Plant Terpenes Affect Intensity and Temporal Parameters of Pheromone Detection in a Moth

Abstract

In moths, the components of the female pheromone blend are detected in the male antennae by pheromone olfactory receptor neurons (Ph-ORNs) expressing narrowly tuned olfactory receptors. Responses to sex pheromones have generally been thought to be independent from the odorant background. However, interactions between pheromone components and plant volatiles have been reported at behavioral and detection levels. To document the mechanisms of such interactions, we analyzed Ph-ORN responses of Spodoptera littoralis to the main pheromone component, Z9E11-14:Ac, in the presence of 4 monoterpenes. To mimic natural contexts in which plant odors and pheromone emanate from different sources, the 2 stimuli were presented with different temporal patterns and from independent sources. Linalool reversibly reduced the firing response to Z9E11-14:Ac and produced an off effect. Geraniol and geranyl and linalyl acetates reduced the responses to Z9E11-14:Ac with a longer time course. Pulses of linalool over prolonged pheromone stimulation resulted in a discontinuous firing activity. Pulses of pheromone were better separated over a background of linalool, compared with odorless air. The data confirm that plant compounds may modulate the intensity and the temporal coding by Ph-ORNs of pheromone information. This modulation might positively affect mate location at high pheromone density especially nearby a pheromone source.

Plant odour stimuli reshape pheromonal representation in neurons of the antennal lobe macroglomerular complex of a male moth

“…The resolution of pulsed pheromone stimuli further improved when heptanal was added, especially for A2 neurons, because of the shortening of the E1 phase and the lengthening of the following inhibition. In S. littoralis, an improvement of pulse resolution in pheromone specific ORNs was also found when pheromone stimuli were applied in a plant odour background (Party et al, 2009;Rouyar et al, 2011). The contrast enhancement between the single spike trains emitted in response to the discontinuous mixture signal in A2 neurons in A. ipsilon is amplified at the neuron population scale.…”

“…Evidence for inhibitory effects of plant compounds on pheromone responses in antennal sensilla responding exclusively to pheromone compounds has been found in several moth species (e.g. Pophof and van der Goes van Naters, 2002;Party et al, 2009), including A. ipsilon, using single sensillum recordings (Deisig et al, 2012). Optical imaging studies have also shown that the input of pheromone information to the AL is reduced when adding plant odours (Deisig et al, 2012).…”

“…All three interaction types have been found in insects at different neuronal levels from the analysis of responses to mixtures of general odorants and mixtures of pheromone components [honeybee (Deisig et al, 2006); moths (Martin and Hildebrand, 2010;Kuebler et al, 2011;Hillier and Vickers, 2011); Drosophila (Silbering and Galizia, 2007)]. Most interactions of mixtures between plant odours and sex pheromones have been described at the behavioural and peripheral levels (reviewed by Reddy and Guerrero, 2004;Party et al, 2009;von Arx et al, 2011).…”

“…Although a few examples of synergistic effects of plant odours added to sex pheromone have been reported (Ochieng et al, 2002;Plettner and Gries, 2010), the most frequently observed effect consisted of a suppression of the pheromonal response when a plant odour is added (Schneider et al, 1964;Den Otter et al, 1978;Kaissling et al, 1989;Pophof and van der Goes van Naters, 2002;Party et al, 2009).…”

“…In virgin males of the noctuid moth Agrotis ipsilon, an increase of responses to the flower volatile heptanal was found in AL neurons of the OG when adding the sex pheromone (Barrozo et al, 2010). Most of these studies [except on the peripheral level (Party et al, 2009;Rouyar et al, 2011)] on mixtures of sex pheromone and plant odours were performed using individual stimulations of odours, thus revealing static aspects (e.g. synergy and inhibition) of odour mixture perception.…”