferred volatiles from leaflets with recently parasitized eggs over volatiles of leaflets with 5-day-old parasitized eggs. When predators and parasitoids are used together to control T. absoluta, parasitoids should be introduced one week before predators are released to prevent high levels of IGP. [ABSTRACT FROM AUTHOR]

Many animals lay their eggs in clusters. Eggs on the periphery of clusters can be at higher risk of mortality. We asked whether the most commonly occurring clutch sizes in pentatomid bugs could result from geometrical arrangements that maximize the proportion of eggs in the cluster's interior. Although the most common clutch sizes do not correspond with geometric optimality, stink bugs do tend to lay clusters of eggs in shapes that protect increasing proportions of their offspring as clutch sizes increase. We also considered whether ovariole number, an aspect of reproductive anatomy that may be a fixed trait across many pentatomids, could explain observed distributions of clutch sizes. The most common clutch sizes across many species correspond with multiples of ovariole number. However, there are species with the same number of ovarioles that lay clutches of widely varying size, among which multiples of ovariole number are not overrepresented. In pentatomid bugs, reproductive anatomy appears to be more important than egg mass geometry in determining clutch size uniformity. In addition, our analysis demonstrates that groups of animals with little variation in ovariole number may nonetheless lay a broad range of clutch shapes and sizes. [ABSTRACT FROM AUTHOR]

Floral nectar is ubiquitously colonized by a variety of microorganisms among which yeasts and bacteria are the most common. Microorganisms inhabiting floral nectar can alter several nectar traits, including nectar odor by producing microbial volatile organic compounds (mVOCs). Evidence showing that mVOCs can affect the foraging behavior of insect pollinators is increasing in the literature, whereas the role of mVOCs in altering the foraging behavior of third-trophic level organisms such as insect parasitoids is largely overlooked. Parasitoids are frequent visitors of flowers and are well known to feed on nectar. In this study, we isolated bacteria inhabiting floral nectar of buckwheat, Fagopyrum esculentum (Polygonales: Polygonaceae), to test the hypothesis that nectar bacteria affect the foraging behavior of the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae) via changes in odors of nectar. In behavioral assays, we found that T. basalis wasps are attracted toward nectar fermented by 4 out of the 14 bacterial strains isolated, which belong to Staphylococcus epidermidis, Terrabacillus saccharophilus (both Firmicutes), Pantoea sp. (Proteobacteria), and Curtobacterium sp. (Actinobacteria). Results of chemical investigations revealed significant differences in the volatile blend composition of nectars fermented by the bacterial isolates. Our results indicate that nectar-inhabiting bacteria play an important role in the interactions between flowering plants and foraging parasitoids. These results are also relevant from an applied perspective as flowering resources, such as buckwheat, are largely used in agriculture to promote conservation biological control of insect pests. [ABSTRACT FROM AUTHOR]

