BVOCs and global change

BVOCs and global change

Review Special Issue: Induced biogenic volatile organic compounds from plants BVOCs and global change Josep Pen˜uelas1 and Michael Staudt2 1 Global...

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Review

Special Issue: Induced biogenic volatile organic compounds from plants

BVOCs and global change Josep Pen˜uelas1 and Michael Staudt2 1

Global Ecology Unit CSIC-CEAB-CREAF, CREAF (Centre de Recerca Ecologica i Aplicacions Forestals), Universitat Autonoma de Barcelona, 08193 Bellaterra, Barcelona, Spain 2 Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, 1919 Route de Mende, 34293 Montpellier cedex 5, France

Biogenic volatile organic compounds (BVOCs) produced by plants are involved in plant growth, reproduction and defense. They are emitted from vegetation into the atmosphere and have significant effects on other organisms and on atmospheric chemistry and physics. Here, we review current knowledge on the alteration of BVOC emission rates due to climate and global changes: warming, drought, land use changes, high atmospheric CO2 concentrations, ozone and enhanced UV radiation. These alterations are very variable depending on the doses, timing, BVOC and species, but in overall terms are likely to increase BVOC emissions. These changed emissions can lead to unforeseeable consequences for the biosphere structure and functioning, and can disturb biosphere feedback on atmospheric chemistry and climate with a direction and intensity that warrants indepth investigation. BVOC emissions: why do they matter in research into global change? It is now widely acknowledged that biological processes in terrestrial ecosystems broadly affect the atmosphere and climate system of Earth, which consequently implies potentially significant feedback effects on current global changes in atmosphere and climate arising from human activities [1]. Of these biological processes, those related to the carbon cycle (i.e. the assimilation and release of CO2 and the carbon sequestration in organic material) have been the focus of much attention [2,3]. However, gases other than CO2 are exchanged between the biosphere and the atmosphere. Vegetation covering the landmasses releases biogenic volatile organic compounds (BVOCs), that comprise a large variety of molecules that differ in size and physicochemical properties as well as in their metabolic origin [4,5]. The emission rates of BVOCs are determined by their synthesis rates and by their physicochemical characteristics, mainly their solubility, volatility and diffusivity. Their emission rates are therefore heavily modulated by internal and external factors [4,6–8]. There is a broader range of production capacity for BVOCs than for photosynthetic carbon assimilation between plant species. As a result, changes in species and community structure of ecosystems, land uses, climate and resource availability can lead to major changes in regional BVOC fluxes, even if the standing biomass and net primary productivity remain unchanged. The functions of these emissions in plant metabolism, growth, reproduction, protection, defense and communiCorresponding author: Pen˜uelas, J. ([email protected]).

cation will evidently be altered by the changes arising from global and climate changes, and as a result of these alterations, the structure and the functioning of organisms, communities and ecosystems might therefore change significantly. Moreover, once emitted into the atmosphere, BVOC molecules gradually split and ultimately oxidize to CO2 unless intermediate products condense and/or deposit on particles and surfaces [9]. Although the CO2 deriving from BVOCs oxidation can also represent a non-negligible fraction of the ecosystem carbon budgets [10,11], it is the chemical degradation of these trace gases and the various resulting intermediate products that are most relevant to air quality and climate. Understanding how trace gas fluxes from terrestrial vegetation directly or indirectly respond to anthropogenic global changes in the physicochemical properties of the atmosphere and the pedosphere is therefore crucial for predicting BVOC-mediated positive or negative feedback loops in the biosphere–atmosphere–climate system and developing effective strategies to mitigate threats of global change [7,12–14]. However, despite the many studies assessing the impact of global warming, drought and high atmospheric CO2 concentrations on CO2 exchange and carbon budgets at various scales, less attention has been devoted to understanding how the strengths of BVOC sources are altered under these conditions [5,7,14–16], and much less to the resulting alterations in BVOC-mediated physiological, ecological, chemical and climatic processes. The first aim of this paper is to review current understanding of the direct and indirect effects of environmental factors associated with global and climate change on BVOC emissions. We analyze the emissions of the following BVOC classes: isoprene, 2-methyl-3-buten-2-ol, monoterpenes, sesquiterpenes, green leaf volatiles (GLVs, i.e. C6 oxylipins and derivatives), herbivore-induced volatiles (HIVs, e.g. many sesquiterpenes or methyl salicylate) and oxygenated VOC (OVOC) including various carbonyls, alcohols and acids. The second aim is to discuss the possible alterations in the physiology of organisms, in the ecological interactions between organisms, and finally in atmospheric chemistry and climate arising from global change-altered BVOC emissions. BVOC emissions in a changing world: an increasingly fragrant world? Effects of climate change: warming and drought The average global temperature increased by 0.76 8C during the twentieth century, and a further increase of

