Fitness costs of intrinsic competition in two egg parasitoids of a true bug

2015

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 ovipo…

Intraguild interactions between two egg parasitoids exploring host patches

2010

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…

Nectar-Inhabiting Bacteria Affect Olfactory Responses of an Insect Parasitoid by Altering Nectar Odors

2022

AbstractFloral 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 buckwhe…

An Insight in the Reproductive Biology of Therophilus javanus (Hymenoptera, Braconidae, and Agathidinae), a Potential Biological Control Agent agains…

2017

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 parasit…

Disentangling higher trophic level interactions in the cabbage aphid food web using high-throughput DNA sequencing

2017

International audience; 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 cab…

Influence of parasitoid-associated viral symbionts on plant–insect interactions and biological control

2021

International audience; Insect parasitoids have evolved symbiotic interactions with several viruses and thousands of parasitoid species have established mutualistic associations with polydnaviruses (PDVs). While PDVs have often been described as virulence factors allowing development of immature parasitoids inside their herbivore hosts, there is increasing awareness that PDVs can affect plant-insect interactions. We review recent literature showing that PDVs alter not only host physiology, but also feeding patterns and composition of herbivore's oral secretions. In turn PDV-induced changes in herbivore phenotype affect plant responses to herbivory with consequences ranging from differential…

The invasive stink bug Halyomorpha halys affects the reproductive success and the experience-mediated behavioural responses of the egg parasitoid Tri…

2021

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…

Mating Status of an Herbivorous Stink Bug Female Affects the Emission of Oviposition-Induced Plant Volatiles Exploited by an Egg Parasitoid

2019

Insect parasitoids are under selection pressure to optimize their host location strategy in order to maximize fitness. In parasitoid species that develop on host eggs, one of these strategies consists in the exploitation of oviposition-induced plant volatiles (OIPVs), specific blends of volatile organic compounds released by plants in response to egg deposition by herbivorous insects. Plants can recognize insect oviposition via elicitors that trigger OIPVs, but very few elicitors have been characterized so far. In particular, the source and the nature of the elicitor responsible of egg parasitoid recruitment in the case of plants induced with oviposition by stink bugs are still unknown. In …

Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids

2018

Symbiotic relationships benefit organisms in utilization of new niches. In parasitoid wasps, symbiotic viruses and venom that are injected together with wasp eggs into the host caterpillar suppress immune responses of the host and enhance parasitoid survival. We found that the virus also has negative effects on offspring survival when placing these interactions in a community context. The virus and venom drive a chain of interactions that includes the herbivore and its food plant and attracts the hyperparasitoid enemies of the parasitoid. Our results shed new light on the importance of symbionts associated with their host in driving ecological interactions and highlight the intricacy of how…

Egg parasitoid attraction toward induced plant volatiles is disrupted by a non-host herbivore attacking above or belowground plant organs.

2014

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 …

Behavioral responses of the parasitoidMelittobia digitatato volatiles emitted by its natural and laboratory hosts

2010

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 …

I batteri associati al nettare fiorale influiscono sulle longevità degli insetti parassitoidi

2023

I parassitoidi adulti frequentemente visitano le piante in fioritura, ricercando nettare fiorale per coprire i loro bisogni energetici e nutrizionali. In letteratura, infatti, i benefici del nettare sulla fitness dei parassitoidi sono ampiamente documentati. Sebbene il nettare fiorale costituisca un substrato ideale per la crescita di comunità microbiche che possono alterarne le caratteristiche organolettiche, l'effetto della fermentazione batterica del nettare sui parassitoidi non è stato ancora sufficientemente esplorato. In questo lavoro è stata studiata la longevità dei parassitoidi adulti utilizzando nettare sintetico fermentato da diversi ceppi batterici appartenenti ai phyla Firmicut…

The ovipositing female of Ooencyrtus telenomicida relies on physiological mechanisms to mediate intrinsic competition with Trissolcus basalis

2012

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 mechan…

Chemo-orientation responses in hymenopteran parasitoids induced by substrate-borne semiochemicals

2013

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) trailfollowing 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 indu…

Plant-phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars

2021

Early Access; International audience; 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…