The European tarnished plant bug, Lygus rugulipennis Poppius, is considered a major pest in chrysanthemum nurseries in The Netherlands. Adults puncture plant's apical meristem, after which the growing point splits and growth is inhibited. Flower buds and flowers can also be severely damaged. Both types of damage result in economic losses for growers. Despite the importance of this pest for chrysanthemum nurseries, there is only very limited information about L. rugulipennis development on chrysanthemum plants, Chrysanthemum × morifolium Ramat., and whether L. rugulipennis can be controlled using trap plants is not known. We investigated whether: (1) L. rugulipennis could develop from egg to adult on the vegetative and flowering stages of chrysanthemum; (2) their performance was enhanced when a supplemental prey source (Ephestia kuehniella Zeller eggs) or another common pest (the green peach aphid, Myzus persicae Sulzer) was present; and (3) there were alternative plant species more attractive than chrysanthemum for use as trap plants for local pest control or monitoring of L. rugulipennis. L. rugulipennis developed on both vegetative and flowering chrysanthemum stages without any additional food source. Nonetheless, when chrysanthemum was supplemented with E. kuehniella eggs, L. rugulipennis achieved the best performance in terms of the number of adults developed and faster developmental time. Interestingly, L. rugulipennis developed faster on chrysanthemum infested with the aphid M. persicae compared to non‐infested plants, however, there was no difference in the number of adults developed. In a trap plant experiment with 16 plant species in the vegetative stage, we found that white mustard, Sinapis alba L., was significantly more attractive than chrysanthemum to both adult and nymph L. rugulipennis. Further research is needed to evaluate the potential of S. alba as a trap plant for monitoring L. rugulipennis and how the presence of prey in the crop influences L. rugulipennis. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Invasive species, because of their lack of co-evolutionary history with recipient communities, can act as "evolutionary traps" causing disconnects between natural enemy behavioural responses and the suitability of the invasive species as a prey/host resource. Invasion of exotic species in non-native environments may have several ecological effects, including consequences for the experience-mediated behavioural responses of indigenous foragers. Experience is usually thought to help resident species to buffer against negative impacts of new invasive species, including escaping from evolutionary traps. Here we hypothesized that the impact of foraging experience depends on whether an indigenous egg parasitoid can correctly assess the resource suitability of a new invasive species for offspring development. We showed that the invasive stink bug Halyomorpha halys acts as an evolutionary trap for the indigenous egg parasitoid Trissolcus basalis leading to unsuccessful development of ~ 95% of the eggs laid in this host species. In a mixed scenario in which the associated resident stink bug Nezara viridula co-occurs with the invasive H. halys, we showed that oviposition experience in the low quality invasive host induces in T. basalis similar responses to those of the associated host. These results suggest that foraging experience does not lead to avoidance of an evolutionary trap. We discuss parasitoid foraging experience and reproductive success in the light of the evolutionary trap framework with implication for biological control. [ABSTRACT FROM AUTHOR]

Plant growth-promoting fungi belonging to genus Trichoderma are known to help plants when dealing with biotic stressors by enhancing plant defenses. While beneficial effects of Trichoderma spp. against plant pathogens have long been documented, fewer studies have investigated their effect on insect pests. Here, we studied the impact of Trichoderma root colonization on the plant defense responses against stink bug feeding attack. For this purpose, a model system consisting of tomato plant, Solanum lycopersicum cv Dwarf San Marzano, Trichoderma harzianum strain T22 and the southern green stink bug, Nezara viridula, was used. We firstly determined stink bug performance in terms of relative growth rate and survival on tomato plants inoculated by T. harzianum T22. Then, we evaluated relative expression of plant defense-related genes on inoculated plants induced by stink bug feeding. We found evidence that T. harzianum T22 affects tomato defense responses against N. viridula nymphs leading to reduction of growth rate. Our results also showed that T. harzianum T22 enhances plant direct defenses by an early increase of transcript levels of jasmonic acid marker genes. Yet this effect was time-dependent and only detected 8 h after herbivore induction. Taken together, our findings provide better understanding on the mechanisms underlying tomato induced resistance against herbivorous stink bugs. [ABSTRACT FROM AUTHOR]

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. © 2019 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. [ABSTRACT FROM AUTHOR]

Parasitoids depend on other insects for the development of their offspring. Their eggs are laid in or on a host insect that is consumed during juvenile development. Parasitoids harbor a diversity of microbial symbionts including viruses, bacteria, and fungi. In contrast to symbionts of herbivorous and hematophagous insects, parasitoid symbionts do not provide nutrients. Instead, they are involved in parasitoid reproduction, suppression of host immune responses, and manipulation of the behavior of herbivorous hosts. Moreover, recent research has shown that parasitoid symbionts such as polydnaviruses may also influence plant-mediated interactions among members of plant-associated communities at different trophic levels, such as herbivores, parasitoids, and hyperparasitoids. This implies that these symbionts have a much more extended phenotype than previously thought. This review focuses on the effects of parasitoid symbionts on direct and indirect species interactions and the consequences for community ecology. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Abstract: 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. [ABSTRACT FROM AUTHOR]

