Ted Turlings

Research interests

We mainly study the chemical ecology of plant-insect interactions. By unraveling how plants defend themselves against insect attacks and how specialized insects have evolved to circumvent these defenses, we hope to provide ideas for novel, sustainable strategies for the control of agricultural pests.

Quite some years ago, we revealed that plants under attack by caterpillars initiate a systemic release of specific volatiles. This plant response results in an odour that serves as a signal used by parasitic wasps to locate their hosts, whereas several herbivorous insects are repelled by the odour. Studies into the mechanisms of the plant response showed that it is greatly enhanced by factors in the oral secretions of herbivorous insects. This work initially started at the USDA in Gainesville, Florida, where we eventually isolated and identified a powerful elicitor from the regurgitant of Spodoptera larvae, a fatty acid-amino acid conjugate, which was named volicitin. We also studied how caterpillar-induced volatiles can prime neighboring plants to prepare for incoming attack, and we identified indole as a key inducible volatile in such interactions among maize plants.

Our work at the University of Neuchâtel on root signals revealed that root feeding by larvae of the important maize pest Diabrotica virgifera virgifera results in the release of E-(β)-caryophyllene. This sesquiterpene was identified with the help of our collaborators at the Max Planck Institute for Chemical Ecology in Jena and was found to be highly attractive to entomopatogenic nematodes. Many American maize lines do not release this signal and this is reflected in poor attraction of and infection by the nematodes in field experiments conducted with the help of scientists at CABI Bioscience, Switzerland. By genetically transforming a non-emitting maize line we obtained ultimate evidence for the key role of E-(β)-caryophyllene in the attraction of entomopathogenic nematodes.

Now that we have obtained considerable insight into the ecology and the mechanisms of these above- and belowground multi-trophic level interactions, we are applying this knowledge to better understand the evolutionary, ecological and applicable aspects of chemical signalling between plants and insects. It is envisioned that our studies will contribute to the development of sustainable pest management practices inspired by nature. 

Our current work revolves around four objectives:

• Deciphering the odorous language used by plants that are under insect or pathogen attack, with the ultimate objective to use sensors for odour-based, real-time detection of pest and diseases.
• Understanding the inducible volatile signals that cotton plants emit and that trigger defense responses in neighboring plants.
• Develop, in collaboration with CABI-Switzerland, a new formulation of entomopathogenic nematodes against the invasive fall armyworm, which is devastating maize fields in Africa and Asia.
• Unraveling the intricacies of how different stages of Diabrotica beetles sequester defense compounds for their own protection.

Publications

Complete publication list

Publication list for the last five years

2020

Kapranas A, Sbaiti I, Degen T, Turlings TJC 2020. Biological control of cabbage fly Delia radicum with entomopathogenic nematodes: selecting the most effective nematode species and testing a novel application method. Biological Control 144: 104212

Bruno P, Machado RAR, Glauser G, Köhler A, Campos-Herrera R, Bernal J, Toepfer S, Erb M, Robert CAM, Arce CC, Turlings TCJ 2020. Entomopathogenic nematodes from Mexico that can overcome the resistance mechanisms of the western corn rootworm. Scientific Reports (in press).

De Lange ES, Laplanche D, Guo H, Xu W, Vlimant M, Erb M, Ton J, Turlings TCJ 2020. Spodoptera frugiperda caterpillars suppress herbivore-induced volatile emissions in maize. Journal of Chemical Ecology. (online: doi: 10.1007/s10886-020-01153-x)

Jaffuel G, Sbaiti I, Turlings CJT 2020. Encapsulated entomopathogenic nematodes can protect maize plants from Diabrotica balteata larvae. Insects11(1): 27; https://doi.org/10.3390/insects11010027

Xu H, Zhou G, Dötterl S, Schäffler I, Degen T, Chen L, Turlings TCJ 2020. Distinct roles of cuticular aldehydes as pheromonal cues in two Cotesiaparasitoids. Journal of Chemical Ecology 46:128-137

2019

Xu H, Zhou G, Dötterl S, Schäffler I, von Arx M, Roeder G, Degen T, Chen L, Turlings TCJ 2019. The combined use of an attractive and repellent sex pheromone by a gregarious parasitoid. Journal of Chemical Ecology 45: 559-569

Abdala-Roberts L, Quijano-Medina T, Moreira X, Parra-Tabla V, Berny-Mier y Teran J, Grandi L, Glauser G, Turlings TCJ, Benrey B 2019. Bottom-up effects of plant defenses and climate on geographic variation in insect herbivory on wild cotton (Gossypium hirsutum). American Journal of Botany 106:1059-1067

