A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner

Christelle Aurélie Maud Robert, Matthias Erb, Bruce Elliott Hibbard, B. W. French, Claudia Zwahlen & Ted Turlings

Résumé 1. Leaf-herbivore attack often triggers induced resistance in plants. However, certain specialist herbivores can also take advantage of the induced metabolic changes. In some cases, they even manipulate plant resistance, leading to a phenomenon called induced susceptibility. Compared to above-ground plant-insect interactions, little is known about the prevalence and consequences of induced responses below-ground.
2. A recent study suggested that feeding by the specialist root herbivore Diabrotica virgifera virgifera makes maize roots more susceptible to conspecifics. To better understand this phenomenon, we conducted a series of experiments to study the behavioural responses and elucidate the underlying biochemical mechanisms.
3. We found that D. virgifera benefitted from feeding on a root system in groups of intermediate size (39 larvae/plant in the laboratory), whereas its performance was reduced in large groups (12 larvae/plant). Interestingly, the herbivore was able to select host plants with a suitable density of conspecifics by using the induced plant volatile (E)-beta-caryophyllene in a dose-dependent manner. Using a split root experiment, we show that the plant-induced susceptibility is systemic and, therefore, plant mediated. Chemical analyses on plant resource reallocation and defences upon herbivory showed that the systemic induced-susceptibility is likely to stem from a combination of (i) increased free amino acid concentrations and (ii) relaxation of defence inducibility.
4. These findings show that herbivores can use induced plant volatiles in a density-dependent manner to aggregate on a host plant and change its metabolism to their own benefit. Our study furthermore helps to explain the remarkable ecological success of D. virgifera in maize fields around the world.
Mots-clés defence inducibility relaxation, diabrotica virgifera virgifera, induced susceptibility, resource reallocation, root-herbivore interactions, zea mays, western corn-rootworm, below-ground herbivory, cell-wall invertase, larvae coleoptera, water-stress, arabidopsis-thaliana, insect herbivores, amino-acids, maize, chrysomelidae
Citation Robert, C. A. M., Erb, M., Hibbard, B. E., French, B. W., Zwahlen, C., & Turlings, T. (2012). A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner. Functional Ecology, 26(6), 1429-1440.
Type Article de périodique (Anglais)
Date de publication 2012
Nom du périodique Functional Ecology
Volume 26
Numéro 6
Pages 1429-1440