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

Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, SE-230 53 Alnarp, Sweden.
Journal of Experimental Biology (Impact Factor: 2.9). 10/2010; 213(Pt 19):3332-9. DOI: 10.1242/jeb.044396
Source: PubMed


We 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 μg) 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.

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Available from: Qing-He Zhang
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    • "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). Our results raise a question about the actual emission rates of trans-4-thujanol from spruce tree bark in nature. "
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    ABSTRACT: Key message Spruce trees emit significant amounts of trans-4-thujanol, but the amount of this compound in bark decreases with tree age. Trans-4-thujanol acts as an efficient repellent for the bark beetle Ips typographus. Context The spruce bark beetle, Ips typographus, is an economically significant pest of Norway spruce (Picea abies) that preferentially infests and kills old trees. Aims We looked for spruce volatiles that were perceivable by I. typographus and that differed as the host tree aged. Methods Bark beetles were collected in the wild. Bark samples from spruce trees of different age were hydrodistilled. Gas chromatography–electroantennogram detection (GC-EAD) was used to identify which compounds induced beetle olfactory responses. These were identified by gas chromatography–mass spectrometry (GC-MS). Behavioural responses of bark beetles were tested using a Y-tube olfactometer. Results Several EAD peaks were recorded, of which trans-4-thujanol was consistently active and could be identified chemically unequivocally. The antennae of I. typographus females responded to a lower dosage of the compound than males, but both sexes were repelled by it. The bark of 10-year-old spruce trees contained 3 times more trans-4-thujanol than that of 35- 40-year-old trees, 27 times more than that of 70- to 80-year-old trees, and 200 times more than that of 120-year-old trees. Conclusions Trans-4-thujanol is a bioactive compound in Norway spruce bark that varies in amount with tree age and affects spruce bark beetle behaviour under laboratory conditions. It is suggested that trans-4-thujanol might play a role in both spruce tree defence and tree choice by beetles.
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    • "For instance, mass-trapping using aggregation pheromones , sometimes in combination with host plant volatiles (Guarino et al., 2011), has been successful for other weevil species (Cross et al., 2006; Rhino et al., 2010; Smith, 1998). In addition, plant compounds from both hosts and non-hosts might act as anti-attractants, like in many species of bark beetles (Andersson et al., 2010; Zhang and Schlyter, 2004). "
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    • "An independent perception of these compounds in the periphery might enable quick adaptation of the invasive insect to changing situations regarding host plant suitability just by altering the central processing of the mixture information (Carlsson 2007). Andersson et al. (2010) differentiated between behaviourally synergistic, inhibitory and redundant stimulus compounds suggesting that the ORNs of I. typographus were remarkably narrowly tuned in their response specificity to a small number of structurally related compounds. Stimulus compounds perceived by one type of ORN could be substituted in behavioural experiments without alteration of the outcome. "
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