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 organismsmay 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. [ABSTRACT FROM AUTHOR]

Therophilus javanus is a koinobiont, solitary larval endoparasitoid currently being considered as a biological control agent against the pod borer Maruca vitrata, a devastating cowpea pest causing 20–80% crop losses in West Africa. We investigated ovary morphology and anatomy, oogenesis, potential fecundity, and egg load in T. javanus, as well as the effect of factors such as age of the female and parasitoid/host size at oviposition on egg load. The number of ovarioles was found to be variable and significantly influenced by the age/size of the M. vitrata caterpillar when parasitized. Egg load also was strongly influenced by both the instar of M. vitrata caterpillar at the moment of parasitism and wasp age. The practical implications of these findings for improving mass rearing of the parasitoid toward successful biological control of M. vitrata are discussed. [ABSTRACT FROM AUTHOR]

The lack of understanding of complex food-web interactions has been a major gap in the history of biological control. In particular, a better understanding of the functioning of pest food-webs and how they vary between native and invaded geographical ranges is of prime interest for biological control research and associated integrated pest management. Technical limitations associated with the deciphering of complex food-webs can now be largely overcome by the use of high throughput DNA sequencing techniques such as Illumina MiSeq. We tested the efficiency of this next generation sequencing technology in a metabarcoding approach, to study aphid food-webs using the cabbage aphid as model. We compared the variations in structure and composition of aphid food-webs in the species' native range (United Kingdom, UK) and in an invaded range (New Zealand, NZ). We showed that Illumina MiSeq is a well suited technology to study complex aphid food-webs from aphid mummies. We found an unexpectedly high top down pressure in the NZ cabbage aphid food-web, which coupled to a large ratio of consumer species / prey species and a lack of potential inter-specific competition between primary parasitoids, could cause the NZ food-web to be more vulnerable than the UK one. This study also reports for the first time the occurrence of a new hyperparasitoid species in NZ, as well as new associations between hyperparasitoids parasitoids and the cabbage aphid in this country. We conclude that the complexity of aphid food-webs in agricultural systems could often be underestimated, particularly at higher trophic levels; and that the use of high throughput DNA sequencing tools, could largely help to overcome this impediment. [ABSTRACT FROM AUTHOR]

Due to a growing demand of food production worldwide, new strategies are suggested to allow for sustainable production of food with minimal effects on natural resources. A promising alternative to the application of chemical pesticides is the implementation of crops resistant to insect pests. Plants produce compounds that are harmful to a wide range of attackers, including insect pests; thus, exploitation of their natural defense system can be the key for the development of pest-resistant crops. Interestingly, some plants possess a unique first line of defense that eliminates the enemy before it becomes destructive: egg-killing. Insect eggs can trigger (1) direct defenses, mostly including plant cell tissue growth or cell death that lead to eggs desiccating, being crushed or falling off the plant or (2) indirect defenses, plant chemical cues recruiting natural enemies that kill the egg or hatching larvae (parasitoids). The consequences of plant responses to eggs are that insect larvae do not hatch or that they are impeded in development, and damage to the plant is reduced. Here, we provide an overview on the ubiquity and evolutionary history of egg-killing traits within the plant kingdom including crops. Up to now, little is known on the mechanisms and on the genetic basis of egg-killing traits. Making use of egg-killing defense traits in crops is a promising new way to sustainably reduce losses of crop yield. We provide suggestions for new breeding strategies to grow egg-killing crops and improve biological control. [ABSTRACT FROM AUTHOR]