Zhang P-J, Wei J-N, Zhao C, Zhang Y-F, Li C-Y, Liu S-S, Dicke M, Yu X-P, Turlings TCJ 2019. Airborne host-plant manipulation by whiteflies via an inducible blend of plant volatiles. Proc. Natl. Acad. Science USA 116: 7387-7396

Imperiali, N, Jaffuel G, Shelby K, Campos-Herrera R, Geisert R, Maurhofer M, Loper J, Keel C, Turlings TCJ, Hibbard BE 2019. Protecting maize from rootworm damage with the combined application of arbuscular mycorrhizal fungi, Pseudomonas bacteria and entomopathogenic nematodes. Scientific Reports 9, 3127 

Abdala-Roberts L, Pérez Niño B, Moreira X, Parra-Tabla V, Grandi L, Glauser G, Benrey B, Turlings TCJ 2019. Effects of early-season insect herbivory on subsequent pathogen infection and ant abundance on wild cotton (Gossypium hirsutum). Journal of Ecology 107: 1518-1529

Jaffuel G, Půža V, Hug A-S, Meuli R G, Nermuť J, Turlings TCJ, Desurmont GA, Campos-Herrera R 2019. Molecular detection and quantification of slug parasitic nematodes from the soil and their hosts. Journal of invertebrate pathology 160: 18-25

Gasmi L, Martínez-Solís M, Frattini A, Ye M, Collado MC, Turlings TCJ, Erb M, Herrero S 2019. Can herbivore-induced volatiles protect plants by increasing the herbivores' susceptibility to natural pathogens? Applied and Environmental Microbiology (online: DOI: 101128/AEM.01468-18)

Machado RAR, Bruno P, CC Marques Arce, Liechti N, Köhler A, Bernal J, Bruggmann R, Turlings TCJ 2019. Photorhabdus khanii subsp. guanajuatensis subsp. nov., isolated from Heterorhabditis atacamensis, and Photorhabdus luminescens subsp. mexicana subsp. nov., isolated from Heterorhabditis mexicana entomopathogenic nematodes. International Journal of Systematic and Evolutionary Microbiology (online: doi: 10.1099/ijsem.0.003154)

2018

Ye M, Veyrat N, Xu H, Turlings TCJ, Erb M 2018. An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars. Science Advances 4.

Xu H, Turlings TCJ 2018. Plant Volatiles as Mate-Finding Cues for Insects. Trends in Plant Science 23: 100-111.

Turlings TCJ, Erb M 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annual Review of Entomology 63: 433-452.

Sobhy IS, Bruce TJ, Turlings TC 2018. Priming of cowpea volatile emissions with defense inducers enhances the plant's attractiveness to parasitoids when attacked by caterpillars. Pest Management Science 74: 966-977.

Jaffuel G, Chappuis L, Guillarme D, Turlings TCJ, Glauser G 2018. Improved separation by at-column dilution in preparative hydrophilic interaction chromatography. Journal of Chromatography A 1532: 136-143.

Jaffuel G, Blanco-Pérez R, Hug A-S, Chiriboga X, Meuli RG, Mascher F, Turlings TCJ, Campos-Herrera R 2018. The evaluation of entomopathogenic nematode soil food web assemblages across Switzerland reveals major differences among agricultural, grassland and forest ecosystems. Agriculture, Ecosystems & Environment 262: 48-57.

Girod P, Rossignaud L, Haye T, Turlings TCJ, Kenis M 2018. Development of Asian parasitoids in larvae of Drosophila suzukii feeding on blueberry and artificial diet. Journal of Applied Entomology 142: 483-494.

Girod P, Lierhmann O, Urvois T, Turlings TCJ, Kenis M, Haye T 2018. Host specificity of Asian parasitoids for potential classical biological control of Drosophila suzukii. Journal of Pest Science.

Gaillard MDP, Glauser G, Robert CAM, Turlings TCJ 2018. Fine-tuning the ‘plant domestication-reduced defense’ hypothesis: specialist vs generalist herbivores. New Phytologist 217: 355-366.

Desurmont GA, Guiguet A, Turlings TCJ 2018. Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning. Biological Invasions 20: 195-206.

de Lange ES, Farnier K, Degen T, Gaudillat B, Aguilar-Romero R, Bahena-Juárez F, Oyama K, Turlings TCJ 2018. Parasitic wasps can reduce mortality of teosinte plants infested with fall armyworm: support for a defensive function of herbivore-Induced plant volatiles. Frontiers in Ecology and Evolution 6.

Chiriboga M. X, Guo H, Campos-Herrera R, Röder G, Imperiali N, Keel C, Maurhofer M, Turlings TCJ 2018. Root-colonizing bacteria enhance the levels of (E)-β-caryophyllene produced by maize roots in response to rootworm feeding. Oecologia 187: 459-468.

