Plant-emitted semi-volatiles shape the infochemical environment and herbivore resistance of heterospecific neighbors

Abstract

Plant-emitted volatiles have been reported to shape ecological interactions occurring among species within single or between multiple trophic levels. The ecological contribution of volatiles to plant-herbivore, plant-pathogen, plant-to-plant and multitrophic interactions can be mutualistic, or may either favor or disfavor the players involved in the infochemical network. Emitting, perceiving or being passively engaged with airborne volatiles can result in ecological costs and/or benefits, render competitive advantage and shape population dynamics. We recently demonstrated a cost-effective way for plants to take advantage of volatile-based defense: by adsorbing neighbor-emitted compounds to defend against herbivory. We found that specific semi-volatiles emitted by Rhododendron tomentosum Harmaja are adsorbed to neighboring birch (Betula spp.) foliage in a natural habitat, in a field set-up and in the laboratory. These semi-volatiles were found to deter certain birch herbivores, and may thus confer associational resistance to birch. Here we show the relative change in the volatile profile of birch that occurs when neighbored by R. tomentosum. We further discuss the potential wider role of biogenic semi-volatiles for ecological interactions in natural environments and suggest how they might be utilized for pest management in agricultural crop production.

Plant-emitted, airborne volatiles are an ingenious way for plants to send and receive information on their surrounding environment. Plant volatiles are influenced by a multitude of internal and external factors¹ and have a range of ecological roles such as defense against biotic² and abiotic stressors³ and attraction of pollinators.⁴ Their ability to confer increased resistance has been suggested to create the plasticity plants need to survive in changing environments.⁵ As plant populations are dynamically changing systems, complexly influenced by the biotic and abiotic environment, volatiles emitted by plants growing in heterogeneous associations will become intermingled. The mixture of chemicals emitted by different plants may appear chaotic, but the effects of emissions by neighboring species on the indirect defense of another may be definable. Background volatiles may mask, enhance or be irrelevant to foraging insects in their search for valuable resources that are indicated by volatile plant emissions.⁶ The persistence of plant-emitted volatiles—partly based on their chemical structure⁷—is of great significance to their effects on other neighboring plants. Slowly vaporizing semi-volatiles are of particular interest since they may be quick to condense on neighboring plant surfaces and significantly alter the chemical profile of the exposed plant.

We have recently shown that birch foliage adsorbs specific semi-volatiles emitted from wild rosemary Rhododendron tomentosum Harmaja.⁸ Three R. tomentosum-specific semi-volatiles (ledol, palustrol and ledene) formed 24.5 ± 6.6% and 16.1 ± 7.9% of the total terpenoids emitted by two birch species, B. pendula and B. pubescens, respectively, when they were exposed to neighboring R. tomentosum in a field set-up (B. pendula) or in a natural habitat (B. pubescens) (Fig. 1). This shows a significant difference in the field experiment to the control treatment [p < 0.001 (Mann-Whitney U test)], from which these R. tomentosum-specific compounds were not found. Four hours after removing the B. pendula seedlings from the mixed association, the percentage of these three compounds had decreased to 8.8 ± 2.0%, but they still differed significantly from the control treatment (p < 0.001, Mann-Whitney U test). As the plants were first sampled before noon (10:00 a.m.) and then again 4 h after removing them from the associations (at ca. 2:00 p.m.), part of the loss probably indicates the temperature dependent release of semi-volatile compounds from surfaces.⁹ Therefore, the next step to understanding the ecological function of sticky semi-volatiles is to test how temperature affects the volatility of the adsorbed semi-volatiles and how the patterns of semi-volatiles staying adsorbed or volatilizing into the surrounding air correspond to the activity of herbivores.

Figure 1.

Relative proportion (mean, % of total emission) of sesquiterpenoids (SQT), R. tomentosum-specific ledol, palustrol and ledene and other terpenoids from volatile profiles of control and R. tomentosum-neighboring birches. (A–D) Emissions of B. pendula grown in con-specific association (A: 10 min after removing the plants from the treatments and B: 4 h post-exposure) and R. tomentosum mixed association (C: 10 min post-exposure and D: 4 h post-exposure). n = 12. E and F: Emissions of B. pubescens growing in a natural habitat, with R. tomentosum growing at E: >5 m and F: <0.5 m distance. n = 6.

