Louise E. M. Vet

Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists

Plants function in a complex multitrophic environment. Most multitrophic studies, however, have almost exclusively focused on aboveground interactions, generally neglecting the fact that above- and belowground organisms interact. The spatial and temporal dynamics of above- and belowground herbivores, plant pathogens, and their antagonists, can differ in space and time. This affects the temporal interaction strengths and impacts of above- and belowground higher trophic level organisms on plants. Combining both above- and belowground compartments in studies of multitrophic interactions throughout the life cycle of plants will improve our understanding of ecology and evolution in the real world.

Learning of Host-Finding Cues by Hymenopterous Parasitoids

Interactions between insect parasitoids and their arthropod hosts characteristically result in the premature death of the hosts, and are obligatory for the development of the parasitic insects. This obviously places strong pressure on the hosts to avoid detection by parasitoids, and on the parasitoids themselves to improve encounter rates with suitable hosts. To confront the challenge of finding the often-inconspicuous, well-hidden hosts, parasitoids have developed various sophisticated searching strategies that depend on a vast array of environmental cues.

Semiochemicals and learning in parasitoids

There is increasing evidence that parasitoid responses to semiochemicals, important stimuli in the host location process, are influenced by experience. This paper focuses on the role of learning, in particular associative learning, in responses to odors. Emphasis is placed on associative learning during the adult stage, the influence of preadult experience is discussed briefly. New data on learning in the speciesLeptopilina heterotoma are given. It is demonstrated that females can learn to respond to a novel odor, which they subsequently use in microhabitat selection. Learning was shown to be associative whereby host products (contact kairomone) or an oviposition experience could function as the reinforcers (reward). The effect of learning seemed stronger when parasitoids were rewarded with an oviposition experience. The paper concludes with a discussion on the application of parasitoid learning in pest management.

How to hunt for hiding hosts: the reliability-detectability problem in foraging parasitoids.

Foraging parasitoids may use stimuli that are derived from their host or from the food of their host, often plants. But how usable are 2nd and 1st trophic level stimuli and what is their relative importance in parasitoid foraging? It is argued that foraging parasitoids are facing a reliability-detectability problem: host-derived stimuli are the most reliable in indicating host presence, accessibility and suitability but they are generally hard to detect. Plant stimuli, on the other hand, are easier to detect but arc generally less reliable indicators. Parasitoids have evolved different non-exclusive strategies to solve this problem. (1) Infochemical detour: parasitoids resort to information from other, more detectable, host stages than the one under attack. (2) Herbivore-induced synomones: parasitoids use specific plant produced volatiles that are released upon damage by a specific herbivore species. In the present paper we put most emphasis on a third strategy (3) Associative learning: through associative learning parasitoids link easy-to-detect stimuli to reliable but hard-to-detect stimuli. Specific mechanisms by which associative learning can improve foraging success are discussed.

Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species

Plants that are infested by herbivores emit volatile cues that can be used by the natural enemies of the herbivores in their search for hosts. Based on results from behavioral studies, we investigated to what extent intact and herbivore-infested plant species and varieties from the food plant range of Pieris herbivore species differ in the composition of the volatile blends. Parasitoids of Pieris species, Cotesia glomerata and C. rubecula, show differential responses towards various herbivore-infested food plants, whereas differences in responses to plants infested by other herbivore species were less clear. Chemical analysis of the headspace samples of red cabbage, white cabbage, and nasturtium plants that were infested by P. brassicae or P. rapae larvae, or that were intact, yielded 88 compounds including alcohols, ketones, aldehydes, esters, nitriles, terpenoids, sulfides, (iso)thiocyanates, carboxylic acids, and others. The analysis revealed that herbivore-infested plants emit the largest number of compounds in the highest amounts. The plant species affected the volatile blend more than did the herbivore species, and differences between plant varieties were less pronounced than differences between plant species. Differences in headspace composition between plants infested by P. brassicae or P. rapae were mainly of a quantitative nature. Herbivore-infested nasturtium differed considerably from the cabbage varieties in a qualitative way. Headspace compositions of red and white cabbage varieties were comparable to that of the food plant Brussels sprouts (Brassica oleracea gemmifera cv. Titurel) as determined in earlier studies in our laboratory. With respect to plant response to herbivory, nasturtium differed considerably from the cabbage varieties analyzed so far and shows resemblance with Lima bean, cucumber, and corn. These plant species produce a greater quantity and variety of volatiles under herbivore attack than intact plants. The results of this study are discussed in relation to behavioral observations on C. glomerata and C. rubecula.

