Turlings, Ted

2018, Girod, Pierre,, Turlings, Ted

La production agricole est en constante évolution afin d’améliorer le rendement. Actuellement, 40% de la production agricole est perdue à cause des ravageurs des cultures (majoritairement des insectes exotiques). Leur contrôle est une des priorités majeures à laquelle les chercheurs font face aujourd’hui. Le commerce international et le changement climatique ont accéléré la dissémination de nouvelles espèces exotiques à travers le monde. L’une de ces espèces récemment introduite, est la Drosophile à ailes tachetées, Drosophila suzukii. Cette mouche originaire d’Asie orientale a été recensée en Europe et en Amérique du Nord en 2008 et depuis, génère une attention particulière car elle cause de sérieuses pertes économiques dans les productions maraichères des petits fruits. A contrario des autres Drosophilidae qui habituellement pondent dans la matière en décomposition, D. suzukii pond ses œufs dans les fruits frais. La larve en s’alimentant, entraine alors la dégradation du fruit. Actuellement, le contrôle de D. suzukii consiste à utiliser des traitements chimiques et à mettre en place des pratiques culturales adaptées. Des évaluations sur l’utilisation potentielle de la lutte biologique visant à utiliser des parasitoïdes de drosophiles dans les zones envahies ont été menées, cependant la majorité de ces espèces indigènes n’ont pu se développer dans D. suzukii car elles n’étaient pas adaptées. C’est pourquoi, l‘introduction d’ennemis naturels de la région native de D. suzukii est envisagée. Ainsi l’objectif de cette thèse était d’évaluer le potentiel de différents parasitoïdes larvaires (généralement plus spécifique) Asiatique de D. suzukii en tant qu’agent de lutte biologique. Ce projet a débuté par la collection de parasitoïdes en Asie (Chapitre 1) permettant ainsi d’évaluer leur efficacité. Au moins huit espèces de parasitoïdes ont été recensées, dont certaines nouvelles espèces. Les taux de parasitismes en Asie sont très variables (0-80%) mais, dans chaque région le complexe de parasitoïdes est dominé par deux Hyménoptères (Famille: Figitidae), Ganaspis sp. et Leptopilina japonica. De nombreuses souches de ces espèces ainsi qu’un troisième Hyménoptère (Famille: Braconidae) Asobara japonica ont été collecté et importé en Suisse afin de conduire des expériences de laboratoire en quarantaine. Différents aspects de leur biologie ont été étudiés (Chapitre 2) et comparés à une espèce européenne Leptopilina heterotoma. La période de pré-oviposition et le temps de développement ont été mesurés, ainsi que la capacité à se développer dans D. suzukii dans le fruit (myrtille) ou sur substrat artificiel ont été comparé. Les trois espèces asiatiques ont été capables de se développer sur D. suzukii, alors que les œufs et les larves de L. heterotoma ont été majoritairement encapsulés par D. suzukii. Asobara japonica et L. japonica ont réussi à se développer sur D. suzukii sur les deux substrats, alors que Ganaspis sp. a pondu très peu d’œufs dans les larves sur substrat artificiel, suggérant ainsi qu’il est peut-être spécialisé dans les drosophiles vivant dans un habitat « fruit frais ». Dans un second temps (Chapitre 3), la spécificité de ces mêmes parasitoïdes a été évaluée lors de tests en non-choix sur D. suzukii, cinq espèces de drosophiles européennes et une Tephritidae sur myrtilles et/ou deux milieux artificiels. D’une part, ces tests ont montré que A. japonica était le plus généraliste et d’autre part, que Ganaspis sp. était l’espèce la plus spécifique. Cependant, d’importantes variations entre les deux souches de Ganaspis sp. ont été observées. La souche japonaise étant strictement spécifique à D. suzukii dans les myrtilles, alors que la souche chinoise a bien parasité D. suzukii mais également une espèce non-cible D. melanogaster sur un substrat artificiel enrichi en fruit mixés. La souche de L. heterotoma européen a attaqué D. suzukii mais étant non adapté à cet hôte, quasiment tous les œufs et les larves ont été encapsulés au contraire de ceux pondus dans les drosophiles européennes. Dans une dernière étude (Chapitre 4), les tests d’olfactométrie ont confirmé les tests en non-choix. La souche japonaise de Ganaspis sp. montrant une forte attractivité pour D. suzukii dans les fruits frais en comparaison des fruits en décomposition et du substrat artificiel enrichi en fruit, au contraire de la souche chinoise. Pris dans leur ensemble, ces résultats sont prometteurs pour le contrôle biologique de D. suzukii en Europe et ont montré que Ganaspis sp. est le candidat le plus prometteur. Cependant, des variations intra-spécifiques de la spécificité de l'hôte ont été observées. D'autres