Nina E. Fatouros

Wageningen University & Research | WUR · Department of Biosystematics

Knowledge of plant recognition of insects is largely limited to a few resistance ( R ) genes against sap‐sucking insects. Hypersensitive response (HR) characterizes monogenic plant traits relying on R genes in several pathosystems. HR‐like cell death can be triggered by eggs of cabbage white butterflies ( Pieris spp.), pests of cabbage crops ( Bras...

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...

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) in...

The hypersensitive response (HR) characterizes monogenic qualitative resistance traits in several pathosystems. Knowledge on its role in plant resistance to insects is so far limited to a few resistance ( R ) gene-based resistances against piercing-sucking insects. Egg deposition by cabbage white butterflies ( Pieris spp.), pests of cabbage crops (...

Foraging parasitoids rely on infochemicals, derived from the habitat, host plant and/or host insect itself. Here, we studied the olive fruit fly Bactrocera oleae (Rossi) (Diptera: Tephritidae), a major pest in olive agroecosystem and its larval parasitoid, Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae), a well-established and abundant wa...

Plants perceive and respond to herbivore insect eggs. Upon egg deposition on leaves, a strong hypersensitive response (HR)-like cell death can be activated leading to egg desiccation and/or dropping. In Brassica spp., including many crops, the HR-like mechanism against eggs of cabbage white butterflies ( Pieris spp.) is poorly understood. Using two...

Insect eggs are exposed to a plethora of abiotic and biotic threats. Their survival depends on both an innate developmental program and genetically determined protective traits provided by the parents. In addition, there is increasing evidence that ( a) parents adjust the egg phenotype to the actual needs, ( b) eggs themselves respond to environmen...

Biological control, which uses natural enemies to reduce pest populations, is a non-polluting powerful method to manage impacts of (invasive) pests. Currently, polyphagous mirid predators are increasingly used in commercial, augmentative biological control. Information about their foraging behaviour is essential, especially if one intends to use se...

Egg parasitoids of herbivorous insects use an interplay of short- and long-range chemical cues emitted by hosts and host plants to find eggs to parasitize. Volatile compounds that attract egg parasitoids can be identified via behavioral assays and used to manipulate parasitoid behavior in the field for biological control of herbivorous pests. Howev...

Background Cabbage white butterflies (Pieris spp.) can be severe pests of Brassica crops such as Chinese cabbage, Pak choi (Brassica rapa) or cabbages (B. oleracea). Eggs of Pieris spp. can induce a hypersensitive response-like (HR-like) cell death which reduces egg survival in the wild black mustard (B. nigra). Unravelling the genetic basis of thi...

Background Cabbage white butterflies (Pieris spp.) can be severe pests of Brassica crops such as Chinese cabbage, Pak choi (Brassica rapa) or cabbages (B. oleracea). Eggs of Pieris spp. can induce a hypersensitive response-like (HR-like) cell death which reduces egg survival in the wild black mustard (B. nigra). Unravelling the genetic basis of thi...

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 (...

Evolutionary arms-races between plants and insect herbivores have long been proposed to generate key innovations such as plant toxins and detoxification mechanisms that can drive diversification of the interacting species. A novel front-line of plant defence is the killing of herbivorous insect eggs. We test whether an egg-killing plant trait has a...

Brassica plants activate a strong hypersensitive response (HR)-like necrosis underneath eggs of cabbage white butterflies, but their molecular response to eggs is poorly understood. Here, we developed a method to generate egg wash to identify potential insect egg-associated molecular patterns (EAMPs) inducing HR-like necrosis. We found that egg was...

Plants can respond to eggs laid by herbivorous insects on their leaves by preparing (priming) their defense against the hatching larvae. Egg-mediated priming of defense is known for several plant species, including Brassicaceae. However, it is unknown yet for how long the eggs need to remain on a plant until a primed defense state is reached, which...

Biological control is widely successful at controlling pests, but effective biocontrol agents are now more difficult to import from countries of origin due to more restrictive international trade laws (the Nagoya Protocol). Coupled with increasing demand, the efficacy of existing and new biocontrol agents needs to be improved with genetic and genom...

The cover image is based on the Original Article Plant responses to insect eggs are not induced by egg‐associated microbes, but by a secretion attached to the eggs by Luis R. Paniagua Voirol et al., https://doi.org/10.1111/pce.13746.

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...

Microbes play crucial roles in the biology of herbivorous insects, and the last decade has provided exciting new evidence for a prominent role of microbial symbiosis in detoxification of plant toxins, manipulation of plant defences and defence against natural enemies. We provide an order by order update of symbioses across herbivorous insects, part...

