Volatile-Mediated Signalling Between Potato Plants in Response to Insect Herbivory is not Contingent on Soil Nutrients

Abstract

Plant-plant signalling via volatile organic compounds (VOCs) has been studied intensively, but its contingency on abiotic conditions (e.g., soil nutrients, drought, warming) is poorly understood. To address this gap, we carried out a greenhouse experiment testing whether soil nutrients influenced signalling between potato (Solanum tuberosum) plants in response to insect leaf herbivory by the generalist caterpillar Spodoptera exigua. We placed pairs of plants in plastic cages, where one plant acted as a VOC emitter and the other as a receiver. We factorially manipulated soil nutrients for both emitter and receiver plants, namely: unfertilized (baseline soil nutrients) vs. fertilized (augmented nutrients). Then, to test for signalling effects, half of the emitters within each fertilization level were damaged by S. exigua larvae and the other half remained undamaged. Three days after placing larvae, we collected VOCs from emitter plants to test for herbivory and fertilization effects on VOC emissions and placed S. exigua larvae on receivers to test for signalling effects on leaf consumption and larval mass gain as proxies of induced resistance. We found that herbivory increased total VOC emissions and altered VOC composition by emitter plants, but these effects were not contingent on fertilization. In addition, bioassay results showed that receivers exposed to VOCs from herbivore-damaged emitters had lower levels of herbivory compared to receivers exposed to undamaged emitters. However, and consistent with VOC results, fertilization did not influence herbivore-induced signalling effects on receiver resistance to herbivory. In sum, we found evidence of S. exigua-induced signalling effects on resistance to herbivory in potato plants but such effects were not affected by increased soil nutrients. These results call for further work testing signalling effects under broader range of nutrient concentration levels (including nutrient limitation), teasing apart the effects of specific nutrients, and incorporating other abiotic factors likely to interact or covary with soil nutrients.

Keywords: Fertilization; Plant-herbivore interaction; Plant-plant communication; Solanum tuberosum; Spodoptera exigua; Volatile organic compounds.

Fig. 1

Experimental design to test for effects of soil nutrients on communication between potato (Solanum tuberosum) plants (N = 80). We paired potato plants designated as emitters and receivers, with half of the emitters receiving damage by Spodoptera exigua larvae (i.e., herbivore-damaged plants) and half serving as undamaged controls. Both emitter and receiver plants were also subject to two fertilization treatments (fertilized vs. unfertilized), resulting in a three-way factorial design

Fig. 2

Effects of emitter herbivore damage treatment (undamaged vs. damaged by Spodoptera exigua) on the total emission of volatile organic compounds (VOCs, in nanograms per hour) produced by unfertilized vs. fertilized emitter potato (Solanum tuberosum) plants. Values shown are model back-transformed least-square means ± SE (N = 18–20)

Fig. 3

Unconstrained ordination (PCoA) showing the effects of (a) emitter herbivore damage treatment (undamaged vs. damaged by Spodoptera exigua feeding) and (b) fertilization treatment (unfertilized vs. fertilized) on the composition of VOCs released by potato (Solanum tuberosum) plants. Biplot arrows represent linear associations with the two most influential volatiles based on their R² values scaled to reflect relative magnitude of effects. Diamonds represent the centroids for each herbivore damage or fertilization treatment and associated 95% ellipses. The first two axes together accounted for 79.46% and 72.4% of total variation in volatile composition due to herbivore damage and fertilization treatments, respectively

Fig. 4

Percentage of leaf removed by Spodoptera exigua on receiver potato (Solanum tuberosum) plants previously exposed to undamaged (white bars) or herbivore-damaged (grey bars) conspecific emitter plants. Foliar damage on unfertilized and fertilized receivers for each emitter herbivore damage by fertilization combination are shown. Values are model back-transformed least square means ± SE (N = 10)