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Plants and trees live surrounded by individuals of the same species (conspecifics) and different species (heterospecifics). Co-occurring species may share their preferences for soil, light, nutrient and moisture conditions and benefit from the presence of each other through interactions such as mycorrhizal symbiosis (Urcelay et al., 2003). However, associational resistance, where a species experiences reduced herbivore attack through coexistence with other plant species (Karban, 2007), might be an important mediator of species abundance. Recent research has revealed that plants can sense their neighbours without direct physical contact; mechanisms for this include detection of a reduced ratio of red to far-red in light reflected from neighbouring foliage (Tao et al., 2008), or detection of plant-emitted volatile compounds (Baldwin et al., 2006; Heil & Karban, 2010). Plant volatiles have various ecological roles, including attraction and deterrence of herbivores (Baker et al., 1998; Bruce et al., 2005), while herbivore-induced emissions may attract natural enemies to suppress herbivore pressure in the process of indirect defence (Turlings et al., 1990; Dicke, 2009). In natural environments, it is evident that the volatile bouquets of neighbouring species become mixed. However, existing evidence that volatiles affect herbivore abundance on neighbouring plants (Karban, 2007) and behaviour of insects (De Moraes et al., 1998) in nature suggest that this does not result in an infochemical chaos, but that individual organisms can benefit from volatile cues.
Previous research on plant–plant signalling via airborne plant-emitted volatiles has revealed that induced volatiles are able to activate volatile compound release (Choh et al., 2004), defence gene expression (Arimura et al., 2000) and synthesis of phenolics, proteinase inhibitors (Tscharntke et al., 2001) and extrafloral nectar (Heil & Silva Bueno, 2007) in signal-receiving plants. It has recently been shown that exposure to volatiles can prime plants to have faster defence responses upon subsequent herbivore attack (Kessler et al., 2006; Heil & Silva Bueno, 2007). However, passive adsorption of volatiles emitted by neighbouring plants might also be an important, but understudied, way for volatiles to act in natural environments. Choh et al. (2004) found that volatiles can be adsorbed to and re-released from conspecific plants. To show this, they treated Lima bean (Phaseolus lunatus) leaves with a protein-synthesis inhibitor to suppress production of herbivore-induced volatiles. These leaves were then exposed to spider mite (Tetranychus urticae)-infested Lima bean plants, and were subsequently shown to emit volatiles associated with herbivore damage. As the receiver leaves were unable to synthesize these volatiles, a passive adsorption and release process was concluded. In the laboratory, exogenous monoterpene fumigation resulted in nonemitting oak (Quercus suber) leaves subsequently releasing monoterpenes for more than 12 h (Delfine et al., 2000). However, passive adsorption and re-release of volatiles has not been demonstrated interspecifically under field conditions.
Neighbour-emitted compounds could be ecologically beneficial to the plant to which they adsorb, if they either deter herbivores (Karban, 2007) or attract herbivore natural enemies. For the emitting plant, this would probably present a neutral situation: it will emit the same volatiles despite its neighbour. However, it might also have an impact on competitive dynamics, for example, if there were phytotoxic effects on receiver plant foliage (Barney et al., 2005). Improving the performance of a neighbour’s herbivores by attracting them in higher numbers or by attenuating the foraging efficiency of natural enemies of a neighbour’s herbivores might lead to negative effects of neighbouring. The fitness of the emitting plant may even be altered, for example, by reduced root and light competition. Benefits or costs of coexistence mediated by volatile communication are multifaceted (Heil & Karban, 2010). The importance of volatile-mediated plant–herbivore interactions is ultimately dependent on the amount of herbivore pressure and whether it is significant enough in the ecosystem to affect plant fitness (Karban, 2007).
Rhododendron tomentosum (Stokes) H. Harmaja (formerly known as Ledum palustre L.) is an abundant perennial evergreen shrub distributed throughout boreal ecosystems (Urcelay et al., 2003). R. tomentosum has a characteristic aromatic profile as a result of its high volatile terpenoid content (Butkiene et al., 2008). These compounds have both medicinal (Harbilas et al., 2009) and arthropod-repellent properties (Jaenson et al., 2005, 2006). The specific volatiles emitted by R. tomentosum are the sesquiterpene alcohols palustrol (C15H26O) and ledol (C15H26O) and the sesquiterpene ledene (C15H24) (Jaenson et al., 2005). In addition, it emits the monoterpene β-myrcene (C10H16) as a major compound (Jaenson et al., 2005, 2006; Butkiene et al., 2008). Betula spp. (Betulaceae) trees commonly coexist with R. tomentosum in natural ecosystems (Urcelay et al., 2003). Reanalysis of chromatograms from our earlier study of mountain birch (Betula pubescens ssp. czerepanovii (Orlova) Hämet-Ahti) leaf volatiles (Mäntyläet al., 2008) indicated traces of ledol and palustrol, when R. tomentosum had been growing nearby. The emission of these specific ‘sticky’ volatiles makes R. tomentosum an excellent species for studying how passive adsorption of volatiles might contribute to associational resistance and neighbouring plant interactions. Oxygenated sesquiterpenoids are particularly resistant to degradation by ozone in the atmosphere (Pinto et al., 2007), have semi-volatile characteristics (boiling point at 240–400°C and low vaporization rate to gaseous phase at 20–25°C (Hübner & Röpcke, 2009)) and could therefore persist on surfaces such as leaf foliage (Helmig et al., 2004).
We established a field experiment with potted silver birch (Betula pendula Roth) growing either alone or in identical plots with R. tomentosum as neighbours, that is, exposed to airborne volatiles but isolated below ground. We first tested whether the semi-volatile sesquiterpenoids or other volatiles released from R. tomentosum were adhered to and subsequently re-released from B. pendula leaves. Ecologically, this would mean a change in the volatile profile experienced by herbivores attacking B. pendula when it coexists with R. tomentosum. Additionally, we collected volatiles in a natural peatland ecosystem, where downy birch (Betula pubescens Ehrh.) and R. tomentosum coexisted.
Betula species host numerous herbivores from different feeding guilds (Koponen, 1983; Atkinson, 1992). To test for associational resistance in B. pendula neighbouring R. tomentosum, we screened for the attractiveness of R. tomentosum-neighbouring birch leaves to three species of generalist herbivores, the green leaf weevil Polydrusus flavipes Degeer (Coleoptera: Curculionidae), the autumnal moth Epirrita autumnata (Borkhausen) (Lepidoptera: Geometridae) and the birch aphid Euceraphis betulae Koch. (Homoptera: Aphididae). E. autumnata larvae are major pests of birch trees in boreal and subarctic ecosystems and may appear in extensive outbreaks that can result in total destruction of birch foliage (Haukioja et al., 1988). Leaf weevils can be a serious problem for birch forest plantations. In the field experiment, we also screened for season-long natural abundance of other herbivores in R. tomentosum associated and control B. pendula plots.
We report passive adsorption and re-release of specific R. tomentosum-emitted volatiles by birch leaves in field and laboratory experiments, as well as in observations in a natural habitat. Our results show a volatile-mediated ecologically meaningful plant–tree interaction, which might benefit the receiver without its own input contribution. Associational resistance in Betula spp. through coexistence with R. tomentosum is suggested based on certain herbivore-repellent effects observed for R. tomentosum and R. tomentosum volatile-exposed birches.