Response of predatory mites to a herbivore-induced plant volatile: genetic variation for context-dependent behaviour

Abstract

Plants infested with herbivores release specific volatile compounds that are known to recruit natural enemies. The response of natural enemies to these volatiles may be either learned or genetically determined. We asked whether there is genetic variation in the response of the predatory mite Phytoseiulus persimilis to methyl salicylate (MeSa). MeSa is a volatile compound consistently produced by plants being attacked by the two-spotted spider mite, the prey of P. persimilis. We predicted that predators express genetically determined responses during long-distance migration where previously learned associations may have less value. Additionally, we asked whether these responses depend on odors from uninfested plants as a background to MeSa. To infer a genetic basis, we analyzed the variation in response to MeSa among iso-female lines of P. persimilis by using choice-tests that involved either (1) MeSa presented as a single compound or (2) MeSa with background-odor from uninfested lima bean plants. These tests were conducted for starved and satiated predators, i.e., two physiological states, one that approximates migration and another that mimics local patch exploration. We found variation among iso-female lines in the responses to MeSa, thus showing genetic variation for this behavior. The variation was more pronounced in the starved predators, thus indicating that P. persimilis relies on innate preferences when migrating. Background volatiles of uninfested plants changed the predators' responses to MeSa in a manner that depended on physiological state and iso-female line. Thus, it is possible to select for context-dependent behavioral responses of natural enemies to plant volatiles.

Fig. 1

Experimental set-up of the I-tube olfactometer. The diagram depicts a horizontal tube (the glass I-tube) with two openings, where the bigger one serves as an air-outlet. The thick vertical arrow below the I-tube indicates the location of the small opening—the point of release of the predators. The broken line indicates a thin capillary inside the glass tube to provide structure, on each side ending in a metal pin leading down into the trap vial. The trap vials were connected with plastic tubes to jars that either contain a capillary with MeSa or not. The remaining arrows indicate the direction of air-flow. Above the set-up there was a source of dispersed light (not shown)

Fig. 2

The responses of eighteen iso-female lines of Phytoseiulus persimilis by starved predators in the tests (a) MeSa plus clean air vs. clean air, (b) MeSa plus the background of GLVs vs. GLVs, and by satiated predators in the tests (c) MeSa plus clean air vs. clean air, (d) MeSa plus the background of GLVs vs. GLVs. The bars show the proportion of individuals choosing the arm containing MeSa (y-axis) calculated for each line (x-axis). The horizontal lines indicate the average responses obtained by pooling replicates over all iso-female lines within each of the experimental treatments. Note that in each panel the ordering of lines from low to high response results in a different sequence of lines, e.g., line 10 is on the right in (c) and (d) but on the left in (a) and in the middle in (b)

Fig. 3

Illustration of the interaction between iso-female line, hunger level and GLVs context in selected iso-female lines; the graphs present the mean proportions of individuals choosing MeSa (values on the y-axis) categorized by the factors. Open circles connected by dashed line refer to the responses of the starved predators, closed squares connected by solid line to the responses of the satiated predators, and the x-axis presents the categorization with respect to GLVs context

Fig. 4

Variation in the mean proportion of no-choice individuals (y-axis) in the 18 iso-female lines (x-axis) of Phytoseiulus persimilis categorized by hunger level and GLVs context. No-choice individuals are those that remained in the glass tube for the duration of the test, i.e. did not make a choice. The panels present the proportions observed for starved predators in the tests (a) MeSa plus clean air vs. clean air, (b) MeSa plus the background of GLVs vs. GLVs, and for satiated predators in tests (c) MeSa plus clean air vs. clean air, (d) MeSa plus the background of GLVs vs. GLVs