études seront nécessaires sur son statut taxonomique et sur l'existence de biotypes ou d'espèces cryptiques avant que des lâchers sur le terrain puissent être envisagés en Europe., Agricultural processes are constantly improved to improve crop yields. However, 40% of crop productions are currently lost to pests each year. Insect pests are one of the main factors of these losses and their management is one of the top priorities that researchers are facing worldwide. An important part of these losses are caused by pest with alien origins. Globalization and climate change speed up the spread of new invasive pests. One of these recent invasive pests is the spotted wing Drosophila, Drosophila suzukii. This fly of East Asian origin was first found in Europe and North America in 2008, and since then, it has generated much attention due to severe economic losses in berry and stone fruit crops. Unlike other Drosophilidae that usually develop in decaying matters, D. suzukii lays its eggs inside ripening fruits and damages are mainly caused by larval feeding, resulting in the degradation of fruits. Currently, the management of D. suzukii relies on chemical treatments and cultural methods. Studies have been undertaken to investigate the potential of biological control using native parasitoid species associated with D. suzukii in its invaded regions, but the majority of these species failed to develop as they were not able to locate the host in ripening fruits. Therefore, the introduction of natural enemies from the native region of the pests is envisaged. In Drosophilidae, the most abundant and specific natural enemies are usually larval parasitoids. Thus, the objective of this thesis was to assess the potential of Asian larval parasitoids of D. suzukii as biological control agents in Europe. The project started with surveys in China and Japan (Chapter 1) to study the larval parasitoid complex of the fly in its region of origin and assess parasitism. At least eight parasitoid species were collected, including some new to science. Parasitism rates in Asia were highly variable (0-80%) but, in all investigated regions, the parasitoid complex was dominated by two hymenopterans of the family Figitidae, Ganaspis sp. and Leptopilina japonica. Several strains of these two species and a third species, the Braconidae Asobara japonica, were imported to Switzerland for laboratory experiments in quarantine conditions. Several aspects of their biology were investigated (Chapter 2) and compared with the European species Leptopilina heterotoma. The pre-oviposition period and their development time were measured, and their ability to parasitise D. suzukii in fruit (blueberry) and artificial diet was compared. The three Asian species were successfully reared on D. suzukii larvae, in contrast to L. heterotoma whose eggs and larvae were encapsulated by the host larvae. Asobara japonica and L. japonica were highly successful in both media, while Ganaspis sp. laid very few eggs in larvae in the artificial diet, suggesting that it may be specialised in Drosophila species living in fresh fruits. In a second step (Chapter 3), the specificity of the same parasitoids was assessed through no-choice tests on D. suzukii, five European Drosophila spp. and one Tephritidae, in blueberry and/or two different artificial diets. On the one hand, these tests showed that A. japonica was the most polyphagous species. On the other hand Ganaspis sp. showed the highest specificity. However, important variations between two tested Ganaspis sp. strains were observed. The Japanese strain was strictly specific to D. suzukii in blueberry, whereas another strain from China parasitised D. suzukii and the non-target D. melanogaster in a diet enriched with blended fruit. The European L. heterotoma massively attacked D. suzukii but almost all eggs and larvae were encapsulated, in contrast to eggs laid in European Drosophila spp. In a last study (chapter 4), olfactometer tests confirmed the no-choice tests. Ganaspis sp. from Japan showed a strong attractiveness towards D. suzukii in fresh fruits compared to decaying fruits and to diet enriched with fruit, in contrast to the Chinese strain. Taken all together, these results are promising for the biological control of D. suzukii in Europe and showed that Ganaspis sp. is the most promising candidate. It is both the most important parasitoid of D. suzukii in Asia and the most specific one in laboratory tests. However, important intra-specific variations in host specificity have been observed. More studies are needed on its taxonomic status and the existence of biotypes or cryptic species before field releases can be envisaged in Europe.