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]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Research on interspecific competitive interactions among insect parasitoids has often been characterized by laboratory studies in which host insects are exposed to female parasitoids of different species in various sequences and combinations. In the last years, an increasing number of studies have investigated interspecific interactions under field and semi-field conditions although just a few number of works focused on egg parasitoids. In this work, we undertook a two-year study to investigate interspecific interactions between Trissolcus basalis (Wollaston) (Hymenoptera: Platygastridae) and Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae), two egg parasitoids of the pest Nezara viridula (L.) (Heteroptera: Pentatomidae) that co-occur in cultivated crops. Under semi-field (in out-door mesh cages) and field conditions, we investigated: 1) the seasonal occurrence of competing parasitoid species on sentinel egg masses; 2) the impact achieved by competing species on the shared host on naturally laid egg masses; 3) the outcome of intraguild interactions under controlled conditions. Results from sentinel egg masses showed that T. basalis occurs in May and successfully parasitizes hosts until the end of September/beginning of October, whereas O. telenomicida is mainly occurring in July-August. In both years, it was found that T. basalis is predominant. From naturally laid egg masses, results indicated that T. basalis achieves higher impact on the hosts, even in those egg masses which are parasitized by more than one female of different species ( =  multiparasitism). Results from manipulating intraguild interactions showed that T. basalis achieves higher impact on N. viridula when released alone, but it suffers from competition with O. telenomicida. The ecological factors that play a role in intraguild interactions in the context of biological control perspective are discussed. [ABSTRACT FROM AUTHOR]

Hymenopteran parasitoids can utilize substrate-borne semiochemicals released by conspecifics or by their hosts, increasing the likelihood of successful mating and host location. According to the literature, two substrate-borne chemo-orientation patterns can occur: (1) biased random searching, a non-directional reaction toward the chemicals (kinesis), and (2) trail-following searching, a directional response toward the source emitting the chemical compounds (taxis). These two different strategies can be adopted by parasitoids to locate hosts and mates. In host location, random searching is induced by allelochemicals indirectly associated with the host, whereas trail-following behavior is induced by allelochemicals directly emitted by the target organism. In mate finding, sex pheromones emitted by conspecifics can induce either the random searching or the trail-following behavior, although the spatial distribution of virgin conspecifics could be an important factor driving the evolution of substrate-borne chemo-orientation patterns. The chemical nature of substrate-borne semiochemicals has not yet been fully elucidated. Most studies have shown that crude extracts are biologically active for eliciting parasitoid arrestment response, but few studies have clearly characterized their chemical nature. However, experimental evidence indicates that cuticular lipids located in the external layer of insects' bodies play a role in parasitoid-parasitoid and host-parasitoid communication. The ecological role of parasitoid chemo-orientation in host and mate location is discussed from a biological control perspective. [ABSTRACT FROM AUTHOR]

We investigated intraguild interactions between two egg parasitoids of Nezara viridula (L.) (Heteroptera: Pentatomidae), Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae) and Trissolcus basalis (Wollaston) (Hymenoptera: Platygastridae), as the former has the potential to be a facultative hyperparasitoid of the latter. We assessed the suitability of N. viridula eggs for the development of O. telenomicida as a function of egg age when they were unparasitized, or had been attacked by T. basalis at different times prior to exposure to O. telenomicida females. Ooencyrtus telenomicida can exploit healthy N. viridula host eggs up to 5 days of age, just prior to the emergence of N. viridula. This window of opportunity can be extended for an additional 6–7 days through interspecific competition or facultative hyperparasitism. While there are minor fitness costs for O. telenomicida as the result of interspecific larval competition, those costs are greater with facultative hyperparasitism. In choice assays O. telenomicida females discriminated between different quality N. viridula eggs, avoiding those where their progeny would have to develop as facultative hyperparasitoids of T. basalis. Results are discussed with respect to the possible effects that the costs of intraguild parasitism might have on biological control programmes. [ABSTRACT FROM AUTHOR]

Interspecific competitive interactions can occur either between adult parasitoids searching/exploiting hosts (extrinsic competition) or between parasitoid larvae developing within the same host (intrinsic competition). Understanding how interspecific competition between parasitoids can affect pest suppression is important for improving biological pest control. The purpose of this work was to review both extrinsic and intrinsic competition between egg parasitoid species. These are organisms that are often candidates for biological control programs due to their ability to kill the pest before the crop feeding stage. We first reviewed the literature about interspecific competitive abilities of adult parasitoids in terms of comparative host location strategies highlighting which ecological and behavioral factors are likely to shape extrinsic competition. Then we focused on the interspecific competitive interactions between immatures developing within the same host taking into account which factors play a key role in the outcome of intrinsic competition. Finally we conclude stressing on the need to elucidate the overall competitive interaction that parasitoid species may experience in the field in order to enhance biological control success. [ABSTRACT FROM AUTHOR]

