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Turlings, Ted

Nom
Turlings, Ted
Affiliation principale
Fonction
Professeur ordinaire
Email
ted.turlings@unine.ch
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https://libra.unine.ch/handle/123456789/330

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  • Publication
    Accès libre
    From Asia to Europe: evaluation of parasitoids for the biological control of the invasive fruit pest "Drosophila suzukii"
    (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.
  • Publication
    Métadonnées seulement
    The prospect of applying chemical elicitors and plant strengtheners to enhance the biological control of crop pests
    (2014)
    Sobhy, Islam S.
    ;
    Erb, Matthias 
    ;
    Lou, Yonggen
    ;
    Turlings, Ted 
    An imminent food crisis reinforces the need for novel strategies to increase crop yields worldwide. Effective control of pest insects should be part of such strategies, preferentially with reduced negative impact on the environment and optimal protection and utilization of existing biodiversity. Enhancing the presence and efficacy of native biological control agents could be one such strategy. Plant strengthener is a generic term for several commercially available compounds or mixtures of compounds that can be applied to cultivated plants in order to 'boost their vigour, resilience and performance'. Studies into the consequences of boosting plant resistance against pests and diseases on plant volatiles have found a surprising and dramatic increase in the plants' attractiveness to parasitic wasps. Here, we summarize the results from these studies and present new results from assays that illustrate the great potential of two commercially available resistance elicitors. We argue that plant strengtheners may currently be the best option to enhance the attractiveness of cultivated plants to biological control agents. Other options, such as the genetic manipulation of the release of specific volatiles may offer future solutions, but in most systems, we still miss fundamental knowledge on which key attractants should be targeted for this approach.
  • Publication
    Métadonnées seulement
    Phylogeography of Chelonus insularis (Hymenoptera: Braconidae) and Campoletis sonorensis (Hymenoptera: Ichneumonidae), two primary neotropical parasitoids of the fall armyworm (Lepidoptera: Noctuidae)
    (2010-9)
    Jourdie, V.
    ;
    Virla, E.
    ;
    Murillo, H.
    ;
    Bento, J. M. S.
    ;
    Turlings, Ted 
    ;
    Alvarez, N.
    In a previous study, we observed no spatial genetic structure in Mexican populations of the parasitoids Chelonus insularis Cresson (Hymenoptera: Braconidae) and Campoletis sonorensis Cameron (Hymenoptera: Ichneumonidae) by using microsatellite markers In the current study, we Investigated whether for these important parasitoids of the fall armyworm (Lepidoptera: Noctuidae) there is any genetic structure at a larger scale Insects of both species were collected across the American continent and their phylogeography was Investigated using both nuclear and mitochondria] markers Our results suggest an ancient north-south migration of C insularis, whereas no clear pattern] could be determined for C sonorensis. Nonetheless, the resulting topology indicated the existence of a cryptic taxon within this later species. a few Canadian specimens determined as C. sonorensis branch outside a clack composed of the Argentinean Chelonus grioti Blanchard, the Brazilian Chelonus flavicincta Ashmead, and the rest of the C sonorensis individuals The individuals revealing the cryptic taxon were collected from Thichoplusia in (Hubner) (Lepidoptera. Noctuidae) on tomato (Lycopersicon spp) and may represent a biotype that has adapted to the early season phenology of its host. Overall, the loosely defined spatial genetic structure previously shown at a local fine scale also was found at the larger scale, for both species Dispersal of these insects may be partly driven by wind as suggested by genetic similarities between Individuals coming from very distant locations.
  • Publication
    Accès libre
    Isolation and characterization of polymorphic microsatellite loci in two primary parasitoids of the noctuid Spodoptera frugiperda: Chelonus insularis and Campoletis sonorensis (Hymenoptera)
    (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.
  • Publication
    Accès libre
    Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies
    (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.
  • Publication
    Métadonnées seulement
    Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naive parasitoids
    (2006)
    Rostas, Michael
    ;
    Ton, Jurriaan
    ;
    Mauch-Mani, Brigitte 
    ;
    Turlings, Ted 
    Plants attacked by insects release volatile compounds that attract the herbivores' natural enemies. This so-called indirect defense is plastic and may be affected by an array of biotic and abiotic factors. We investigated the effect of fungal infection as a biotic stress agent on the emission of herbivore-induced volatiles and the possible consequences for the attraction of two parasitoid species. Maize seedlings that were simultaneously attacked by the fungus Setosphaeria turcica and larvae of Spodoptera littoralis emitted a blend of volatiles that was qualitatively similar to the blend emitted by maize that was damaged by only the herbivore, but there was a clear quantitative difference. When simultaneously challenged by fungus and herbivore, the maize plants emitted in total 47% less of the volatiles. Emissions of green leaf volatiles were unaffected. In a six-arm olfactometer, the parasitoids Cotesia marginiventris and Microplitis rufiventris responded equally well to odors of herbivore-damaged and fungus- and herbivore-damaged maize plants. Healthy and fungus-infected plants were not attractive. An additional experiment showed that the performance of S. littoralis caterpillars was not affected by the presence of the pathogen, nor was there an effect on larvae of M. rufiventris developing inside the caterpillars. Our results confirm previous indications that naive wasps may respond primarily to the green leaf volatiles.
  • Publication
    Métadonnées seulement
    The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps
    (2006)
    D'Alessandro, Marco
    ;
    Held, Matthias 
    ;
    Triponez, Yann
    ;
    Turlings, Ted 
    After herbivore attack, plants release a plethora of different volatile organic compounds (VOCs), which results in odor blends that are attractive to predators and parasitoids of these herbivores. VOCs in the odor blends emitted by maize plants (Zea mays) infested by lepidopteran larvae are well characterized. They are derived from at least three different biochemical pathways, but the relative importance of each pathway for the production of VOCs that attract parasitic wasps is unknown. Here, we studied the importance of shikimic acid derived VOCs for the attraction of females of the parasitoids Cotesia marginiventris and Microplitis rufiventris. By incubating caterpillar-infested maize plants in glyphosate, an inhibitor of the 5-enolpyruvylshikimate-3-phospate (EPSP) synthase, we obtained induced odor blends with only minute amounts of shikimic acid derived VOCs. In olfactometer bioassays, the inhibited plants were as attractive to naive C. marginiventris females as control plants that released normal amounts of shikimic acid derived VOCs, whereas naive M. rufiventris females preferred inhibited plants to control plants. By adding back synthetic indole, the quantitatively most important shikimic acid derived VOC in induced maize odors, to inhibited plants, we showed that indole had no effect on the attraction of C. marginiventris and that M. rufiventris preferred blends without synthetic indole. Exposing C. marginiventris females either to odor blends of inhibited or control plants during oviposition experiences shifted their preference in subsequent olfactometer tests in favor of the experienced odor. Further learning experiments with synthetic indole showed that C. marginiventris can learn to respond to this compound, but that this does not affect its choices between natural induced blends with or without indole. We hypothesize that for naive wasps the attractiveness of an herbivore-induced odor blend is reduced due to masking by nonattractive compounds, and that during oviposition experiences in the presence of complex odor blends, parasitoids strongly associate some compounds, whereas others are largely ignored.
  • Publication
    Accès libre
    Odour-mediated long-range avoidance of interspecific competition by a solitary endoparasitoid : a time-saving foraging strategy
    (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.
  • Publication
    Accès libre
    A comparison of naïve and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odours
    (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.
  • Publication
    Accès libre
    Evaluating the Induced-Odour Emission of a Bt Maize and its Attractiveness to Parasitic Wasps
    (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.