Search

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.

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 vola-tiles 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.

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 re-leases, 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. Interest-ingly, in choice experiments with unparasitized and old parasitized eggs, predators started to consume unparasitized eggs signifi-cantly 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 par

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.

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.

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 harbor a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behavior. 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 ichnoviruses-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., 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 harbor a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behavior. 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 ichnoviruses-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.

Within the Brassicaceae, wild as well as crop species are challenged by specialist herbivores including cabbage white butterflies (Pieris spp.). The wild crucifer Brassica nigra responds to oviposition by Pieris butterflies by the synergistic expression of two egg-killing traits. Genotypes that express a hypersensitive response (HR)-like necrosis (direct egg-killing) also emit oviposition-induced plant volatiles (OIPVs) attracting Trichogramma egg parasitoids (indirect egg-killing). This so-called double defense line can result in high butterfly egg mortalities. It remains unknown whether this strategy is unique to B. nigra or more common in Brassica species. To test this, we examined the response of different Trichogramma evanescens lines to OIPVs emitted by B. nigra and three close relatives (Brassica napus, Brassica rapa, and Brassica oleracea). Furthermore, we evaluated whether HR-like necrosis played a role in the attraction toward plant volatiles. Our results show a specificity in wasp attraction to different plant species. Three out of four plant species attracted a specific T. evanescens strain, including the crops B. rapa and B. napus. Parasitoid attraction was positively affected by presence of HR-like necrosis in one plant species. Our findings imply that, despite being a true generalist in terms of host range, T. evanescens shows intraspecific variation during host searching, which should be taken into account when selecting parasitoid lines for biocontrol of certain crops. Finally, we conclude that also crop plants within the Brassicaceae family possess egg-killing traits and can exert the double-defense line which may enable effective selection of egg-killing defense traits by cabbage breeders.