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

Authors: ROBERT, CHRISTELLE - University Of Neuchatel; ERB, MATTHIAS - Max Planck Society; Hibbard, Bruce; French, Bryan; ZWAHLEN, CLAUDIA - University Of Neuchatel; TURLINGS, TED - University Of Neuchatel

Submitted to: Functional Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/29/2012
Publication Date: 7/9/2012
Citation: Christelle, R.A., Erb, M., Hibbard, B.E., French, B.W., Zwahlen, C., Turlings, T.C. 2012. A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density dependent manner. Functional Ecology. 26:1429-1440.

Interpretive Summary: Leaf-herbivores have previously been found to trigger induced defences in plants, but some specialist herbivores can take advantage of these induced changes and use them to their advantage. Compared to above-ground plant-insect interactions, little is known about this phenonema below ground. A recent study suggested that feeding by the western corn rootworm (WCR) makes corn roots more susceptible to other WCR larvae. To better understand this, we conducted a series of experiments to study the behavioral responses of WCR to increased numbers of feeding larvae and to determine the underlying biochemical aspects of the host plant that alter WCR behavior. We found that WCR benefited from feeding on a root system in groups of intermediate size, whereas its performance was reduced in larger groups. Interestingly, WCR were able to select host plants with an optimal density of other larvae by using a damage induced release of a volatile chemical from the plant. Chemical analyses showed that the induced-susceptibility is likely to stem from a combination of (i) increased free amino acid concentrations in the plant roots and (ii) the relaxation of plant-defense inducibility. These findings show that WCR can use induced plant volatiles to aggregate on a host plant and can change the plant's metabolism to its own benefit, perhaps helping to explain the remarkable ecological success of WCR in corn fields around the world.

Technical Abstract: 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 behavioral responses and elucidate the underlying biochemical mechanisms. 3. We found that D. virgifera benefited from feeding on a root system in groups of intermediate size, whereas its performance was reduced in large groups. Interestingly, the herbivore was able to select host plants with an optimal density of conspecifics by using the induced plant volatile (E)-ß-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 defenses 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 defense inducibility. 4. These findings show that herbivores can use induced plant volatiles in an optimal, 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.