Ongoing studies by our group showed that the outcome of the intrinsic competition between two solitary egg parasitoids, Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) and Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae), is dominated by O. telenomicida. In this article we investigated the role played by the ovipositing O. telenomicida female in the suppression of a T. basalis competitor. Laboratory experiments were conducted by allowing an O. telenomicida female to puncture the eggs of Nezara viridula (L.) (Heteroptera: Pentatomidae) with her ovipositor (= no oviposition) or to parasitize them. The results show that O. telenomicida relies on some physiological mechanisms to mediate its interspecific intrinsic competition with T. basalis. In fact, the emergence of T. basalis was strongly reduced in host eggs that were parasitized either before or after being punctured by O. telenomicida at fixed time intervals (5, 15, 30, or 45 h). The low percentage of emergence of T. basalis (ranging from approximately 4-20%) was a consequence of the delay and growth rate reduction of larval development. Furthermore, the percentage of eclosion of N. viridula nymphs was negatively affected by the O. telenomicida female's punctures (96% from healthy host eggs, 4% from punctured host eggs). Host eggs punctured or oviposited in by O. telenomicida showed alterations in the ooplasm including some melanized-like areas near the hole made with the ovipositor; such alterations indicate that the adult parasitoid releases substances that affect the host eggs survival. These results suggest that the O. telenomicida female influences both the physiological interspecific parasitoid-parasitoid interaction, as well as the host-parasitoid interaction, providing, for the first time in egg parasitoids, evidence that physiological suppression of some competitive egg parasitoids is mediated by the ovipositing female. [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]

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 to C, 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. [ABSTRACT FROM AUTHOR]

The response of the generalist egg parasitoid Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae) to host-related chemical cues from tomato plants, Solanum lycopersicum L., and adults of Nezara viridula (L.) (Heteroptera: Pentatomidae) was investigated in laboratory-based no-choice and paired-choice tests. In Y-tube olfactometer experiments, when female wasps were exposed to volatiles from plants in different conditions, they were attracted only to volatiles produced by N. viridula adult-infested tomato plants. When female wasps were exposed to adults of N. viridula, they were attracted to volatiles from virgin males, and, at a lower level, to volatiles from mated females in preoviposition state. Finally, studies in open arena showed that chemical footprints left by adults of N. viridula did not induce arrestment responses in wasp females. These results are discussed in terms of extrinsic competition with other beneficial egg parasitoids that in field can compete for the same egg mass, since intraguild interactions may affect the success of a biological control program. [ABSTRACT FROM AUTHOR]

Intraguild interactions between two egg parasitoids, Trissolcus basalis (Hymenoptera: Scelionidae) and Ooencyrtus telenomicida (Hymenoptera: Encyrtidae), exploring egg masses of the Southern Green Stink Bug (SGSB) Nezara viridula (Heteroptera: Pentatomidae), were investigated in laboratory conditions by single, simultaneous and sequential host attack experiments. Mortality of N. viridula eggs was higher in simultaneous and sequential releases compared to single species releases. In simultaneous host exploitations, T. basalis females displayed an aggressive behavior against O. telenomicida females. The outcome of multiparasitism showed that interspecific larval competition was dominated by O. telenomicida regardless of the sequence in which oviposition occurred and which parasitoid was or was not simultaneously released in the patch. Finally, O. telenomicida can successfully develop in hosts already parasitized by T. basalis up to seven days earlier, acting as a facultative hyperparasitoid, so that intraguild predation (IGP) also occurred. The ecological factors that allow species coexistence and the role played by competition in biological control programs are discussed. [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]