James D. Blande

From Plants to Birds: Higher Avian Predation Rates in Trees Responding to Insect Herbivory

Background An understanding of the evolution of potential signals from plants to the predators of their herbivores may provide exciting examples of co-evolution among multiple trophic levels. Understanding the mechanism behind the attraction of predators to plants is crucial to conclusions about co-evolution. For example, insectivorous birds are attracted to herbivore-damaged trees without seeing the herbivores or the defoliated parts, but it is not known whether birds use cues from herbivore-damaged plants with a specific adaptation of plants for this purpose. Methodology We examined whether signals from damaged trees attract avian predators in the wild and whether birds could use volatile organic compound (VOC) emissions or net photosynthesis of leaves as cues to detect herbivore-rich trees. We conducted a field experiment with mountain birches (Betula pubescens ssp. czerepanovii), their main herbivore (Epirrita autumnata) and insectivorous birds. Half of the trees had herbivore larvae defoliating trees hidden inside branch bags and half had empty bags as controls. We measured predation rate of birds towards artificial larvae on tree branches, and VOC emissions and net photosynthesis of leaves. Principal Findings and Significance The predation rate was higher in the herbivore trees than in the control trees. This confirms that birds use cues from trees to locate insect-rich trees in the wild. The herbivore trees had decreased photosynthesis and elevated emissions of many VOCs, which suggests that birds could use either one, or both, as cues. There was, however, large variation in how the VOC emission correlated with predation rate. Emissions of (E)-DMNT [(E)-4,8-dimethyl-1,3,7-nonatriene], β-ocimene and linalool were positively correlated with predation rate, while those of highly inducible green leaf volatiles were not. These three VOCs are also involved in the attraction of insect parasitoids and predatory mites to herbivore-damaged plants, which suggests that plants may not have specific adaptations to signal only to birds.

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 plants 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.

Plant volatile organic compounds (VOCs) in ozone (O3) polluted atmospheres: the ecological effects.

Tropospheric ozone (O3) is an important secondary air pollutant formed as a result of photochemical reactions between primary pollutants, such as nitrogen oxides (NOx), and volatile organic compounds (VOCs). O3 concentrations in the lower atmosphere (troposphere) are predicted to continue increasing as a result of anthropogenic activity, which will impact strongly on wild and cultivated plants. O3 affects photosynthesis and induces the development of visible foliar injuries, which are the result of genetically controlled programmed cell death. It also activates many plant defense responses, including the emission of phytogenic VOCs. Plant emitted VOCs play a role in many eco-physiological functions. Besides protecting the plant from abiotic stresses (high temperatures and oxidative stress) and biotic stressors (competing plants, micro- and macroorganisms), they drive multitrophic interactions between plants, herbivores and their natural enemies e.g., predators and parasitoids as well as interactions between plants (plant-to-plant communication). In addition, VOCs have an important role in atmospheric chemistry. They are O3 precursors, but at the same time are readily oxidized by O3, thus resulting in a series of new compounds that include secondary organic aerosols (SOAs). Here, we review the effects of O3 on plants and their VOC emissions. We also review the state of current knowledge on the effects of ozone on ecological interactions based on VOC signaling, and propose further research directions.

A Comparison of Semiochemically Mediated Interactions Involving Specialist and Generalist Brassica -feeding Aphids and the Braconid Parasitoid Diaeretiella rapae