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Review 1.8–4.0 8C is projected during the twenty-first century [17]. The effects of temperature on BVOCs release from vegetation range from direct effects on biochemical reactions in the BVOCs producing metabolic pathways to indirect effects such as the lengthening of the growing season. We know that, in the short term at least, a rise in temperature exponentially increases the emission rates of most BVOCs [18,19]. It does so not only by enhancing the enzymatic activities of synthesis but also by raising the BVOCs vapor pressure and by decreasing the resistance of the diffusion pathway [20]. BVOC emissions are thus expected to increase sharply as global temperatures rise. By applying the most frequently used algorithms of emission response to temperature [18], it can be estimated that climate warming over the past 30 years [17] could have already increased BVOC global emissions by 10%. A further 2–3 8C rise in the mean global temperature, which is predicted to occur early this century [17], could increase BVOC global emissions by an additional 30–45% [7]. Furthermore, global warming in boreal and temperate environments not only means warmer average and warmer winter temperatures but also implies an extended plant activity season [21], increasing total annual emissions even further. However, more recent studies have shown that the capacity for isoprenoid emissions is also related to slower day-to-day changes in mean temperature, probably involving changes in the expression level of isoprenoid synthases, and not only their catalytic potential [22–25]. In the most recent global emission model [26], an effort was made to modify the instantaneous algorithm to allow for some short-term acclimation of the key temperature-sensitive coefficients. Other results suggest that previous regional model inventories based on one fixed emission factor probably overestimate regional emissions, and

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species-specific expressions of seasonality in temperature response can be necessary [27,28]. Further studies of medium- to long-term responses of BVOC emission to warming are therefore warranted to complement and extend the few available studies which, as expected, show mostly increased emissions (Box 1, references in Table S1 in the supplementary material online). Furthermore, many investigations have been conducted in the laboratory, and we still do not know much about the emissions of BVOCs in response to warming in the field. We also know very little about some regions of our planet, such as the Arctic, which are likely to experience the most pronounced effects of climatic warming. Recent studies have measured emissions of isoprene, the reactive BVOC from vegetation with the highest emission levels, on a subarctic heath experimentally subjected to a 3–4 8C air temperature enhancement [29]. These studies have measured increased emissions ranging between 56% and 83%, depending on the year. Their results confirm the increased emission percentages anticipated using the standard algorithms of Guenther et al. [18]. However, other field studies in Mediterranean shrublands have not found clear or general responses to a warming of around 1 8C [30,31]. It is possible that the likely positive response to temperature was limited to the cold biomes such as the Arctic ecosystem [29], and that the positive effects might thus not be expressed at more southerly Mediterranean latitudes which are more waterlimited than energy-limited. In fact, there have been few studies in the warmer regions, and only variable and complex species-specific and compound-specific responses to long-term 1 8C warming have been reported [13,30,31]. Further fieldwork is thus clearly warranted. Warming does not only have the abovementioned direct effects on BVOC emissions. It has numerous indirect

Box 1. Global change effects on BVOC emissions Figure I shows the number of published results (based on Table S1 in the supplementary material online) reporting emission increases, emission decreases and no emission change in response to the main drivers of global and climate change. Such literature compilation raises three major points that should be taken into consideration for future programs of BVOC research: (i) there is a much lower number of studies available on induced BVOCs (HIVs and GLVs) and OVOCs than on constitutive isoprenoids, notably for the effects of drought and warming (Figure Ia). (ii) Among the global change components, the long-term effects of eutrophication, warming and UV-B have not been the focus of much attention in the past, in part because of methodological and/or technical constraints, whereas the effects of drought as well as the short-term responses to temperature (Figure Ib) have been studied many times on many plant species. (iii) Even within most of the better studied categories, the published data show apparent contrasting responses suggesting either that global effects on emissions from vegetation are highly uncertain or unpredictable (for instance because effects are highly species specific) and/or that considerable divergences and limitations in applied methods and experimental approaches exist. However, when putting the data under scrutiny, the apparent contrasting effects of some factors are less so. This is the case of drought responses that can largely be attributed to a dosedependent response; severe drought generally decreases emissions, whereas mild drought has no effect or even increases emissions. Similarly, the contrasting results within the literature reporting effects of elevated CO2, ozone and eutrophication on constitutive isoprenoid emissions can result from different groups of BVOCs (e.g.