2006, Tamò, Cristina, Ricard, Ingrid, Held, Matthias, Davison, A. C., Turlings, Ted

Many parasitic wasps that exploit herbivores as their hosts make use of herbivoreinduced plant odours to locate their victims and these wasps often exhibit an ability to learn to associate specific plant-produced odours with the presence of hosts. This associative learning is expected to allow generalist parasitoids to focus on cues that are most reliably associated with current host presence, but evidence supporting this hypothesis is ambiguous. Using a six-arm olfactometer we compared the responses of three generalist larval endoparasitoids, Cotesia marginiventris (Hymenoptera: Braconidae), Microplitis rufiventris (Hymenoptera: Braconidae) and Campoletis sonorensis (Hymenoptera: Ichneumonidae), to the induced odours of three plant species: maize (Zea mays), cowpea (Vigna unguiculata), and cotton (Gossypium hirsutum). We tested the responses of naïve females as well as of females that were first conditioned by parasitising host larvae feeding on one of the plant species. Despite similarities in biology and host range the three wasp species responded entirely differently. Naïve C. marginiventris and C. sonorensis chose equally among the induced odours of the three plants, whereas naïve M. rufiventris, which may have a somewhat more restricted host range, tended to prefer the odour of maize. After conditioning, most C. marginiventris females chose the odour of the plant species that they had experienced, but conditioned M. rufiventris showed an even stronger preference for maize odours, independently of the plant they had experienced. Cotesia sonorensis did not show any change in its preference after conditioning. We speculate that its extremely broad host range allows C. sonorensis females to use fixed responses to cues commonly associated with plants damaged by Lepidoptera. These results imply that different generalist parasitoids may employ different foraging strategies and that associative learning is not necessarily part of it.