Carrasco D, Desurmont GA, Laplanche D, Proffit M, Gols R, Becher PG, Larsson MC, Turlings TCJ, Anderson P 2018. With or without you: Effects of the concurrent range expansion of an herbivore and its natural enemy on native species interactions. Global Change Biology 24: 631-643.

2017

Xu H, Desurmont G, Degen T, Zhou G, Laplanche D, Henryk L, Turlings TCJ 2017. Combined use of herbivore-induced plant volatiles and sex pheromones for mate location in braconid parasitoids. Plant, Cell & Environment 40: 330-339.

Röder G, Mota M, Turlings TCJ 2017. Host plant location by chemotaxis in an aquatic beetle. Aquatic Sciences 79: 309-318.

Jaffuel G, Blanco-Pérez R, Büchi L, Mäder P, Fließbach A, Charles R, Degen T, Turlings TCJ, Campos-Herrera R 2017. Effects of cover crops on the overwintering success of entomopathogenic nematodes and their antagonists. Applied Soil Ecology 114: 62-73.

Imperiali N, Chiriboga X, Schlaeppi K, Fesselet M, Villacrés D, Jaffuel G, Bender SF, Dennert F, Blanco-Pérez R, van der Heijden MGA, Maurhofer M, Mascher F, et al. 2017. Combined field inoculations of Pseudomonas bacteria, arbuscular mycorrhizal fungi, and entomopathogenic nematodes and their effects on wheat performance. Frontiers in Plant Science 8.

Desurmont GA, Köhler A, Maag D, Laplanche D, Xu H, Baumann J, Demairé C, Devenoges D, Glavan M, Mann L, Turlings TCJ 2017. The spitting image of plant defenses: Effects of plant secondary chemistry on the efficacy of caterpillar regurgitant as an anti-predator defense. Ecology and Evolution 7: 6304-6313.

Chiriboga X, Campos-Herrera R, Jaffuel G, Röder G, Turlings TCJ 2017. Diffusion of the maize root signal (E)-β-caryophyllene in soils of different textures and the effects on the migration of the entomopathogenic nematode Heterorhabditis megidis. Rhizosphere 3: 53-59.

Canestrari D, Bolopo D, Turlings TCJ, Röder G, Marcos JM, Baglione V 2017. Formal comment to Soler et al.: Great spotted cuckoo nestlings have no antipredatory effect on magpie or carrion crow host nests in southern Spain. Plos One 12: e0184446.

Brütsch T, Jaffuel G, Vallat A, Turlings TCJ, Chapuisat M 2017. Wood ants produce a potent antimicrobial agent by applying formic acid on tree-collected resin. Ecology and Evolution 7: 2249-2254.

2016

Veyrat N, Robert CAM, Turlings TCJ, Erb M 2016. Herbivore intoxication as a potential primary function of an inducible volatile plant signal. Journal of Ecology 104: 591-600.

Rasmann S, Turlings TCJ 2016. Root signals that mediate mutualistic interactions in the rhizosphere. Current Opinion in Plant Biology 32: 62-68.

Maag D, Köhler A, Robert CAM, Frey M, Wolfender J-L, Turlings TCJ, Glauser G, Erb M 2016. Highly localized and persistent induction of Bx1-dependent herbivore resistance factors in maize. The Plant Journal 88: 976-991.

Liu X-F, Chen H-H, Li J-K, Zhang R, Turlings TCJ, Chen L 2016. Volatiles released by Chinese liquorice roots mediate host location behaviour by neonate Porphyrophora sophorae (Hemiptera: Margarodidae). Pest Management Science 72: 1959-1964.

Jaffuel G, Mäder P, Blanco-Perez R, Chiriboga X, Fliessbach A, Turlings TCJ, Campos-Herrera R 2016. Prevalence and activity of entomopathogenic nematodes and their antagonists in soils that are subject to different agricultural practices. Agriculture, Ecosystems & Environment 230: 329-340.

16.   Desurmont GA, Zemanova MA, Turlings TC 2016. The gastropod menace: Slugs on Brassica plants affect caterpillar survival through consumption and interference with parasitoid attraction. Journal of Chemical Ecology 42: 183-192.

Desurmont GA, Xu H, Turlings TCJ 2016. Powdery mildew suppresses herbivore-induced plant volatiles and interferes with parasitoid attraction in Brassica rapa. Plant, Cell & Environment 39: 1920-1927.

de Lange ES, Farnier K, Gaudillat B, Turlings TCJ 2016. Comparing the attraction of two parasitoids to herbivore-induced volatiles of maize and its wild ancestors, the teosintes. Chemoecology 26: 33-44.

Ardanuy A, Albajes R, Turlings TCJ 2016. Innate and Learned Prey-Searching Behavior in a Generalist Predator. Journal of Chemical Ecology 42: 497-507.