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isoprene and monoterpenes) presenting different responses (Figure Ic). For example, studies reporting negative effects of ozone are more frequent for isoprene emissions than for monoterpene emissions, for which mostly positive or no effects are reported. A similar trend can be seen for elevated CO2 and an opposite one for eutrophication. Monoterpene emission studies reporting divergent results with regard to isoprene emissions were often, although not always, made on conifers or aromatic plants (Table S1 in the supplementary material online) that store terpenes in specialized glandular organs. These terpene storage pools have different metabolic controls than isoprene and also have different functions. This suggests that results from isoprene emission studies cannot easily be extrapolated to the emissions of other constitutive BVOCs. Concerning ozone effects, there is a clear tendency of BVOC emissions to increase under future higher ozone levels, but this is most evident for OVOC emissions, HIV and GLV emissions (Figure Ia) and constitutive monoterpene and sesquiterpene emissions (no study reporting emission decreases), than for isoprene which has shown both positive and negative effects (Figure Ic). As for drought, the contrasting results of ozone on isoprene emissions are partly associated with differences in the ozone dose exposures and genotypic differences in the ozone tolerance of the tested plant material. Interactions play an important role too. For example, ozone effects also depend on other global change components, as for instance drought, that by inducing reductions in stomatal conductance and consequently in ozone uptake reduces the ozone-induced GLV emissions [127]. Many other ozone interactions can exist, for example with elevated CO 2 [13,73,117].

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Figure I. Number of published results (based on Table S1 in the supplementary material online) reporting emission increases, emission decreases and no emission change in response to the main drivers of global and climate change for different BVOC classes. (a) and (b) Isoprenoids (i.e. constitutive isoprene, 2-methyl-3-butenol, monoterpenes and sesquiterpenes); HIVs and GLVs (i.e. herbivore-induced volatiles and green leaf volatiles); OVOCs (i.e. short-chained oxygenated BVOCs). (c) Constitutive isoprenoids are separated into monoterpenes and sesquiterpenes (MTs and STs) and isoprene and 2-methyl-3-butenol (Iso and MBO). The number to the right of each bar indicates the total number of published results. In (a) only results from studies investigating long-term effects of warming and elevated CO2 on BVOC emissions were considered. Incorporating studies on short-term effects increases the number of available results particularly for temperature effects on emissions of constitutive isoprenoids (b).

effects. One of these is the lengthening of the growing season also mentioned above [21], and another indirect effect is the consequent change in land cover. For example, in environments where winter temperatures reach freezing, an increase in the minimum winter temperature of 5 8C would be expected to increase the number of species able to grow there by 7–20% [32]. Indeed, as a consequence of the warming in recent decades, migrations of the tree-

line northward and upslope and an increasing abundance of deciduous woody shrubs in arctic vegetation communities have already occurred [33–35]. Another example of further indirect effects is vegetation changes leading to more leaf litter on the ground [36]. This brings extra nutrients to the soil [37], thus providing an additional resource factor for the likely increase of BVOCs. Indeed, increased isoprene emissions have been reported after 135

