Positive Chemotaxis of the Entomopathogenic Nematode Steinernema australe (Panagrolaimorpha: Steinenematidae) towards High-Bush Blueberry (Vaccinium corymbosum) Root Volatiles

Abstract

The foraging behavior of the infective juveniles (IJs) of entomopathogenic nematodes (EPNs) relies on host-derived compounds, but in a tri-trophic context, herbivore-induced root volatiles act as signals enhancing the biological control of insect pests by recruiting EPNs. In southern Chile, the EPN Steinernema australe exhibits the potential to control the raspberry weevil, Aegorhinus superciliosus, a key pest of blueberry Vaccinium corymbosum. However, there is no information on the quality of the blueberry root volatile plume or the S. australe response to these chemicals as putative attractants. Here, we describe the root volatile profile of blueberries and the chemotaxis behavior of S. australe towards the volatiles identified from Vaccinium corymbosum roots, infested or uninfested with A. superciliosus larvae. Among others, we found linalool, α-terpineol, limonene, eucalyptol, 2-carene, 1-nonine, 10-undecyn-1-ol, and methyl salicylate in root volatiles and, depending on the level of the emissions, they were selected for bioassays. In the dose-response tests, S. australe was attracted to all five tested concentrations of methyl salicylate, 1-nonine, α-terpineol, and 2-carene, as well as to 100 µg mL^-1 of 10-undecyn-1-ol, 0.1 and 100 µg mL^-1 of linalool, and 100 µg mL^-1 of limonene, whereas eucalyptol elicited no attraction or repellency. These results suggest that some volatiles released from damaged roots attract S. australe and may have implications for the biocontrol of subterranean pests.

Keywords: belowground interactions; entomopathogenic nematode recruitment; foraging behavior; olfactometer; root volatiles.

Figure 1

The Gardner–Altman estimation plot for the percentage of IJs collected in the water and the hexane. The grey dots represent the replicates, and the vertical red solid lines and the red dots represent the confidence intervals at 95% and their respective means, respectively. The effect size for the mean difference is shown (right scale), and the triangle and its vertical line represent the estimated difference between the water and the hexane. The bootstrapping confidence interval (95%) was obtained by a two-sided permutation t-test with 5000 permutations.

Figure 2

Dose–response chemotaxis trials. The mean difference (%) of the IJs collected from the olfactometric bioassays between the compound dose and control (±95% CI). The positive values indicate the IJs’ attraction to the dose of the corresponding treatment, and when it is a 95% confidence interval and does not include the value 0%, the difference is considered significant (p < 0.05). Zero represents the control (horizontal dotted line). We estimated the confidence intervals by a two-sided permutation t-test with 5000 permutations.

Figure 3

Schematic representation of the root volatile collection by solid-phase microextraction.

Figure 4

Schematic representation of the olfactometer designed to perform the behavioral assays with Steinernema australe and the selected compounds.