Peripheral modulation of pheromone response by inhibitory host compound in a beetle

Abstract

SUMMARYWe identified several compounds, by gas chromatographic-electroantennographic detection (GC-EAD), that were antennally active in the bark beetle Ips typographus and also abundant in beetle-attacked spruce trees. One of them, 1,8-cineole (Ci), strongly inhibited the attraction to pheromone in the field. Single-sensillum recordings (SSRs) previously showed olfactory receptor neurons (ORNs) on I. typographus antennae selectively responding to Ci. All Ci neurons were found within sensilla co-inhabited by a pheromone neuron responding to cis-verbenol (cV); however, in other sensilla, the cV neuron was paired with a neuron not responding to any test odorant. We hypothesized that the colocalization of ORNs had a functional and ecological relevance. We show by SSR that Ci inhibited spontaneous activity of the cV neuron only in sensilla in which the Ci neuron was also present. Using mixtures of cV and Ci, we further show that responses to low doses (1-10ng) of cV were significantly reduced when the colocalized Ci neuron simultaneously responded to high doses (1-10mg) of Ci. This indicated that the response of the Ci neuron, rather than ligand-receptor interactions in the cV neuron, caused the inhibition. Moreover, cV neurons paired with Ci neurons were more sensitive to cV alone than the ones paired with the non-responding ORN. Our observations question the traditional view that ORNs within a sensillum function as independent units. The colocalization of ORNs might sharpen adaptive responses to blends of semiochemicals with different ecological significance in the olfactory landscape.

Electrophysiological and behavioural responses of Ips typographus (L.) to trans-4-thujanol—a host tree volatile compound

“…Despite trans-4-thujanol being repellent for bark beetles under laboratory conditions, it remains to be investigated whether it is active in the field. We assume that this compound belongs to the group of already known substances decreasing attraction of I. typographus adults, including 1,8-cineole and (−)-limonene both produced by spruce trees (Andersson et al 2010;Schiebe et al 2012), verbenone released by microorganisms in the galleries of bark beetles (review in Byers 2004) and green leaf volatiles emitted by many non-host trees (Zhang et al 1999), as well as ipsenol and ipsdienol produced by I. typographus males to avoid competition in the later phases of tree attack (Birgersson et al 1988).…”

“…For I. typographus for example, α-pinene-the predominant monoterpene in Norway spruce-enhances the attractiveness of the aggregation pheromone (Erbilgin et al 2007;Jakuš and Blaženec 2003). Conversely, 1,8-cineole acts as an antagonist inhibiting attraction to the aggregation pheromone (Andersson et al 2010). A field survey indicated that trees that were attacked but not colonised during an outbreak exhibited a greater content of 1,8-cineole than successfully colonised trees (Schiebe et al 2012), suggesting the involvement of this compound in tree resistance.…”

Host Plant Species Differentiation in a Polyphagous Moth: Olfaction is Enough

“…Another specific feature of cabbage odor is the high proportion of eucalyptol in its GC-EAD active volatile profile. In bark beetles eucalyptol strongly reduces pheromone attraction, and inhibits the activation of pheromone-OSN, through the activation of a co-localised OSN (Andersson et al 2010).…”

Pest Control Compounds Targeting Insect Chemoreceptors: Another Silent Spring?

“…A similar story is emerging for aggregation pheromones of tree-killing bark beetles, which during outbreaks can be a serious threat to forests, both planted and unmodified (Raffa et al, 2016). In the European spruce bark beetle, Ips typographus, the herbivore-induced spruce defense compound, 1,8-cineole (Schiebe et al, 2012), strongly reduces attraction to the aggregation pheromone, which is used to coordinate deadly mass-attacks on trees (Andersson et al, 2010;Binyameen et al, 2014). The sensory neuron that detects 1,8-cineole is housed within the same sensilla as that for one of the essential aggregation pheromone components, and when the 1,8-cineole neuron responds, the response to the aggregation pheromone component in the other neuron is inhibited, probably via passive electrical interactions between neurons (Andersson et al, 2010).…”