Impact of parasitoid-associated polydnaviruses on plant-mediated herbivore interactions

2022

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 parasit…

Attraction of Trichogramma Wasps to Butterfly Oviposition-Induced Plant Volatiles Depends on Brassica Species, Wasp Strain and Leaf Necrosis

2021

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 r…

How to escape from insect egg parasitoids : a review of potential factors explaining parasitoid absence across the Insecta

2020

The egg is the first life stage directly exposed to the environment in oviparous animals, including many vertebrates and most arthropods. Eggs are vulnerable and prone to mortality risks. In arthropods, one of the most common egg mortality factors is attack from parasitoids. Yet, parasitoids that attack the egg stage are absent in more than half of all insect (sub)orders. In this review, we explore possible causes explaining why eggs of some insect taxa are not parasitized. Many insect (sub)orders that are not attacked by egg parasitoids lack herbivorous species, with some notable exceptions. Factors we consider to have led to escape from egg parasitism are parental egg care, rapid egg deve…

Escaping the evolutionary trap: Can size-related contest advantage compensate for juvenile mortality disadvantage when parasitoids develop in unnatur…

2021

Abstract 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 co…

Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores

2018

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 colon…

Thermal stress affects patch time allocation by preventing forgetting in a parasitoid wasp

2015

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 ex…

First extensive characterization of the venom gland from an egg parasitoid: structure, transcriptome and functional role.

2018

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 functio…

First report of Melittobia australica Girault in Europe and new record of M. acasta (Walker) for Italy

2012

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.

Interspecific extrinsic and intrinsic competitive interactions in egg parasitoids

2012

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…

Foraging behaviour of an egg parasitoid exploiting plant volatiles induced by pentatomids : The role of adaxial and abaxial leaf surfaces

2017

Several phases of herbivorous insect attack including feeding and oviposition are known to induce plant defenses. Plants emit volatiles induced by herbivores to recruit insect parasitoids as an indirect defense strategy. So far, volatiles induced by herbivore walking and their putative role in the foraging behavior of egg parasitoids have not been investigated. In this paper we studied the response of the egg parasitoid Trissolcus basalis toward volatiles emitted by Vicia faba plants as consequence of the walking activity of the host Nezara viridula. Olfactometer bioassays were carried out to evaluate wasp responses to plants in which the abaxial or the adaxial surfaces were subjected to wa…

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

2019

Insects typically forage in complex habitats in which their resources are surrounded by non-resources. For herbivores, pollinators, parasitoids, and higher level predators research has focused on how specific trophic levels filter and integrate information from cues in their habitat to locate resources. However, these insights frequently build specific theory per trophic level and seldom across trophic levels. Here, we synthesize advances in understanding of insect foraging behavior in complex habitats by comparing trophic levels in specialist host-parasitoid-hyperparasitoid systems. We argue that resources may become less apparent to foraging insects when they are member of higher trophic …

Prospects of herbivore egg-killing plant defenses for sustainable crop protection

2016

Abstract 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 i…

Intraguild interactions between two egg parasitoids of a true bug in semi-field and field conditions.

2014

International audience; 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 para…

Semiochemical exploitation of host-associated cues by seven Melittobia parasitoid species : Behavioral and phylogenetic implications

2018

Chemical compounds (infochemicals or semiochemicals) play an important role both in intra-specific and inter-specific communication. For example, chemical cues appear to play a key role in the host selection process adopted by insect parasitoids. In recent years significant advances have been made in order to understand the chemical ecology of insect parasitoids. However, little information is available about the evolution of semiochemical use in the host location process of insect parasitoids. Here we investigated the strategy adopted by seven closely related parasitoid species in the genus Melittobia when foraging for four different suitable hosts. By using an integrated approach that com…

Only Females Oviposit: Chemical Discrimination of Adult Stink Bug Sex by the Egg Parasitoid Trissolcus japonicus

2021

Egg parasitoids foraging for suitable hosts scattered in the environment rely mainly on chemical cues. Elucidating the chemical ecology of natural enemies is important in the development of effective and successful strategies for conservation biological control. In this context, the host cuticular hydrocarbons, which are exploited by several species of egg parasitoids as contact kairomones, could be used to retain them by providing information about the presence and the sex of adults of the target species: sex is important because only females of the host species lay the eggs that can be subsequently utilized for parasitoid reproduction. However, the chemical basis of host sex discriminatio…