Diaeretiella rapae, a parasitoid that predominately specializes in the parasitism of Brassica-feeding aphids, attacks Lipaphis erysimi, a specialist feeding aphid of the Brassicaceae and other families in the Capparales, at a greater rate than the generalist-feeding aphid, Myzus persicae. In this study, we investigated the orientation behavior of D. rapae to the volatile chemicals produced when these two aphid species feed on turnip (Brassica rapa var rapifera). We showed no significant preference orientation behavior to either aphid/turnip complex over the other. Isothiocyanates are among the compounds emitted by plants of the Brassicaceae in response to insect feeding damage, including by aphids. We assessed parasitoid orientation behavior in response to laboratory-formulated isothiocyanates. We tested two formulations and discovered significant orientation toward 3-butenyl isothiocyanate. We also assessed plant and aphid glucosinolate content, and showed large levels of glucosinolate concentration in L. erysimi, whereas there was little change in plant content in response to aphid feeding. Our results suggest that during the process of host location, similar cues may be utilized for locating L. erysimi and M. persicae, whereas the acceptance of hosts and their suitability may involve aspects of nonvolatile aphid chemistry.

Real-time monitoring of herbivore induced volatile emissions in the field.

When plants are damaged by herbivorous insects they emit a blend of volatile organic compounds (VOCs) which include a range or terpenoids and green leaf volatiles (GLVs) formed via different metabolic pathways. The precise timing of these emissions upon the onset of herbivore feeding has not been fully elucidated, and the information that is available has been mainly obtained through laboratory based studies. We investigated emissions of VOCs from Populus tremula L. xP. tremuloides Michx. during the first 20 h of feeding by Epirrita autumnata (autumnal moth) larvae in a field site. The study was conducted using Proton Transfer Reaction-Mass Spectrometry (PTR-MS) to measure emissions online, with samples collected for subsequent analysis by complementary gas chromatography-mass spectrometry for purposes of compound identification. GLV emission peaks occurred sporadically from the outset, indicating herbivore activity, while terpene emissions were induced within 16 h. We present data detailing the patterns of monoterpene (MT), GLV and sesquiterpene (SQT) emissions during the early stages of herbivore feeding showing diurnal MT and SQT emission that is correlated more with temperature than light. Peculiarities in the timing of SQT emissions prompted us to conduct a thorough characterization of the equipment used to collect VOCs and thus corroborate the accuracy of results. A laboratory based analysis of the throughput of known GLV, MT and SQT standards at different temperatures was made with PTR-MS. Enclosure temperatures of 12, 20 and 25 degrees C had little influence on the response time for dynamic measurements of a GLV or MT. However, there was a clear effect on SQT measurements. Elucidation of emission patterns in real-time is dependent upon the dynamics of cuvettes at different temperatures.

Air pollution impedes plant‐to‐plant communication by volatiles

Volatile organic compounds (VOCs) emitted by damaged plants convey information to undamaged neighbouring plants, and previous research has shown that these signals are effective over short distances in nature. Many herbivore-induced VOCs react with ozone, which is the most important tropospheric air pollutant in rural areas. We used extrafloral nectar (EFN) secretion as a phenotypic indicator of between-plant communication in Phaseolus lunatus L. (Lima bean) and show that an ozone-rich (80 ppb) atmosphere reduces the distance over which signalling occurs. We found that ozone degrades several herbivore-induced VOCs, a likely mechanism reducing communication distances. Direct exposure to 80-ppb ozone did not affect the VOC emissions from P. lunatus. In addition, we demonstrated that high ozone concentrations, 120 and 160 ppb, induced EFN secretion in exposed plants, whereas more moderate concentrations, 80 and 100 ppb, did not. This suggests that ozone can play a complex role in the indirect defence of P. lunatus.

Plant volatiles in polluted atmospheres: stress responses and signal degradation

Plants emit a plethora of volatile organic compounds, which provide detailed information on the physiological condition of emitters. Volatiles induced by herbivore feeding are among the best studied plant responses to stress and may constitute an informative message to the surrounding community and further function in plant defence processes. However, under natural conditions, plants are potentially exposed to multiple concurrent stresses with complex effects on the volatile emissions. Atmospheric pollutants are an important facet of the abiotic environment and can impinge on a plants volatile-mediated defences in multiple ways at multiple temporal scales. They can exert changes in volatile emissions through oxidative stress, as is the case with ozone pollution. The pollutants, in particular, ozone, nitrogen oxides and hydroxyl radicals, also react with volatiles in the atmosphere. These reactions result in volatile breakdown products, which may themselves be perceived by community members as informative signals. In this review, we demonstrate the complex interplay among stresses, emitted signals, and modification in signal strength and composition by the atmosphere, collectively determining the responses of the biotic community to elicited signals.