2005, Faria, Cristina Arantes de, Turlings, Ted

La consommation d'hydrates de carbone est indispensable pour la survie et reproduction des parasitoïdes adultes. Ceci veut dire que les femelles de nombreux parasitoïdes devront périodiquement arrêter la recherche des hôtes afin de trouver de la nourriture. Si les hôtes et la nourriture se trouvent à différents endroits, la recherche de nourriture peut conduire à une grande perte en temps et en énergie. Ceci est le cas dans la plupart des monocultures agricoles où le nectar est disponible pour une période limitée voire complètement indisponible. Lorsque les hôtes et les sources de nourriture sont proches l'une de l'autre, les parasitoïdes femelles en bénéficient grandement car elles peuvent se concentrer sur la recherche d'hôtes et minimiser le temps consacrée à trouver la nourriture. Dans ce contexte, le miellat produit par les pucerons peut être considéré comme une source de nutrition alternative d'importance vitale car il se trouve en association proche avec les hôtes même pour les parasitoïdes autres que ceux du puceron. Les effets de l'alimentation avec du miellat sur la performance des parasitoïdes larvaires ont été testés (Chapitre 1). Les femelles parasitoïdes ont vécu plus longtemps et ont produit une descendance plus nombreuse en se nourrissant de miellat comparé à des femelles non nourries. Toutefois, elles ont vécu moins longtemps et ont produit moins de descendants que des femelles nourries avec une solution de sucrose. Le miellat était composé de sucres dérivés de la plante et des pucerons et sa composition changeait avec le temps et avec des taux d'infestations différents. La performance relativement basse avec du miellat ne peut pas être expliquée par sa composition mais plutôt par la difficulté à ingérer le miellat qui est très visqueux comparé à la solution de sucrose. Du miellat facilement accessible serait toutefois une source de nourriture très utile pour de nombreux parasitoïdes. Ainsi donc, l'aptitude à apprendre à distinguer entre hôte et les signaux associés à la nourriture devrait être adaptive car cela permettrait aux parasitoïdes d'économiser de l'énergie et du temps lors du changement entre recherche de nourriture et recherche d'hôte et vice-versa. Nous avons évaluée si le parasitoïde apprend les odeurs associées au miellat et si leur état physiologique affecte le choix entre recherche de nourriture et recherche d'hôte (Chapitre 2). C. marginiventris n'est pas attiré de façon innée à de l'orge infesté par des pucerons. Toutefois, quand les femelles avaient une récompense sous forme de nourriture associée avec l'odeur des plantes infestées par des pucerons, elles étaient attirées par ces odeurs les fois suivantes. Lorsque le choix entre odour de nourriture et odeur associée à l'hôte est donné à C. marginiventris, celle-ci décide selon son état physiologique et ses expériences passées. De plus, les femelles affamées réagissaient moins aux odeurs associées aux hôtes que des femelles bien nourries. La grande augumentation de l'utilisation commerciale des plantes transgéniques a provoqué de nombreuses inquiétudes sur leurs risques potentiels pour des organismes noncibles. Dans ce contexte nous avons testé les effets potentiels des plantes transgéniques Bt sur C. marginiventris à travers le miellat produit par les pucerons (Chapitre 3). De façon surprenante les plantes transgéniques furent plus susceptibles aux pucerons que leurs analogues non-transformés. Des concentrations supérieures en acides aminés dans le phloème des transgéniques explique partiellement la différence de performance des pucerons. Ces différences ont aussi affectés les performances de C. marginiventris. Les femelles de ce parasitoïde ont vécu plus longtemps et ont produits plus de descendants quand elles étaient en présence des transgéniques infestées de pucerons comparés aux femelles qui avaient accès aux plantes isogéniques infestées. La composition en sucre du miellat n'a pas pu expliquer les différentes performances des parasitoïdes. D'autres tests ont permis de suggérer que l'amélioration des performances des parasitoïdes était due à un accès plus facile du miellat sur les plantes transgéniques à cause de leur plus grande susceptibilité aux pucerons., Feeding on carbohydrate food sources is critical for survival and reproductive success of adult parasitoids. This means that females of many parasitoids will have to periodically interrupt host foraging to find food. If host and food are located in different patches, food searching can be time and energy consuming. This is especially true for most agricultural monocultures were nectar is available for a short period of time or not available at all. Situations where host and food sources are in close proximity from each other are highly beneficial for parasitoid females as this allows them to concentrate in host foraging and thereby minimize time spend on food searching. In this context, aphid-produced honeydew might be regarded as an alternative food source of key importance as it usually occurs in close association with the hosts even for non-aphid parasitoids. We tested the effect that honeydew feeding has on the performance of larval parasitoids (Chapter 1). Parasitoid females lived longer and produced a higher number of offspring when feeding on honeydew when compared to unfed females. However, they lived shorter and produced a smaller number of offspring than females fed with a sucrose solution. The honeydew was composed of both plant-derived and aphid-produced sugars and its composition changed over time and with different infestation rates. The relatively poor performance on honeydew cannot be explained by the honeydew composition, but rather by the slow uptake of the very viscose honeydew as compared to the sucrose solution. Due to its wide availability and its accessibility, honeydew would still make it a very useful food source for many parasitoids. Therefore an ability to learn to distinguish between host and food associated cues should be adaptive as it would allow the parasitoid to save energy and time when switching from host to food searching and vice-versa. We assessed whether C. marginiventris learns honeydew associated odours and how their physiological state affects the choice between host and 6 food searching (Chapter 2). C. marginiventris was not innately attracted to aphid-infested barley. However, when the females had a food reward associated with the odour of aphidinfested plants they were subsequently attracted to this odour when hungry. When given a choice between food and host associated odours C. marginiventris decides between host and food foraging based on their physiological status and previous experience. Moreover, hungry females were less responsive to host-associated odours than well fed ones. The fast increase in the commercial use of transgenic plants has raised concerns about their potential risks for non-target organisms. In this context, we investigated possible effects of Bt-transgenic plants on C. marginiventris through aphid-produced honeydew (Chapter 3). Surprisingly, transgenic plants were more susceptible to aphids than their corresponding untransformed counterparts. Higher amino acid concentrations in the phloem of the transgenic lines partially explained these differences in aphid performance. The differences in aphid performance also affected the performance of C. marginiventris. Females of this parasitoid lived longer and produced more offspring when in the presence of transgenic plants infested with aphids compared to females that had access to near isogenic lines infested with aphids. The sugar composition of the honeydew did not explain these differences in parasitoid performance. Further tests suggested that the increase in parasitoid performance was rather due to a greater availability of honeydew on the transgenic plants due to their higher susceptibility to aphids.