Relative importance of infochemicals from first and second trophic level in long-range host location by the larval parasitoid Cotesia glomerata.

Recently parasitoids were hypothesized to encounter a reliability-detectability problem relating to chemical stimuli from the first and second trophic level, when searching for hosts. The relative role of infochemicals originating from the host,Pieris brassicae (second trophic level), and its food plant, cabbage (first trophic level), have been investigated with respect to long-range host location by the larval parasitoidCotesia glomerata. Flight-chamber dual choice tests showed that uninfested cabbage plants are least attractive to female wasps. Host larvae and their feces were more attractive than clean plants but far less attractive than artificially damaged and herbivore-damaged plants. The plant-host complex, with host larvae actively feeding on the plant, was the most attractive odor source for the parasitoids. The data indicate that one of the solutionsC. glomerata uses to solve the reliability-detectability problem is to respond to infochemicals that are emitted from herbivore-damaged plants. Whether these infochemicals are herbivore-induced synomones that are produced by the plant remains to be demonstrated. Infochemicals emitted by the herbivore or its by-products are of little importance in the foraging behavior ofC. glomerata.

Interactions between aboveground and belowground induced responses against phytophages

Abstract Since their discovery about thirty years ago, induced plant responses have mainly been studied in interactions of plants with aboveground (AG) pathogens, herbivores and their natural enemies. Many induced responses, however, are known to be systemic and thus it is likely that responses induced by AG phytophages affect belowground (BG) phytophages feeding on the same plant, and vice versa . The awareness that interactions between AG and BG phytophages may be an important aspect in the evolution of induced responses came only recently and little research has been done to date. In this review we first summarise ecological studies that show how AG phytophages may affect BG phytophages, and vice versa . Then we focus on mechanisms governing interactions between AG and BG induced responses, such as cross-talk between signals. We chose the genus Nicotiana and the family Brassicaceae as two examples of plant groups that have been well studied for their induced responses both AG and BG – but not in concert – and explore how interactions between AG and BG induced compounds may link multitrophic interactions associated with these plants. We propose that future research on AG and BG interactions should focus on: 1). Identification of compounds and signalling pathways involved in AG and BG induced responses and analysis of their interaction mechanisms, 2). Evaluation of how induced responses affect interactions between BG and AG phytophages and their natural enemies, 3). Evaluation of the effects of AG and BG phytophages -in combination with their natural enemies- on plant fitness to identify keystone interactions that are driving the natural selection for induced responses in plants. Seit ihrer Entdeckung vor ca. dreisig Jahren werden induzierte pflanzliche Antworten der Pflanzen zumeist mit solchen Pathogenen, Herbivoren und deren naturlichen Feinden untersucht, die an oberirdischen Pflanzenteilen zu finden sind. Viele induzierte Antworten der Pflanzen konnen aber systemisch sein. Daher ist es wahrscheinlich, dass pflanzliche Antworten, die durch oberirdische Organismen induziert werden, auch solche Phytophagen beeinflussen, die unterirdisch an der Pflanze fressen, und umgekehrt. Das Bewustsein darum, dass Interaktionen zwischen ober- und unterirdischen Phytophagen ein wichtiger Aspekt in der Evolution von induzierten pflanzlichen Abwehrreaktionen sein konnen, kam erst in neuerer Zeit auf. Deshalb gibt es bisher wenig Forschung auf diesem Gebiet. In diesem Uberblick werden zunachst die Studien zusammengefasst, die den Einfluss oberirdischer Phytophager auf die unterirdischen Phytophagen zeigen und umgekehrt. Weiterhin wird auf die Mechanismen fokussiert, die Interaktionen zwischen ober- und unterirdisch fressenden Phytophagen steuern, wie z.B. Wechselwirkungen zwischen Signalen. Die Gattung Nicotiana und die Familie Brassicaceae werden als Modellpflanzen ausgewahlt, an denen die induzierte Abwehr gegen entweder oberirdische oder unterirdische Phytophage – aber nicht gegen beide gleichzeitig – bereits gut untersucht wurde. Es wird analysiert, wie Interaktionen zwischen ober- und unterirdisch induzierten Verbindungen mit multitrophischen Interaktionen dieser Pflanzen in Zusammenhang stehen. Es werden Vorschlage unterbreitet, worauf zukunftige Forschung an ober- und unterirdisch induzierten Interaktionen fokussieren sollte: (1) Identifizierung der Verbindungen und der Signalwege, die bei ober- und unterirdischer Induktion von Bedeutung sind und Analyse der Interaktionsmechanismen, (2) Untersuchung der Frage, wie induzierte Reaktionen der Pflanze sich auf Interaktionen zwischen ober- und unterirdischen Phytophagen und deren naturlichen Feinden auswirken, (3) Analyse der Auswirkungen der Effekte von ober- und unterirdisch fressenden Phytophagen unter Berucksichtigung auch ihrer naturlichen Feinde auf die pflanzliche Fitness, um solche Schlusselinteraktionen zu identifizieren, die entscheidend sind fur die Selektion der induzierten pflanzlichen Reaktion auf Angriffe durch Phytophage.

