Utilizing associational resistance for biocontrol: impacted by temperature, supported by indirect defence.

BACKGROUND: Associational herbivore resistance is potentiated by neighbouring heterogenic plant species that impact a focal plant's attraction to herbivores or the damage that they cause. One mechanism to confer associational resistance is believed to be exposure to neighbour-emitted volatiles, the receivers of which range from intra- and interspecific neighbour plants to higher-trophic-level insects. In previous studies the passive adsorption of neighbour-emitted semivolatiles has been reported, but little is known regarding the mechanisms and ecological consequences on the receiver plant and its associated biota. To utilize volatile-based associational resistance for agricultural applications, it is imperative to know its effectiveness under varying diurnal temperatures and whether herbivore natural enemies, providing biological control, are impacted. Mimicking varying diurnal temperatures in a laboratory set-up, we assessed how the tritrophic model system Brassica oleracea var. italica (broccoli)-Plutella xylostella (crucifer specialist herbivore)-Cotesia vestalis (endoparasitoid of P. xylostella) is influenced by exposure to the natural semivolatile emitter plant Rhododendron tomentosum Harmaja. RESULTS: Rhododendron tomentosum-exposed B. oleracea was less susceptible to P. xylostella oviposition at both night-time (12°C) and day-time (22°C) temperatures and less favoured and damaged by P. xylostella larvae at 12°C. Exposure did not interfere with indirect defence, i.e. attraction of the natural enemy C. vestalis on host-damaged, R. tomentosum-exposed B. oleracea under 22°C, while there was a reduction in attraction (marginal preference towards host-damaged B. oleracea) under 12°C. CONCLUSIONS: The ability of R. tomentosum exposure to render associational resistance against an agriculturally important Brassica herbivore P. xylostella without severely compromising the specialist parasitoid C. vestalis host location encourages further studies on the potential of using this naturally abundant plant for biocontrol. The generality of our finding on temperature as a potential regulating mechanism for the efficacy of semivolatile emitter-based associational resistance towards specialist pest larval damage should be further studied in natural and agricultural associations. Our study emphasizes the need to develop techniques to compare volatiles at the leaf versus air interface and associate their appearance and ecological role with times of activity and level of specialisation of herbivores and their natural enemies.

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

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 favour or disfavour 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 defence: 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 sp.) 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.

Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants--a mechanism for associational herbivore resistance?

Plant-emitted semi-volatile compounds have low vaporization rates at 20-25 degrees C and may therefore persist on surfaces such as plant foliage. The passive adsorption of arthropod-repellent semi-volatiles to neighbouring foliage could convey associational resistance, whereby a plant's neighbours reduce damage caused by herbivores. We found that birch (Betula spp.) leaves adsorb and re-release the specific arthropod-repelling C(15) semi-volatiles ledene, ledol and palustrol produced by Rhododendron tomentosum when grown in mixed association in a field setup. In a natural habitat, a higher concentration of ledene was released from birches neighbouring R. tomentosum than from birches situated > 5 m from R. tomentosum. Emission of alpha-humulene, a sesquiterpene synthesized by both Betula pendula and R. tomentosum, was also increased in R. tomentosum-neighbouring B. pendula. In assessments for associational resistance, we found that the polyphagous green leaf weevils (Polydrusus flavipes) and autumnal moth (Epirrita autumnata) larvae both preferred B. pendula to R. tomentosum. P. flavipes also preferred birch leaves not exposed to R. tomentosum to leaves from mixed associations. In the field, a reduction in Euceraphis betulae aphid density occurred in mixed associations. Our results suggest that plant/tree species may be protected by semi-volatile compounds emitted by a more herbivore-resistant heterospecific neighbour.

Smelling global climate change: mitigation of function for plant volatile organic compounds.

Plant volatile organic compounds (VOCs) have important roles in plant adaptation to the environment and serve as infochemicals in multitrophic interactions. Global climate change factors, such as increased atmospheric carbon dioxide, ozone and temperature, could alter how insects perceive such compounds. Here we review recent research on the influence of climate change parameters on the ecological functions of VOCs, with specific focus on terpenoids, the best-characterized VOCs. We summarize how emission patterns and concentrations of VOCs could change in future environments, mainly from the perspectives of plant defense and stress responses. We discuss how higher carbon dioxide concentrations, elevated ozone levels and increased temperatures could affect the biological functions of VOCs, particularly their role in plant defense.