2001, Bernasconi Ockroy, Marco L., Turlings, Ted, Edwards, Peter J., Fritzsche-Hoballah, Ambrosetti, Lara, Bassetti, Paolo, Dorn, Silvia

1 In response to herbivore attack, maize plants (Zea mays L.) emit a specific blend of induced volatiles. Artificial damage and subsequent treatment of the damaged site with caterpillar regurgitant induces the same response. The induced volatile chemicals are known to be highly attractive to several parasitoids of herbivores in laboratory bioassays, but very limited information is available on how the plant odours affect entomophagous insects in the field.

2 Experiments were conducted to determine if induced maize volatiles attract parasitic and predatory insects under field conditions and whether they affect their spatial distribution.

3 In a preliminary field experiment with blue sticky traps near treated (damaged and treated with caterpillar regurgitant) and healthy plants, more entomophagous insects (total number of parasitic Hymenoptera, Anthocoridae and Syrphidae) were trapped near treated plants than near healthy plants.

4 In a second experiment, attraction to the induced volatiles was monitored with sticky traps placed next to treated and healthy maize plants in a regular maize field. No significant differences between the two treatments were found, but significantly more insects (parasitic wasps, thrips and anthocorid bugs) were trapped near to the top of plants than on traps placed near the mid-stem. Displacement of these insect groups within the field seemed to occur principally over the canopy, but under severe weather conditions they travelled lower in the canopy.

5 In a third experiment, the effect of induced maize odours on the spatial distribution of predators and parasitoids was investigated by placing sticky traps at different distances from healthy and treated plants. The higher catches of parasitoids near treated plants and the increased presence of these insects on the downwind side of treated plants support the notion that herbivore-induced maize odours attract natural enemies of maize pests in the field.

2008, Jourdie, Violaine, Alvarez, Nadir, Turlings, Ted, Franck, Pierre

Fifteen and 13 microsatellite loci were isolated, respectively, from Campoletis sonorensis Cameron and from Chelonus insularis Cresson. These two parasitic Hymenoptera are primary parasitoids of Lepidoptera in North, Central and South America, including the important agricultural pest Spodoptera frugiperda. Allelic diversity and heterozygosity were quantified in samples from Mexico. Each locus was polymorphic, with the number of alleles ranging from two to 16 in C. sonorensis and from four to 18 in C. insularis. Heterozygosity ranged from 0.088 to 0.403 in C. sonorensis and from 0.106 to 0.458 in C. insularis.