Application of Chemical Cues in Arthropod Pest Management for Orchards and Vineyards

2013

This chapter reviews the literature on semiochemical-parasitoid systems in perennial crops. The first part of the chapter analyses the possible effects of pheromone-based tactics on parasitoid efficacy. In both orchards and vineyards, the most successful application of synthetic sex pheromones has been their use as mating disruptants. It also discusses the possibility of using parasitoid pheromones to directly affect parasitoid behaviour. The second part of the chapter summarizes research in orchards and vineyards that has tested whether synthetic chemical cues such as herbivore-induced plant volatiles (HIPVs) and host-associated volatiles (HAVs) can be used to manipulate parasitoid behavio…

The role of contact chemoreception in the host location process of an egg parasitoid

2016

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: Pentat…

Evaluating the quality of the Mexican fruit-fly, Anastrepha ludens, as host for the parasitoid Melittobia digitata

2013

We investigated the presence of Melittobia digitata (Hymenoptera: Eulophidae) and its associations with its natural hosts in Veracruz, Mexico. The parasitoid was confirmed to be present and found to attack prepupae of Trypoxylon and Sceliphron (Hymenoptera: Crabronidae and Sphecidae, respectively) mud daubers as well as pupae of the Mexican fruit fly Anastrepha ludens (Diptera: Tephritidae). Since A. ludens is a very important pest of citrus and mango in Mexico and Central America, we evaluated, in laboratory experiments, the quality of A. ludens as host of M. digitata comparing the development of the parasitoid in another unrelated fly species (Sarcophaga [Neobellieria] bullata) (Diptera: …

Behavioral and Chemical Investigations of Contact Kairomones Released by the Mud Dauber Wasp Trypoxylon politum, a Host of the Parasitoid Melittobia …

2011

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 ex…

Behavioral response of the egg parasitoid Ooencyrtus telenomicida to host-related chemical cues in a tritrophic perspective

2010

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 preov…

Testing the habituation assumption underlying models of parasitoid foraging behavior

2016

BackgroundHabituation, a form of non-associative learning, has several well-defined characteristics that apply to a wide range of physiological and behavioral responses in many organisms. In classic patch time allocation models, habituation is considered to be a major mechanistic component of parasitoid behavioral strategies. However, parasitoid behavioral responses to host cues have not previously been tested for the known, specific characteristics of habituation.MethodsIn the laboratory, we tested whether the foraging behavior of the egg parasitoidTrissolcus basalisshows specific characteristics of habituation in response to consecutive encounters with patches of host (Nezara viridula) ch…

Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests

2020

Abstract 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 p…

Competitive interactions in insect parasitoids: effects of microbial symbionts across tritrophic levels

2023

Competition for hosts is a common ecological interaction in insect parasitoids. In the recent years, it has become increasingly evident that microorganisms can act as ‘hidden players’ in parasitoid ecology. In this review, we propose that parasitoid competition should take into consideration the microbial influence. In particular, we take a tritrophic perspective and discuss how parasitoid competition can be modulated by microorganisms associated with the parasitoids, their herbivore hosts, or the plants attacked by the herbivores. Although research is still in its infancy, recent studies have shown that microbial symbionts can modulate the contest outcome. The emerging pattern is that micr…

Trichoderma harzianum Strain T22 Modulates Direct Defense of Tomato Plants in Response to Nezara viridula Feeding Activity

2021

AbstractPlant 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 rela…

Volatile-mediated foraging behaviour of three parasitoid species under conditions of dual insect herbivore attack

2016

Infochemicals play an important role in structuring intra-and interspecific interactions. Many parasitoid wasp species rely on herbivory or oviposition-induced plant volatiles (HIPVs/OIPVs) to locate their herbivorous hosts, and must cope with variation in the volatile blends due to factors such as plant/host species, herbivore density or attack by several herbivores. However, little is known about how dual herbivory or changes in herbivore density affect multiple parasitoid species, each attacking a different herbivore, in the same system. In a natural system, we investigated the effect of dual attack on the ability of three parasitoid species to differentiate between volatiles induced by …

The response of an egg parasitoid to substrate-borne semiochemicals is affected by previous experience

2016

AbstractAnimals 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 …

Microbial symbionts of parasitoids

2020

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…

Attraction of egg-killing parasitoids toward induced plant volatiles in a multi-herbivore context

2015

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 nigr…

Interspecific competition/facilitation among insect parasitoids.