Review nutrient fertilization ([38] and section below), and as a result of the expected increased level of carbon fixation and enhanced activity of the enzymes responsible [39]. Climate models predict an increase in global mean precipitation, but some regions will become considerably drier [17]. In semiarid regions and Mediterranean type climates, accelerated soil water depletion in summer and reduced precipitation will increase drought and associated heat stress in summer [1,17]. These changes in water availability also affect BVOC emissions (Box 1, references in Table S1 in the supplementary material online). The decline in isoprenoid emissions in response to severe droughts, possibly affecting protein levels and substrate supplies [40], might largely offset the predicted impact of rising temperatures on the emission of isoprenoids in arid and semiarid terrestrial ecosystems suffering severe droughts more frequently. However, the effect of drought, like other stressors on plant BVOC emissions, can depend on the level of stress or damage caused to the plant by drought. Severe drought might largely decrease emissions [41], whereas mild drought stress might increase emis¨ . Niinemets in this issue). sions [42] (see review by U Effects of the other components of global change There are also many other global change components apart from those relating to climate, which can limit or promote constitutive and induced BVOC emissions. Of particular interest are land use changes, increased atmospheric CO2 concentrations, tropospheric ozone, nutrient availability and UV radiation. Some BVOCs such as wound-induced GLVs are ubiquitous, but for most constitutive BVOCs the genotype is an important determinant of their emissions. The inducible compounds involved in plant–insect and plant–plant interactions as infochemicals also depend on the plant species and genotype, but also on the type of insect inducer [43]. Because of this species-specificity, changes in land use and cover and the consequent shifts in species dominance can also dramatically affect BVOC emissions. For example, many plant species migrating to northern latitudes and higher altitudes are strong emitters of BVOCs such as isoprene and monoterpenes. This is true of most broad-leaved Populus and Quercus species and essentially all conifers (Ref. [32] and references therein) [44]. In other regions such as tropical areas, increasing areas of rainforest are replaced by plantations, such as of oil palm in Malaysia or of rubber tree in southern China, both of which are strong isoprenoid emitters [45,46]. These plantations not only emit up to 10 times more isoprenoids than natural forest, but some of their emitted compounds can respond more strongly to warming [46]. Other land changes might also greatly increase BVOC emissions, such as the abandonment of agricultural land in temperate regions, and subsequent aforestation with evergreens such as Eucalyptus, Quercus or Pinus, which are strong emitters of BVOCs throughout the year [44]. In the Southeast US, substantial effects of ecological succession, harvesting and plantation management on BOVC emission have been described [47]. Global warming increases the number of species that can grow in given temperate environments and leads to shifts in vegetation types. 136

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However, this is not the cause of the most rapid changes in species distribution. The fastest species movement is as a result of the profit-driven globalized trade in exotic plants and agricultural, forestry and gardening practices that alleviate dispersal limitations and biological and environmental constraints [32]. Rising atmospheric CO2 concentrations could increase the productivity and standing biomass of plants, at least in the short term (although see Ref. [48]), and hence indirectly also facilitate further production and emission of BVOCs. However, it is not entirely clear whether elevated CO2 per se increases the release of BVOCs [49]. The results for BVOC emissions in response to increasing atmospheric CO2 concentrations vary depending on the species and environmental and phenological conditions, but recent work indicates that increasing CO2 concentration might uncouple isoprene emission from photosynthesis (the carbon source for BVOCs) and inhibit isoprene emission at leaf level [50]. Decreases dominate the studies of elevated CO2 effects on isoprenoids, whereas increases dominate the few available studies on HIVs, OVOCs and GLVs (Box 1, Table S1 in the supplementary material online). Future projections applying a global coupled land–atmosphere model to explore the degree to which the inhibition of isoprene under elevated CO2 concentrations opposes the large increase in isoprene emissions due to future climate warming and in the presence of increased global net primary production suggest a compensatory balance between the effects of temperature and CO2 on isoprene emission [51]. Tropospheric ozone concentrations are also likely to increase in the coming decades, either in terms of higher background concentrations and/or frequency in air pollution events [17,52,53]. Both positive and negative effects of ozone on constitutive BVOC emission rates from plants have been reported depending on experimental conditions (temperature, applied ozone concentrations), species, type of BVOCs and seasons ([54], references in Table S1 in the supplementary material online). The problem is that emitted BVOCs readily react with ozone (inside leaves, chambers, BVOC cartridges, etc.) and therefore emission rates could be underestimated. In any case, reported results show an overall more increase than decrease (Box 1). To date, the effects of increasing N-deposition and the resulting global eutrophication on BVOC fluxes has received relatively little attention. Yet, eutrophication arising from human activities [55,56] has an important long-term impact on the functioning and the biodiversity of terrestrial plant communities and therefore cannot be ignored in global change research. As for isoprene and other constitutive BVOC emissions, the majority of studies report a positive effect of N-fertilization (or a positive correlation with foliar nitrogen), although this pattern is not universal [57] (Box 1, references in Table S1 in the supplementary material online). Enhanced UV-B radiation might substantially increase the emissions for the Arctic [58]. However, there have been very few studies on the effect of UV radiation on plant BVOC emissions (Box 1, references in Table S1 in the supplementary material online) and they might depend