Response of the braconid parasitoid Cotesia (=Apanteles) glomerata to volatile infochemicals: effects of bioassay set‐up, parasitoid age and experience and barometric flux

Upon initiating a research project on the role of volatile infochemicals in the tritrophic system Cotesia (= Apanteles) glomerata (L.) ‐ Pieris brassicae (L.) ‐ cabbage, a bioassay was developed to investigate the response of C. glomerata. The bioassay should be effective in terms of high responsiveness and minimum variability and constructed through a comparative approach. Twenty seven treatments, organized in a factorial randomized block design, compared the effect of three bioassay set‐ups (glasshouse flight chamber, wind‐tunnel and Y‐tube olfactometer), three parasitoid age groups (1–2, 4–5 and 8–9 days old females), three pre‐treatment experiences (naive, damage experienced and oviposition experienced wasps) and the day‐to‐day effect on response of C. glomerata to clean cabbage (CC) and plant‐host complex (PHC) in a dual choice test.

Host-Habitat Location Through Olfactory Cues By Leptopilina Cla Vipes (Hartig) (Hym.: Eucoilidae), a Parasitoid of Fungivorous Drosophila: the Influence of Conditioning

This paper deals with the process of olfactory habitat location in Leptopilina clavipes, a larval endo-parasitoid of fungivorous Drosophilidae. Females show a response to the odour of decaying mushrooms in a state likely to contain host larvae. No long-range attraction to host larvae was detected. Attraction to odours from a different microhabitat (fermenting fruits) was shown to be influenced by different types of conditioning. When reared in hosts on a yeast medium, yeast odours were highly attractive to the emerged adult parasitoids, but mushroom odours were still preferred. Conditioning during oviposition (associative learning) was proven to be much stronger, as it did modify the habitat odour preference-pattern. The ecological significance of the learning process is discussed. It is suggested that the function of learning in search is to optimize the discovery and utilization of resources which fluctuate in abundance and time.

Odor learning and foraging success in the parasitoid, Leptopilina heterotoma.

A brief 2-hr experience with hostDrosophila larvae in artificial apple-yeast or mushroom microhabitats had three effects on the foraging behavior of femaleLeptopilina heterotoma (Hymenoptera: Eucoilidae) parasitoids under field conditions. First, experienced females released at the center of circular arrays of apple-yeast and mushroom baits were more likely to find a microhabitat over the course of a daily census than naive ones. Second, for those females that found a microhabitat, experienced ones found it faster than naive ones (i.e., experience reduced travel times). Third, females experienced with a particular microhabitat were more likely to find that micro-habitat than an alternative one. Learned preferences were retained for at least one day and possibly as many as seven. Results generally did not depend on the host species (D. melanogaster orD. simulans) with which females were given experience. Females tended to arrive at baits upwind of the point of release, suggesting that odor is involved in finding host microhabitats and, in particular, in learning to find them more effectively. The implications of these results for the application of semiochemicals in biological control are discussed briefly.