In herbivore assays, two species out of five tested were shown to be either repelled by R. tomentosum volatiles or found in lower incidence on R. tomentosum-exposed birches.⁸ Thus, wider screens to test the effectiveness of R. tomentosum specific semi-volatiles against various insects and also important agricultural pests, would help reveal their exploitation potential e.g., for pest control in organic farming.¹⁰ A recent meta-analysis¹¹ on factors leading to differences in insect responses towards volatiles (e.g., attraction versus repellence) revealed that factors including the sex, feeding guild, taxonomic group and diet breadth of insects can be used to explain patterns of behavior. Furthermore, the complexity of volatile blend, habitat type and other mixing factors may complicate the actual effect. This makes it even more challenging to investigate whether associational resistance¹² by volatiles is an ecologically meaningful interaction in natural environments.¹³

Associational resistance through volatiles would firstly require a significant effect on a particular pest herbivore (and its herbivorous growth stage), the presence of the emitter and receiver at the same habitat and some degree of persistence of the repellent volatiles on receiver foliage. The mechanism of resistance could take several routes (see Table 1 for a summary), which could include an active repellence of herbivores, or an ‘odorous disguise’ preventing herbivores from recognizing host plants. In an agricultural environment (i.e., field), this might be utilized for organic pest control, if found to be functional towards certain key pest species. However, the presence of such an interaction in nature is ecologically and even evolutionarily more interesting. Our results from birch—R. tomentosum suggest this possibility, but further study on the ecological fitness (e.g., reproduction) consequences over a longer time period are needed.

Table 1.

Possible roles for semi-volatiles to affect the herbivore resistance of neighboring, semi-volatile adsorbing species

Effects of neighbor-emitted semi-volatiles	Consequences for the adsorbing plant species
Towards herbivores:
Direct attraction (associational susceptibility)	−
Direct deterrence (associational resistance)	+
Masking of herbivore-attracting volatiles	+
Activation of defences in the adsorbing plant	−/+ Cost for “false” defence activation, but better herbivore resistance
No effect	0
Towards natural enemies of herbivores:
Direct attraction	+
Direct deterrence	−
Interference of tritrophic signalling by masking of herbivore-induced volatiles	−
Increased attraction through induction of adsorbing plant volatile emission	−/+ Cost for “false” defence activation, but better herbivore resistance
No effect	0

+, denotes a beneficial effect; −, a detrimental effect and 0 no effect for the adsorbing species.

Anyhow, our study opens new perspectives for studying the role of sticky semi-volatiles for community ecology plus associational resistance and susceptibility¹² in both agroecosystems and natural landscapes. Indeed, an understanding of adsorbed semi-volatiles might be necessary for us to fully understand species distribution and community level dynamics. With many unknowns still surrounding the research field of between-plant¹⁴ and within-plant¹⁵ signaling via volatile compounds, particularly with respect to the mechanisms involved, the potential for semi-volatile compounds to also have active functions is worth consideration. Further studies should target both the possible role of semi-volatiles in activating chemical defense in perceiving species and interference of multitrophic signaling (attraction of herbivore's natural enemies) (Table 1).

We conclude that plants emitting distinctive persistent semi-volatiles can alter the volatile profile of their neighboring heterospecifics in natural environments. Similarly, as air-mediated volatile signals may induce defense responses in neighbors,¹⁴ the possibility for passive adsorption of protective neighbor volatiles needs to be included when studying ecology of plant volatiles in natural environments.

Addendum to: Himanen SJ, Blande JD, Klemola T, Pulkkinen J, Heijari J, Holopainen JK. Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighboring plants—a mechanism for associational herbivore resistance? New Phytol. 2010;186:722–732. doi: 10.1111/j.1469-8137.2010.03220.