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Figure 1. Overview of effects and possible interactions of global changes in climate and atmospheric composition on/with BVOC emissions, distinguishing between constitutive BVOCs such as isoprene (green) and stress-induced BVOCs (red). Experimental evidence suggests that many global environmental changes have direct effects on BVOC release at leaf level, either increasing (straight lines) or having a diverse effect (broken lines). Note, however, that many of the assumed effects are still tentative particularly over longer time scales. The effects can also be ‘‘dose dependent’’ (strong evidence for drought) and can vary widely between plant species and timing. Nevertheless, our current level of understanding is much better for constitutive BVOCs than for induced BVOC emissions. The possible feedback between changing BVOC fluxes and global environmental changes are depicted in brown. It is assumed that high concentrations of ozone and severe drought (as well as increased UV, actually not shown in the scheme) reduce foliar carbon gain and increase oxidative stress, whereas a higher nutrient availability (eutrophication), higher proportion of diffusive radiation (SOA) and elevated CO2 should increase carbon gain and reduce oxidative stress. The effects of global elevated temperatures on carbon gain and/or oxidative stress depend on the vegetation and/or ecosystem and season considered. There are other possible interactions not shown in the diagram. In addition to direct effects at leaf level, global changes in climate and atmospheric composition indirectly alter BVOC fluxes at an ecosystem level by changing species distribution and standing biomass (which might be even stronger than the direct effects). (+) indicates clear overall positive effects, (+–) indicates both positive and negative effects depending on the severity of the change, the species and/or BVOCs, and (–?) possible not fully demonstrated negative effects.

on plant and BVOC species, and also on the level of stress or damage caused by UV in the plant [59,60]. Therefore, there is still a lack of precise and complete data to answer the question what the effects of all these global change components will be on BVOC emissions. For example, whether or not BVOC emissions will acclimate to long-term warming is still open to question. Even less is known of the effect of many other components such as changing irradiance or air pollution that have been studied to a lesser extent than those reviewed here. Moreover, the complex interactions between each of these global change components and other biotic and abiotic factors introduce a large amount of variability into the responses to global environmental changes. There are countless examples of interactions: by way of an example, moderately elevated temperatures or elevated CO2 have been shown to enhance feeding by certain herbivores and this could in turn increase inducible BVOC emissions [61,62]. However, in spite of this variability, current knowledge seems to indicate that the most likely overall response will be an increase in BVOC emissions mostly driven by current warming [7] (Figure 1, Table S1 in the supplementary material online, Box 1, Figure I). The effects of such increases in both biological and environmental terms might be far-reaching and very intense [15].

Physiological and ecological alterations mediated by changes in BVOC emissions Although the emission of BVOCs can be an unavoidable result of their volatility, most of them have developed important physiological and ecological functions throughout evolution [63,64]. These functions are determined by tissue BVOC concentrations and the emission rates, and thus the changes generated by climate and global changes in their concentrations and emission rates will significantly alter such physiological and ecological functions (Figure 2). By having increased emissions, we will have a changed world with BVOCs gaining dominance as ecological and evolutionary factors [15]. Altered plant protection against abiotic stress Increasing production and emission of BVOCs might be largely beneficial for plants that are very likely to gain protection from abiotic stressors such as heat, air pollution, high irradiance, oxidative stress and mechanical wounding, which are predicted to be more severe in the near future [17], and the effects of which are mitigated by BVOCs [15,16,65–67] as discussed extensively by F. Loreto, and J.P. Schnitlzer in this issue. Let us consider the case for antioxidant protection as one example. Several studies suggest that plants constitutively emitting BVOCs are less damaged by ozone than their non-emitting 137

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Figure 2. Effects of increased BVOCs on plant physiology and ecology. Increased emissions of BVOCs as a likely result of global change (mostly warming) will generate physiological and ecological alterations in plant protection against stress (thermal and oxidative), plant defense against herbivores and pathogens (direct and indirect), plant–plant interaction (communication, allelopathy) and plant reproduction (pollination, fruit and seed dispersal) that warrant an in-depth research effort.

counterparts, possibly by scavenging ozone (or secondary formed reactive oxygen species) inside the leaves and/or outside, close to the surface of leaves [66,67]. Because both emission rates and ozone levels will probably increase in warmer climates, it has even been suggested that BVOCemitting plants might gain a selective advantage over nonemitting plants and gradually replace them in the future [68]. Furthermore, the resulting increase in the atmospheric BVOC load on terrestrial ecosystems would enhance the formation of tropospheric ozone and thus favor BVOC emitting plants even further. However, experimental results on the antioxidant function of BVOCs are still controversial [69]. Moreover, whether the increased production and emission of BVOCs will offer enough protection against the also increased oxidative and abiotic stress warrants further study. Altered plant defense against biotic stressors The increased emissions in response to warming and global change will also affect plant communication and relationships with other organisms. Their defensive role might be one of the most severely affected functions. Plants might gain in deterrence against pathogens or herbivores, in antimicrobial and antifungal defense, in allelopathic potential against neighbors or in attraction of both herbivore predators and parasitoids. Will all these defenses actually be enhanced? Will the signaling effect be more effective or will the organisms receiving the enhanced BVOC messages from plants be confused by the altered emissions? Some studies are starting to consider these questions. For example, the responses of multitrophic BVOCs signaling to climate change have been studied by examining 138

