Herbivore-induced plant volatiles, not natural enemies, mediate a positive indirect interaction between insect herbivores

ABSTRACTIn response to insect herbivory, plants mobilize various defenses. Defense responses include the release of herbivore-induced plant volatiles (HIPVs) that can serve as signals to alert undamaged tissues and to attract natural enemies of the herbivores. Some HIPVs can have a direct negative impact on herbivore survival, but it is not well understood by what mechanisms. Here, we tested the hypothesis that exposure to HIPVs renders insects more susceptible to natural pathogens. Exposure of the caterpillars of the noctuidSpodoptera exiguato indole and linalool, but not exposure to (Z)-3-hexenyl acetate, increased the susceptibility toSpodoptera exiguamultiple nucleopolyhedrovirus(SeMNPV). We also found that exposure to indole, but not exposure to linalool or (Z)-3-hexenyl acetate, increased the pathogenicity ofBacillus thuringiensis. Additional experiments revealed significant changes in microbiota composition after forty-eight hours of larval exposure to indole. Overall, these results provide evidence that certain HIPVs can strongly enhance the susceptibility of caterpillars to pathogens, possibly through effects on the insect gut microbiota. These findings suggest a novel mechanism by which HIPVs can protect plants from herbivorous insects.IMPORTANCEMultitrophic interactions involving insect pests, their natural enemies, microorganisms, and plant hosts are increasingly being recognized as relevant factors in pest management. In response to herbivory attacks, plants activate a wide range of defenses that aim to mitigate the damage. Attacked plants release herbivore-induced plant volatiles (HIPVs), which can act as priming signals for other plants and attract natural enemies of herbivores, and which may have a direct negative impact on herbivore survival. In the present work, we show that exposure of the insects to the induced volatiles could increase the insects’ susceptibility to the entomopathogens naturally occurring in the plant environment. These findings suggest a novel role for plant volatiles by influencing insect interactions with natural pathogens, probably mediated by alterations in the insect microbiota composition. In addition, this work provides evidence for selectable plant traits (production of secondary metabolites) that can have an influence on the ecology of the pests and could be relevant in the improvement of pest management strategies using natural entomopathogens.

Download Full-text

Olfactory learning by predatory arthropods

Animal Biology ◽

10.1163/157075606777304221 ◽

2006 ◽

Vol 56 (2) ◽

pp. 143-155 ◽

Cited By ~ 35

Author(s):

Jetske de Boer ◽

Marcel Dicke

Keyword(s):

Natural Enemies ◽

Plant Volatiles ◽

Phytoseiulus Persimilis ◽

Olfactory Learning ◽

Future Research ◽

Induced Plant Volatiles ◽

Herbivore Species ◽

Herbivore Induced Plant Volatiles ◽

New Evidence ◽

Predatory Arthropods

AbstractMany natural enemies of herbivorous arthropods can use herbivore-induced plant volatiles to locate their prey. The composition of herbivore-induced volatile blends is highly variable, e.g., for different plant or herbivore species. When this variation is predictable during the lifetime of an individual, learning is expected to be adaptive for natural enemies that use such information. Learning has indeed been demonstrated many times for parasitoid wasps that use herbivore-induced plant volatiles to locate their hosts. However, evidence for learning of plant volatiles by predatory mites and insects is scarce and this is the topic of the present paper. We first review previously published research that demonstrated that anthocorid bugs and the predatory mite Phytoseiulus persimilis have the capacity to learn. Next, we present new evidence for an effect of previous experiences of P. persimilis on its responses to mixtures of volatile blends, induced by prey or non-prey herbivores. Finally, we discuss the ecological relevance of olfactory learning by predatory arthropods and the need to address this topic in future research.

Download Full-text

Predatory Earwigs are Attracted by Herbivore-Induced Plant Volatiles Linked with Plant Growth-Promoting Rhizobacteria

Insects ◽

10.3390/insects11050271 ◽

2020 ◽

Vol 11 (5) ◽

pp. 271 ◽

Cited By ~ 1

Author(s):

Kim Bell ◽

Natalia Naranjo-Guevara ◽

Rafaela C. dos Santos ◽

Richard Meadow ◽

José M. S. Bento

Keyword(s):

Plant Growth ◽

Natural Enemies ◽

Plant Volatiles ◽

Plant Growth Promoting Rhizobacteria ◽

Specialist Herbivore ◽

Generalist Herbivore ◽

Induced Plant Volatiles ◽

Plant Growth Promoting ◽

Herbivore Induced Plant Volatiles ◽

Growth Promoting

Plant-associated microbes may induce plant defenses against herbivores. Plants, in turn, can attract natural enemies, such as predators, using herbivore-induced plant volatiles. Intricate communication occurs between microorganisms, plants, and insects. Given that many aspects related to mechanisms involved in this symbiotic system remain unknown, we evaluated how beneficial soil-borne microorganisms can affect the interactions between plants, herbivores, and natural enemies. For this study, we established a multitrophic system composed of the predatory earwig Doru luteipes (Dermaptera: Forficulidae), arugula (Eruca sativa, Brassicaceae) as the host plant, Plutella xylostella (Lepidoptera: Plutellidae) larvae as a specialist herbivore, Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae as a generalist herbivore, and Bacillus amyloliquefaciens as the plant growth-promoting rhizobacteria (PGPR), in a series of nocturnal olfactometry experiments. By assessing earwig preference towards herbivore-induced and PGPR-inoculated plants in different combinations, we showed that the interaction between rhizobacteria, plants, and herbivores can affect the predatory earwig’s behavior. Furthermore, we observed a synergistic effect in which earwigs were attracted by plants that presented as PGPR inoculated and herbivore damaged, for both specialist and generalist herbivores. Our findings help fill the important knowledge gap regarding multitrophic interactions and should provide useful guidelines for their application to agricultural fields.

Download Full-text