2006, Tamò, Cristina, Roelfstra, Lise-Lore, Guillaume, Suzanne, Turlings, Ted

1. In studies on optimal foraging strategies, long-range decisions in the pursuit of resource are rarely considered. This is also the case for sympatric parasitoids, which may be confronted with the decision to accept or reject host larvae that are already parasitized by a competing species. They can be expected to reject already parasitized hosts if it is likely that they will lose the resulting intrinsic competition. However, examples of such interspecific host discrimination are rare.
2. We propose that parasitoids that are not egg-limited should reject inferior hosts only if it saves them time, and that this will be achieved mainly when the parasitoids are able to detect competitors from a distance. We tested this hypothesis using the sympatric parasitoids Cotesia marginiventris (Cresson) and Campoletis sonorensis (Cameron).
3.C. sonorensis was found to be the superior intrinsic competitor but, upon contact with a host larva, both wasps readily accepted hosts that had already been parasitized by the other species. However, in an olfactometer experiment, C. marginiventris females were found to strongly avoid the odour of their superior competitor.
4. These results are in accordance with a time optimization scenario, whereby the inferior competitor accepts competition if it costs only an egg, but avoids competition if it may save time that can be allocated to the search for more profitable hosts.
5. Models on host discrimination strategies in parasitoids had not yet considered discrimination from a distance. Long-range foraging decisions can also be expected for other organisms that have to choose between resources of varying suitability and profitability.

2004, D'Alessandro, Marco, Turlings, Ted

Many parasitic wasps (parasitoids) exploit volatile organic compounds (VOCs) emitted by herbivore-infested plants in order to locate their hosts, but it remains largely unknown which specific compounds within the volatile blends elicit the attractiveness to parasitoids. One way of studying the importance of specific VOCs is to test the attractiveness of odor blends from which certain compounds have been emitted. We used this approach by testing the attraction of naive and experienced females of the two parasitoids Cotesia marginiventris and Microplitis rufiventris to partially altered volatile blends of maize seedlings (Zea mays var. Delprim) infested with Spodoptera littoralis larvae. Adsorbing filter tubes containing carbotrap-C or silica were installed in a four-arm olfactometer between the odor source vessels and the arms of the olfactometer. The blends breaking through were tested for chemical composition and attractiveness to the wasps. Carbotrap-C adsorbed most of the sesquiterpenes, but the breakthrough blend remained attractive to naive C. marginiventris females. Silica adsorbed only some of the more polar VOCs, but this essentially eliminated all attractiveness to naive C. marginiventris, implying that among the adsorbed compounds there are some that play key roles in the attraction. Unlike C. marginiventris, M. rufiventris was still attracted to the latter blend, showing that parasitoids with a comparable biology may employ different strategies in their use of plant-provided cues to locate hosts. Results from similar experiments with modified odor blends of caterpillar-infested cowpea (Vigna unguiculata) indicate that key VOCs in different plant species vary greatly in quality and/or quantity. Finally, experienced wasps were more strongly attracted to a specific blend after they perceived the blend while ovipositing in a host. Considering the high number of distinct adsorbing materials available today, this in situ modification of complex volatile blends provides a new and promising approach pinpointing on key attractants within these blends. Advantages and disadvantages compared to other approaches are discussed.

2007, Rasmann, Sergio, Turlings, Ted

Herbivore-damaged plants emit volatile organic compounds that attract natural enemies of the herbivores. This form of indirect plant defence occurs aboveground as well as belowground, but it remains unclear how simultaneous feeding by different herbivores attacking leaves and roots may affect the production of the respective defence signals. We employed a setup that combines trapping of volatile organic signals and simultaneous measurements of the attractiveness of these signals to above and belowground natural enemies. Young maize plants were infested with either the foliar herbivore Spodoptera littoralis, the root herbivore Diabrotica virgifera virgifera, or with both these important pest insects. The parasitic wasp Cotesia marginiventris and the entomopathogenic nematode Heterorhabditis megidis were strongly attracted if their respective host was feeding on a plant, but this attraction was significantly reduced if both herbivores were on a plant. The emission of the principal root attractant was indeed reduced due to double infestation, but this was not evident for the leaf volatiles. The parasitoid showed an ability to learn the differences in odour emissions and increased its response to the odour of a doubly infested plant after experiencing this odour during an encounter with hosts. This first study to measure effects of belowground herbivory on aboveground tritrophic signalling and vice-versa reemphasizes the important role of plants in bridging interactions between spatially distinct components of the ecosystem.