Elevated atmospheric ozone increases concentration of insecticidal Bacillus thuringiensis (Bt) Cry1Ac protein in Bt Brassica napus and reduces feeding of a Bt target herbivore on the non-transgenic parent.

Sustained cultivation of Bacillus thuringiensis (Bt) transgenic crops requires stable transgene expression under variable abiotic conditions. We studied the interactions of Bt toxin production and chronic ozone exposure in Bt cry1Ac-transgenic oilseed rape and found that the insect resistance trait is robust under ozone elevations. Bt Cry1Ac concentrations were higher in the leaves of Bt oilseed rape grown under elevated ozone compared to control treatment, measured either per leaf fresh weight or per total soluble protein of leaves. The mean relative growth rate of a Bt target herbivore, Plutella xylostella L. larvae was negative on Bt plants in all ozone treatments. On the non-transgenic plants, larval feeding damage was reduced under elevated ozone. Our results indicate the need for monitoring fluctuations in Bt toxin concentrations to reveal the potential of ozone exposure for altering dosing of Bt proteins to target and non-target herbivores in field environments experiencing increasing ozone pollution.

Effects of elevated carbon dioxide and ozone on volatile terpenoid emissions and multitrophic communication of transgenic insecticidal oilseed rape (Brassica napus).

Does transgenically incorporated insect resistance affect constitutive and herbivore-inducible terpenoid emissions and multitrophic communication under elevated atmospheric CO(2) or ozone (O(3))? This study aimed to clarify the possible interactions between allocation to direct defences (Bacillus thuringiensis (Bt) toxin production) and that to endogenous indirect defences under future climatic conditions. Terpenoid emissions were measured from vegetative-stage non-Bt and Bt Brassica napus grown in growth chambers under control or doubled CO(2), and control (filtered air) or 100 ppb O(3). The olfactometric orientation of Cotesia vestalis, an endoparasitoid of the herbivorous diamondback moth (Plutella xylostella), was assessed under the corresponding CO(2) and O(3) concentrations. The response of terpenoid emission to CO(2) or O(3) elevations was equivalent for Bt and non-Bt plants, but lower target herbivory reduced herbivore-inducible emissions from Bt plants. Elevated CO(2) increased emissions of most terpenoids, whereas O(3) reduced total terpenoid emissions. Cotesia vestalis orientated to host-damaged plants independent of plant type or CO(2) concentration. Under elevated O(3), host-damaged non-Bt plants attracted 75% of the parasitoids, but only 36.8% of parasitoids orientated to host-damaged Bt plants. Elevated O(3) has the potential to perturb specialized food-web communication in Bt crops.

Constitutive and herbivore-inducible glucosinolate concentrations in oilseed rape (Brassica napus) leaves are not affected by Bt Cry1Ac insertion but change under elevated atmospheric CO2 and O3.

Glucosinolates are plant secondary compounds involved in direct chemical defence by cruciferous plants against herbivores. The glucosinolate profile can be affected by abiotic and biotic environmental stimuli. We studied changes in glucosinolate patterns in leaves of non-transgenic oilseed rape (Brassica napus ssp. oleifera) under elevated atmospheric CO2 or ozone (O3) concentrations and compared them with those from transgenic for herbivore-resistance (Bacillus thuringiensis Cry1Ac endotoxin), to assess herbivory dynamics. Both elevated CO2 and O3 levels decreased indolic glucosinolate concentrations in transgenic and non-transgenic lines, whereas O3 specifically increased the concentration of an aromatic glucosinolate, 2-phenylethylglucosinolate. The herbivore-inducible indolic glucosinolate response was reduced in elevated O3 whereas elevated CO2 altered the induction dynamics of indolic and aliphatic glucosinolates. Herbivore-resistant Bt plants experienced minimal leaf damage after target herbivore Plutella xylostella feeding, but exhibited comparatively similar increase in glucosinolate concentrations after herbivory as non-transgenic plants, indicating that the endogenous glucosinolate defence was not severely compromised by transgenic modifications. The observed differences in constitutive and inducible glucosinolate concentrations of oilseed rape under elevated atmospheric CO2 and O3 might have implications for plant-herbivore interactions in Brassica crop-ecosystems in future climate scenarios.