Molecular Plant Volatile Communication

Plants produce a wide array of volatile organic compounds (VOCs) which have multiple functions as internal plant hormones (e.g., ethylene, methyl jasmonate and methyl salicylate), in communication with conspecific and heterospecific plants and in communication with organisms of second (herbivores and pollinators) and third (enemies of herbivores) trophic levels. Species specific VOCs normally repel polyphagous herbivores and those specialised on other plant species, but may attract specialist herbivores and their natural enemies, which use VOCs as host location cues. Attraction of predators and parasitoids by VOCs is considered an evolved indirect defence, whereby plants are able to indirectly reduce biotic stress caused by damaging herbivores. In this chapter we review these interactions where VOCs are known to play a crucial role. We then discuss the importance of volatile communication in self and nonself detection. VOCs are suggested to appear in soil ecosystems where distinction of own roots from neighbours roots is essential to optimise root growth, but limited evidence of above-ground plant self-recognition is available.

Where do herbivore-induced plant volatiles go?

Herbivore induced plant volatiles (HIPVs) are specific volatile organic compounds (VOC) that a plant produces in response to herbivory. Some HIPVs are only produced after damage, while others are also produced by intact plants, but in lower quantities. Among the known functions of HIPVs are within plant volatile signaling to activate systemic plant defenses, the priming and activation of defenses in neighboring plants and the attraction of natural enemies of herbivores. When released into the atmosphere a plants control over the produced compounds ends. However, many of the HIPVs are highly reactive with atmospheric oxidants and their atmospheric life times could be relatively short, often only a few minutes. We summarise the potential ecological and atmospheric processes that involve the reaction products of HIPVs in their gaseous, liquid and solid secondary organic aerosol (SOA) forms, both in the atmosphere and after deposition on plant surfaces. A potential negative feedback loop, based on the reactions forming SOA from HIPVs and the associated stimulation of sun screening cloud formation is presented. This hypothesis is based on recent field surveys in the geographical areas facing the greatest degree of global warming and insect outbreaks. Furthermore, we discuss how these processes could benefit the individual plant or conspecifics that originally released the HIPVs into the atmosphere. Further ecological studies should aim to elucidate the possible reasons for biosynthesis of short-lived volatile compounds to have evolved as a response to external biotic damage to plants.

Foliar methyl salicylate emissions indicate prolonged aphid infestation on silver birch and black alder.

It is well documented that when plants are damaged by insects they respond by emitting a range of volatile organic compounds (VOCs). While there have been numerous reports concerning VOCs induced by chewing herbivores, there are relatively few studies detailing the VOCs induced by aphid feeding. The effects of aphid feeding on VOCs emitted by boreal forest trees have been particularly neglected. Herbivore-induced VOCs have relevance to direct and indirect plant defence and atmospheric chemistry. In this study, we analysed the VOCs emitted by Betula pendula (Roth) and Alnus glutinosa (L.) (Gaertn.) infested by specialist aphid species under laboratory conditions. We also complemented this by collecting VOCs from leaf beetle-damaged saplings under field conditions. In addition to induction of some inducible terpenes, we detected substantial aphid-induced emissions of methyl salicylate (MeSA) in both B. pendula and A. glutinosa. MeSA emission intensity depended on the length of aphid infestation. Feeding by beetles induced emission of (E)-DMNT in both tree species and (E)-beta-ocimene in A. glutinosa but had no effect on MeSA emissions. MeSA has been shown to have aphid-repellent qualities and has been shown recently to have impact on formation of secondary organic aerosols in the atmosphere. We discuss our results in relation to these two phenomena.