2005, Turlings, Ted, Jeanbourquin, Philippe, Held, Matthias, Degen, Thomas

The current discussion on the safety of transgenic crops includes their effects on beneficial insects, such as parasitoids and predators of pest insects. One important plant trait to consider in this context is the emission of volatiles in response to herbivory. Natural enemies use the odours that result from these emissions as cues to locate their herbivorous prey and any significant change in these plant-provided signals may disrupt their search efficiency. There is a need for practical and reliable methods to evaluate transgenic crops for this and other important plant traits. Moreover, it is imperative that such evaluations are done in the context of variability for these traits among conventional genotypes of a crop. For maize and the induction of volatile emissions by caterpillar feeding this variability is known and realistic comparisons can therefore be made. Here we used a six-arm olfactometer that permits the simultaneous collection of volatiles emitted by multiple plants and testing of their attractiveness to insects. With this apparatus we measured the induced odour emissions of Bt maize (Bt11, N4640Bt) and its near-isogenic line (N4640) and the attractiveness of these odours to Cotesia marginiventris and Microplitis rufiventris, two important larval parasitoids of common lepidopteran pests. Both parasitoid species were strongly attracted to induced maize odour and neither wasp distinguished between the odours of the transgenic and the isogenic line. Also wasps that had previously experienced one of the odours during a successful oviposition divided their choices equally between the two odours. However, chemical analyses of collected odours revealed significant quantitative differences. The same 11 compounds dominated the blends of both genotypes, but the isogenic line released a larger amount of most of these. These differences may be due to altered resource allocation in the transgenic line, but it had no measurable effect on the wasps’ behaviour. All compounds identified here had been previously reported for maize and the differential quantities in which they were released fall well within the range of variability observed for other maize genotypes.

2004, Hoballah, Maria Elena, Degen, Thomas, Bergvinson, David, Savidan, Anita, Tamò, Cristina, Turlings, Ted

1 Native natural enemies have the potential to control fall armyworm Spodoptera frugiperda (Smith) in tropical maize grown in Mexico, where this insect pest causes severe economic losses to farmers. It has been proposed that enhancing herbivore-induced volatile emissions in maize plants may help to increase the effectiveness of natural enemies, which use these volatiles to locate their prey. This will only be of immediate benefit to farmers if the activity of the natural enemies results in a direct reduction in herbivory. Here we report on field surveys for the most common natural enemies in a tropical maize-growing region in Mexico and the potential effects of these enemies on herbivory by fall armyworm.
2 Caterpillars were collected in maize fields near Poza Rica in the state of Veracruz during January and February 1999, 2000 and 2001. Plants were either naturally infested by S. frugiperda, or artificially infested with laboratory-reared larvae. Ten species of parasitoids emerged from the collected larvae and eight species of predators that are known to feed on larvae and eggs were observed on the plants. Campoletis sonorensis (Cameron) (Hymenoptera: Ichneumonidae) was the dominant parasitoid species, in 1999 and 2001.
3 Of the nine larval parasitoids collected, six (all solitary) are known to reduce herbivory, whereas one causes the host to eat more (for two species this is not known). This implies that enhancing the effectiveness of solitary endoparasitoids may benefit subsistence farmers in developing countries by immediately reducing herbivory. The overall benefit for the plant resulting from parasitoid activity also has important implications for the evolutionary role of parasitoids in contributing to selection pressures that shape indirect defences in plants.