2015

Competition for limited resources is a widespread ecological interaction in animals. In the case of insect parasitoids, species can compete for host resources both at the adult stage as well as at the larval stage. Interspecific competition can play a role in sizing and shaping community structures. In addition of being relevant for basic ecological studies, understanding how interspecific competition between parasitoids affects pest suppression is important for biological control. In this opinion paper we review recent advances in the field of interspecific competition among parasitoids in a biological control perspective. We first discuss adult competition, highlighting which factors are …

Diversity and composition of the microbiome associated with eggs of the Southern green stinkbug, Nezara viridula (Hemiptera: Pentatomidae).

2022

Although microbial communities of insects from larval to adult stage have been increasingly investigated in recent years, little is still known about the diversity and composition of egg-associated microbiomes. In this study, we used high-throughput amplicon sequencing and quantitative PCR to get a better understanding of the microbiome of insect eggs and how they are established using the Southern green stinkbug Nezara viridula (L.) (Hemiptera: Pentatomidae) as a study object. First, to determine the bacterial community composition, egg masses from two natural populations in Belgium and Italy were examined. Subsequently, microbial community establishment was assessed by studying stinkbug e…

Hyperparasitoids exploit herbivore-induced plant volatiles during host location to assess host quality and non-host identity

2019

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 th…

The Ecology of Hyperparasitoids.

2021

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 nutri…

Contrasting reproductive traits of competing parasitoids facilitate coexistence on a shared host pest in a biological control perspective

2022

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 …

Intraguild interactions between egg parasitoids: window of opportunity and fitness costs for a facultative hyperparasitoid.

2013

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. viri…

Indagini sulle infestazioni di Aphis gossypii Glover su melone invernale (Cucumis melo Var. Helios) in aziende a conduzione biologica della Sicilia o…

2011

Investigations on the aphid infestation occurring on winter melon crops (Cucumis melo var. Helios) in organic farms of western Sicily The winter melon (Cucumis melo L.) is an important crop in Sicily. Previous studies carried out in western Sicily have shown that the aphid species Aphis gossipii is the key pest of winter melon crops.A. gossypii is a cosmopolitan species with very polyphagous habits; this phytophagous insect is capable of serious economic damage due to direct feeding of the sap plant and due to the honeydew secretion and the consequent presence of sooty mold and due to the possible transmission of viruses. The aim of this work was to investigate the levels of aphid infestati…

Lygus rugulipennis on chrysanthemum : Supplemental prey effects and an evaluation of trap plants

2022

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…

Climate change impact on extrinsic and intrinsic competition between egg parasitoids

2012

Climate changing is a real phenomenon and the last decade was the warmest decade ever. The impact of climate change on animal communities is complex, affecting species interactions in all trophic levels, in different ways and in different bio-geographic zones. Here we will discuss about the possible effects of climate changes in shaping the competition between egg parasitoid species to consume the same hosts. Egg parasitoids are important biological control agents due to their ability to kill the pest before the crop-feeding stages emerge. Competitive effects can be divided in “extrinsic competition”, the indirect interactions between adult females searching for hosts, and “intrinsic compet…

How can two competing egg parasitoid species coexist in a host patch?