2015

Sobhy IS, Erb M, Turlings TCJ 2015. Plant strengtheners enhance parasitoid attraction to herbivore-damaged cotton via qualitative and quantitative changes in induced volatiles. Pest Management Science 71: 686-693.

Pineda A, Soler R, Pozo MJ, Rasmann S, Turlings TCJ 2015. Editorial: Above-belowground interactions involving plants, microbes and insects. Frontiers in Plant Science 6: 318.

Maag D, Erb M, Bernal JS, Wolfender J-L, Turlings TCJ, Glauser G 2015. Maize Domestication and Anti-Herbivore Defences: Leaf-Specific Dynamics during Early Ontogeny of Maize and Its Wild Ancestors. Plos One 10.

Köhler A, Maag D, Veyrat N, Glauser G, Wolfender JL, Turlings TCJ, Erb M 2015. Within-plant distribution of 1,4-benzoxazin-3-ones contributes to herbivore niche differentiation in maize. Plant Cell and Environment 38: 1081-1093.

Klauser D, Desurmont GA, Glauser G, Vallat A, Flury P, Boller T, Turlings TCJ, Bartels S 2015. The Arabidopsis Pep-PEPR system is induced by herbivore feeding and contributes to JA-mediated plant defence against herbivory. Journal of Experimental Botany 66: 5327-5336.

Kim J, Jaffuel G, Turlings TCJ 2015. Enhanced alginate capsule properties as a formulation of entomopathogenic nematodes. Biocontrol 60: 527-535.

Jaffuel G, Hiltpold I, Turlings TCJ 2015. Highly potent extracts from Pea (Pisum sativum) and Maize (Zea mays) roots can be used to induce quiescence in entomopathogenic nematodes. Journal of Chemical Ecology 41: 793-800.

Hiltpold I, Jaffuel G, Turlings TCJ 2015. The dual effects of root-cap exudates on nematodes: from quiescence in plant-parasitic nematodes to frenzy in entomopathogenic nematodes. Journal of Experimental Botany 66: 603-611.

Erb M, Veyrat N, Robert CAM, Xu H, Frey M, Ton J, Turlings TCJ 2015. Indole is an essential herbivore-induced volatile priming signal in maize. Nature Communications 6.

Erb M, Robert CAM, Marti G, Lu J, Doyen GR, Villard N, Barrière Y, French BW, Wolfender J-L, Turlings TCJ, Gershenzon J 2015. A physiological and behavioral mechanism for leaf-herbivore induced systemic root resistance. Plant Physiology 169: 2884-2894.

Desurmont GA, Laplanche D, Schiestl FP, Turlings TCJ 2015. Floral volatiles interfere with plant attraction of parasitoids: ontogeny-dependent infochemical dynamics in Brassica rapa. BMC Ecology 15: 1-11.

Chabaane Y, Laplanche D, Turlings TCJ, Desurmont GA 2015. Impact of exotic insect herbivores on native tritrophic interactions: a case study of the African cotton leafworm, Spodoptera littoralis and insects associated with the field mustard Brassica rapa. Journal of Ecology 103: 109-117.

Campos-Herrera R, Puza V, Jaffuel G, Blanco-Perez R, Cepulyte-Rakauskiene R, Turlings TCJ 2015. Unraveling the intraguild competition between Oscheius spp. nematodes and entomopathogenic nematodes: Implications for their natural distribution in Swiss agricultural soils. Journal of Invertebrate Pathology 132: 216-227.

Campos-Herrera R, Jaffuel G, Chiriboga X, Blanco-Perez R, Fesselet M, Puza V, Mascher F, Turlings TCJ 2015. Traditional and molecular detection methods reveal intense interguild competition and other multitrophic interactions associated with native entomopathogenic nematodes in Swiss tillage soils. Plant and Soil 389: 237-255.

Campos-Herrera R, Jaffuel G, Chiriboga X, Blanco-Perez R, Fesselet AM, Hug S, Meuli RG, Mäder P, Mascher F, Turlings TCJ 2015. Understanding the assemblage of entomopathogenic nematodes soil food web in natural and agricultural areas: new insights from a Swiss ecological research network. Journal of Nematology 47: 228-228.

Benrey B, Degen T, Turlings TCJ 2015. Special Issue: 15th International Symposium on Insect-Plant Relationships Preface. Entomologia Experimentalis Et Applicata 157: 1-1.

Amorós-Jiménez R, Robert CM, Ángeles Marcos-García M, Fereres A, Turlings TCJ 2015. A Differential Role of Volatiles from Conspecific and Heterospecific Competitors in the Selection of Oviposition Sites by the Aphidophagous Hoverfly Sphaerophoria rueppellii. Journal of Chemical Ecology 41: 493-500.