Plants can detect cues associated with the risk of future herbivory and modify defence phenotypes accordingly; however, our current understanding is limited both with respect to the range of early warning cues to which plants respond and the nature of the responses. Here we report that exposure to volatile emissions from plant tissues infested with...

An insect's phenotype can be influenced by the experiences of the parental generation. However, the effects of the parental symbiotic microbiome and host plant use on the offspring are unclear. We addressed this gap of knowledge by studying Pieris brassicae, a multivoltine butterfly species feeding on different brassicaceous plants across generatio...

Plants can enhance their defence against herbivorous insects by responding to insect egg depositions preceding larval feeding. The similarity of plant responses to insect eggs with those to phytopathogens gave rise to the hypothesis that egg‐associated microbes might act as elicitors. We tested this hypothesis by investigating first if elimination...

The preference-performance hypothesis (PPH) states that herbivorous female insects prefer to oviposit on those host plants that are best for their offspring. Yet, past attempts to show the adaptiveness of host selection decisions by herbivores often failed. Here, we tested the PPH by including often neglected oviposition-induced plant responses, an...

Biological control is widely successful for controlling pests, but effective biocontrol agents are now more difficult to obtain due to more restrictive international trade laws. Coupled with increasing demand, the efficacy of existing and new biocontrol agents needs to be improved with genetic and genomic approaches. Although they have been underut...

Evolutionary arms-races between plants and herbivores have been proposed to generate key innovations that can drive diversification of the interacting species. Recent studies reveal that plant traits that target herbivore insect eggs are widespread throughout the plant kingdom. Within the Brassicaceae family, some plants express a hypersensitive re...

According to the preference-performance hypothesis (PPH), also known as ‘mother-knows-best hypothesis’, herbivorous insects prefer those plants for oviposition, which yield the best offspring performance. Yet, most studies testing the PPH neglect the possibility that plant responses to insect eggs may affect both egg survival and larval performance...

Two new minute egg parasitoid wasp species belonging to the genus Trichogramma (Hymenoptera: Trichogrammatidae), T. chagres sp. nov. and T. soberania sp. nov., were found in a tropical lowland rainforest in Panama, Central America. In this paper, we describe, illustrate and discuss the biology and morphological and molecular characterization of the...

1. Parasitoid females foraging for hosts rely on cues derived from the insect host, the host plant and/or their interaction, and all of these can be learned during the immature and adult stages. 2. The present study investigated the importance of rearing history on foraging behaviour of Diaeretiella rapae, an endoparasitoid often associated with ap...

Significance 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...

The insect’s microbiota is well acknowledged as a “hidden” player influencing essential insect traits. The gut microbiome of butterflies and moths (Lepidoptera) has been shown to be highly variable between and within species, resulting in a controversy on the functional relevance of gut microbes in this insect order. Here, we aim to (i) review curr...

Plants employ various defences killing the insect attacker in an early stage. Oviposition by cabbage white butterflies (Pieris spp.) on brassicaceous plants, including Brassica nigra, induces a hypersensitive response (HR) - like leaf necrosis promoting desiccation of eggs. To gain a deeper insight into the arms race between butterflies and plants,...

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 rang...

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 b...

To successfully exert defenses against herbivores and pathogens plants need to recognize reliable cues produced by their attackers. Up to now, few elicitors associated with herbivorous insects have been identified. We have previously shown that accessory reproductive gland secretions associated with eggs of Cabbage White butterflies (Pieris spp.) i...

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...

Induction of plant defences, specifically in response to herbivore attack, can save costs that would otherwise be needed to maintain defences even in the absence of herbivores. However, plants may suffer considerable damage during the time required to mount these defences against an attacker. This could be resolved if plants could respond to early...

1. Herbivory can change plant quality, which may have consequences for interactions between the inducing herbivore and other insect community members. 2. Studies investigating the effects of plant quality on herbivore performance often have neglected the egg stage, and instead introduced larvae onto the plant. Recently, we reported that herbivore o...

Animals use information from their environment while foraging for food or prey. When parasitic wasps forage for hosts, they use plant volatiles induced by herbivore activities such as feeding and oviposition. Little information is available on how wasps exploit specific plant volatiles over time, and which compounds indicate changes in host quality...

Plants can respond to insect egg deposition and thus resist attack by herbivorous insects from the beginning of the attack, egg deposition. We review ecological effects of plant responses to insect eggs and differentiate between egg-induced plant defenses that directly harm the eggs and indirect defenses that involve egg parasitoids. Furthermore, w...

Evolutionary theory of plant defences against herbivores predicts a trade-off between direct (anti-herbivore traits) and indirect defences (attraction of carnivores) when carnivore fitness is reduced. Such a trade-off is expected in plant species that kill herbivore eggs by exhibiting a hypersensitive response (HR)-like necrosis, which should then...