2013

Interspecific competitions among parasitoids can affect community structures, and, as a consequence at applicative level, biological control programs. For example, competitions can cause local displacement of inferior species or niche separation. However, the coexistence of species attacking the same host is possible when they adopt different strategies to exploit the resource. In this work we evaluated in field and semi-field conditions intraguild interactions between two egg parasitoids, Trissolcus basalis and Ooencyrtus telenomicida exploring egg masses of Nezara viridula. In semi-field trials, pepper plants were covered with mesh net creating small cages with five plants inside. In each…

Effect of dual biotic stress on plant volatile synomones used by egg parasitoids

2014

Studies on semiochemical communication have demonstrated that broad bean plant, Vicia faba, emits volatile synomones induced by feeding and oviposition activities of the southern green stink bug, Nezara viridula, which recruit the egg parasitoid Trissolcus basalis. However plants growing in agro-ecosystems can be attacked by several herbivore species that could affect both above and belowground plant tissues with possible consequences for parasitoid recruitment. For example, broad bean plants can also be attacked by the leaf weevil, Sitona lineatus, and simultaneous attacks by the southern green stink bug and the leaf weevil can occur in agro- ecosystems. The purpose of this work was to inv…

The behavioral responses of the egg parasitoid Ooencyrtus telenomicida to semiochemicals from first and second trophic level

2009

In this study the responses of females of the egg parasitoid Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae) to volatile and contact chemicals from its host Nezara viridula (L.) (Heteroptera: Pentatomidae) and from host plant Solanum lycopersicum L. were investigated in a Y-tube olfactometer and in open arena. Our results in the Y-tube olfactometer tests showed that: (1) female wasps were attracted to volatiles from adult host virgin male and to volatiles from a host mated female, showing a clear preference for the volatiles emitted from the former; volatiles from host virgin females did not attract O. telenomicida females; (2) only volatiles produced by host-damaged plant com…

Intraguild interaction between egg parasitoids: the role of the host egg mass size and parasitoids’ reproductive capacities

2013

In Sicily, field collections of egg masses of the southern green stink bug, Nezara viridula (L.) (Heteroptera:Pentatomidae), revealed that two solitary parasitoids, Trissolcus basalis (Wollaston) (Hymenoptera: Platygastridae) and Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae), can exploit the same egg mass. Previous finding showed that parasitoid species differ in host location and larval competitive abilities and a host finding-larval competition trade-off may be important for coexistence. The aim of this work was to evaluate the role played by the host egg mass size and the importance of species reproductive capacities in the outcome of interspecific competition. Under labo…

Intraguild interactions between two egg parasitoids of a true bug: from laboratory to field investigations

2011

Intraguild interactions can play a role in species coexistence and in sizing and shaping community structures. In addition, understanding how competitive interactions between parasitoid guilds can affect pest suppression may improve biological control. Interspecific competitive effects can be divided in “extrinsic competition”, the indirect interactions between adult females searching for or exploiting hosts, and “intrinsic competition”, the competition that occurs between larvae developing in the same host. In this work we performed both laboratory and field investigations to address on intraguild interactions occurring between Trissolcus basalis (Hymenoptera: Scelionidae) and Ooencyrtus t…

Indagine su Henosepilachna elaterii (Rossi) (=Epilachna chrysomelina (F.)) e Raphidopalpa foveicollis (Lucas) in meloneti biologici della Sicilia occ…

2011

Investigations on Henosepilachna elaterii (Rossi) and Raphidopalpa foveicollis (Lucas) in an organic cultivation of winter melon in western Sicily. A study on H. elaterii and R. Foveicollis, serious pests of winter melon, was conducted in two organic melon fields of the western Sicily. Dynamics of population and infestation levels were investigated. In addition, the possible influence of mulching on R. Foveicollis infestation has been taken into account. Our results showed that H. elaterii occurred only in one field from the beginning of June and it infested 60% of the plants in the mid-July, then the pest population density dropped to about 10%. R. foveicollis occurred in both locations fr…

Outcomes of intraguild interactions between two egg parasitoids in field and semi-field conditions

2012

Intraguild interactions between two egg parasitoids, Trissolcus basalis (Wollaston) and Ooencyrtus telenomicida (Vassiliev) exploring egg masses of the Southern Green Stink Bug Nezara viridula (L.) were investigated in field and semi-field conditions. Field trials were conducted in tomato fields by using sentinel and naturally laid egg masses in 2010 and 2011. Egg parasitoids monitoring, by sentinel egg masses placed weekly on plants during the tomato growing season and recollected one week later, showed that T. basalis occurs from June to October, whereas O. telenomicida occurs mainly in July and August. In the same fields, collections of naturally laid egg masses display different types o…

Behavioral responses of the parasitoid Melittobia digitata to volatiles emitted by its natural and laboratory hosts

2010

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 ofmud 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 n…

The parasitoid complex of Prays oleae (Bern.) in organic olive orchard.