Phoretic arthropods use other animals as vehicles to migrate to new environments. Among insect parasitoids, phoresy is almost exclusively restricted to minute wasp species that develop in or on the smallest and most inconspicuous life stage of their host: the egg. Females of about 35 egg parasitoid species are known to hitch-hike with adult hosts t...

Herbivory induces direct resistance responses in plants that negatively affect subsequently colonizing herbivores. Moreover, eggs of herbivorous insects can also activate plant resistance, which in some cases prevents hatching larvae from feeding. Until now, plant-mediated effects of eggs on subsequent herbivory, and the specificity of such respons...

Animals can store learned information in their brains through a series of distinct memory forms. Short-lasting memory forms can be followed by longer-lasting, consolidated memory forms. However, the factors determining variation in memory consolidation encountered in nature have thus far not been fully elucidated. Here, we show that two parasitic w...

Plants release volatiles induced by herbivore feeding that may affect the diversity and composition of plant-associated arthropod communities. However, the specificity and role of plant volatiles induced during the early phase of attack, i.e. egg deposition by herbivorous insects, and their consequences on insects of different trophic levels remain...

Phoretic insects utilize other animals to disperse to new environments. We recently discovered how egg parasitoids use an exciting phoretic strategy to reach egg-laying sites of their butterfly hosts. In the laboratory, female Trichogramma wasps detect and mount mated female cabbage white butterflies that emit an anti-aphrodisiac pheromone. Hardly...

Egg deposition by the Large Cabbage White butterfly Pieris brassicae on Brussels sprouts plants induces indirect defense by changing the leaf surface, which arrests the egg parasitoid Trichogramma brassicae. Previous studies revealed that this indirect defense response is elicited by benzyl cyanide (BC), which is present in the female accessory rep...

1. Female parasitoids have evolved various foraging strategies in order to find suitable hosts. Egg parasitoids have been shown to exploit plant cues induced by the deposition of host eggs. 2. The tiny wasp Trichogramma brassicae uses oviposition‐induced cues from Brussels sprouts to locate eggs of the cabbage white butterflies Pieris brassicae and...

Parasitic wasps employ a wide range of chemical cues to find their hosts. Very recently, we discovered how 2 closely related egg parasitoids, Trichogramma brassicae and Trichogramma evanescens, exploit the anti-aphrodisiac pheromone benzyl cyanide of one of their hosts, the gregarious large cabbage white butterfly Pieris brassicae that deposits a c...

A new species belonging to the genus Ooencyrtus Ashmead is described. Ooencyrtus marcelloi sp. nov. has been reared from eggs of Heliconiini (Lepidoptera: Nymphalidae, Heliconiinae) collected in Panama on Passiflora spp. The new species is compared with its closest Ooencyrtus species, i.e. O. caligo Noyes, O. neustriae Mercet, O. flavipes (Timberla...

During mating in many butterfly species, males transfer spermatophores that contain anti-aphrodisiacs to females that repel conspecific males. For example, males of the large cabbage white, Pieris brassicae (Lepidoptera: Pieridae), transfer the anti-aphrodisiac, benzyl cyanide (BC) to females. Accessory reproductive gland (ARG) secretion of a mated...

Many insects possess a sexual communication system that is vulnerable to chemical espionage by parasitic wasps. We recently discovered that a hitch-hiking (H) egg parasitoid exploits the antiaphrodisiac pheromone benzyl cyanide (BC) of the Large Cabbage White butterfly Pieris brassicae. This pheromone is passed from male butterflies to females duri...

Plants can recruit parasitic wasps in response to egg deposition by herbivorous insects–a sophisticated indirect plant defense mechanism. Oviposition by the Large Cabbage White butterfly Pieris brassicae on Brussels sprout plants induces phytochemical changes that arrest the egg parasitoid Trichogramma brassicae. Here, we report the identification...

Female parasitic wasps seek hosts for their offspring often in a dynamic environment. Foraging egg parasitoids rely on a variety of chemical cues originating from the adult host, host products, or the host plant rather than from the attacked host stage—the insect egg itself. Besides pupae, insect eggs are the most inconspicuous host stage attacked...

The Palaearctic leaf beetle Chrysomela lapponica usually feeds upon willows in the northern region of its occurrence. However, in Central Europe, some populations are known that have specialised on birch. In this study, we investigated the significance of other herbivores occurring together on the same host plants as possible exploitative competito...

Parasitoids are confronted with many different infochemicals of their hosts and food plants during host selection. Here, we investigated the effect of kairomones from the adult host Pieris brassicae and of cues present on Brussels sprout plants infested by P. brassicae eggs on the behavioral response of the egg parasitoid Trichogramma evanescens. A...