2007

I semiochimici utilizzati nella localizzazione dell’ospite da parte del parassitoide oofago Ooencyrtus telenomicida

2009

Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae) è un parassitoide oofago di Nezara viridula (L.) (Heteroptera: Pentatomidae) di origine paleartica frequentemente diffuso in Sicilia. Scopo del presente lavoro è stato quello di investigare il processo di localizzazione dell’ospite nel sistema tritrofico Solanum lycopersicum L. – N. viridula – O. telenomicida. In particolare sono stati condotti esperimenti in olfattometro a Y, per valutare il ruolo attrattivo dei composti volatili emessi sia dalle piante, sia dagli adulti della cimice verde, e in arena aperta, per biosaggiare. la risposta delle femmine del parassitoide alle tracce lasciate sul substrato dagli adulti di N. viridul…

Integrating natural enemies and semiochemicals in cultural control for an effective IPM

2012

Since their discovery, many semiochemicals (behavior modifying chemicals) have been identified and synthetized, and a number of techniques have been developed to use them in integrated pest management (IPM) programs against insect pests. In particular, the uses of semiochemicals in IPM to monitor insect pest populations and to interfere with their behavior preventing agricultural damage are widely adopted by the growers. In the same time, evidences that semiochemicals can also modify the behavior of insect natural enemies inspired researchers to explore the possibility to use semiochemicals to conserve and/or enhance the efficacy of natural enemies in cropping systems. However the use of se…

Indagine su Raphidopalpa foveicollis (Lucas) nella coltura del melone biologico della Sicilia occidentale.

2012

Investigations on Raphidopalpa foveicollis (Lucas) in an organic cultivation of winter melon in western Sicily Red pumpkin beetle (Raphidopalpa foveicollis), is a Chrysomelidae beetle that lives on various species of cucurbits with greater preference for Cucumis sp. Both larval and adult stages are injurious to the crops. The former feeds on roots and stems of the plants, while the latter feeds on foliage, petals and fruits. In Sicily, this insect has occurred in the past as a secondary pest on the winter melon, but sometimes it reaches levels of infestation to arouse considerable concern among farmers. In order to implement economic methods of pest control a study on organic cultivation of…

Studio sul complesso parassitario di Prays oleae (Bernard) e sui livelli di parassitizzazione in un oliveto biologico della Sicilia occidentale.

2009

Study on the parasitoid complex of Prays oleae (Bernard) and parasitism levels in an organic olive orchard in western Sicily (Italy). Prays oleae is a serious pest of the olive tree in the Mediterranean basin. This phytophagous infests fruits (carpophagous generation) and leaves (phyllophagous generation). In cases of high population densities crop losses, caused mainly by fruit drop, may be heavy. The aim of this work was to investigate on 1) parasitoid species living on P. oleae, 2) their incidence parasitoid complex, 3) parasitism levels and 4)the influence on the fruit fall. Observations were conducted in an organic olive grove near Contessa Entellina (PA) (Sicily, Italy) (37.43.44 N; 1…

Supplementary material 3 from: Lefort M, Wratten S, Cusumano A, Varennes Y, Boyer S (2017) Disentangling higher trophic level interactions in the cab…

2018

Exploratory statistics addressing sequencing depth per country and MOTU rarefaction.

Supplementary material 2 from: Lefort M, Wratten S, Cusumano A, Varennes Y, Boyer S (2017) Disentangling higher trophic level interactions in the cab…

2018

Supporting Information 2

Supplementary material 1 from: Lefort M, Wratten S, Cusumano A, Varennes Y, Boyer S (2017) Disentangling higher trophic level interactions in the cab…

2018

OSR aphid mummy collection. Sampling location and size / Amplification success of mummies' DNA extracts by Illumina sequencing.

Data from: Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids

2018

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 multi-trophic 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 …

Data from: Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores

2018

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 o…