induced BVOC emissions over ranges of temperatures [61]. Not only will stress-induced BVOC emissions increase under warmer climates but so will the emissions of constitutive BVOCs such as isoprene (discussed above). This increasing chemical background noise level might affect biotic interactions mediated by other BVOCs [16,70]. Given the fact that the complexity of interactions such as those of multitrophic relationships with the blends of HIVs varies according to the plant and herbivore species, and the developmental stages and conditions of those species [71,72], the effects of increased temperature on communication can be strongly system-specific, making it difficult to develop general predictions. Higher O3 concentrations might also increase the induction of BVOC emissions, resembling the hypersensitive response to pathogen or herbivore attack [54,73]. The resulting increased BVOC concentrations in the stomatal cavity and in the leaf boundary layer [74] could enhance plant defenses against bacterial and fungal pathogens and herbivores. However, they could also disguise herbivore-induced BVOCs as cues and could also degrade certain BVOCs [75], thus disturbing herbivores, higher trophic level and plant–plant interactions [76]. However, some studies on the effects of O3 on tritrophic interactions have reported altered volatile emission patterns by O3 with no effect on the orientation of a predatory mite (Phytoseiulus persimilis) or parasitoid (Cotesia plutellae) [73,75]. It could be that natural enemies learn to exploit degraded BVOC products rather than the primary emitted BVOCs, or that long-distance signals between plants and predators or parasitoids could be provided by the more stable HIV compounds, such as MeSA, methanol and benzyl cyanide [75]. Again, more research is

Review needed in different ecosystems and experimental settings to examine the response of defensive functions (including tritrophic interactions) to this other global change component – increased O3 concentrations. As elevated CO2 has been reported as reducing constitutive isoprenoid emissions [77,78] (Box 1), although with several exceptions ([49], Box 1, Table S1 in the supplementary material online), there should be decreasing signaling effectiveness at higher trophic levels. However, this response is not general. For example, in the system consisting of cabbage, Brassica oleracea, the herbivore insect Plutella xylostella and the generalist predator Podisus maculiventris, as well as the specialist parasitoid Cotesia plutellae, elevated CO2 has been found to have minimal effects on terpenoid production and the minor BVOC decreases nevertheless led to both predator and parasitoid species failing to respond to the volatile signal [73]. However, in a similar laboratory study with young Brassica napus plants, elevated CO2 levels increased constitutive and herbivore-inducible terpenoid emissions but did not affect the olfactometric orientation of C. plutellae to P. xylostella damaged plants [62]. It is again clear that these laboratory studies also need to be conducted in the field (e.g. in FACE experiments) and in tritrophic systems to draw more clear conclusions on the effects of elevated CO2. Certainly, in these relationships, animals themselves also respond to the climate and global changes, complicating analyses of the possible alterations of the interactions even further. For example, insects (herbivores, predators and parasitoids) have higher metabolic activity at higher temperatures and might be more receptive to plant infochemicals but they also experience other abiotic stresses including ozone and elevated CO2-mediated reduction in plant quality [79,80] with unknown overall effects on the performance of insects. Altered plant–plant interaction Some BVOCs, such as terpenes, methyl jasmonate, methyl salicylate or GLVs, can act as airborne signals between plants [81] and between organs within the same plant [82]. Herbivore-induced BVOCs elicit a defensive response in undamaged plants and undamaged parts of the plant, thus playing a physiological role in the systemic response of a plant to local damage [82]. This communication [83] can occur between neighbors of the same or different species [84]. On perception by receiver plants, these BVOC signals can directly activate herbivore defense mechanisms or might prime a subset of defense-related genes for earlier and/or stronger induction on subsequent defense elicitation [85]. This plant– plant communication role of BVOCs and the plant–plant allelopathic role of certain BVOCs such as monoterpenes inhibiting the cytochromic pathway of respiration [85] or the growth and seed germination of neighboring plants [86] can also be increased with higher BVOC emissions in a warmer world. Volatile terpenoids in allelopathic root exudates affecting competing plant species could also be increased further by elevated CO2 [87]. In any case, as in the previous enhanced BVOC emission related issues, further studies are warranted.

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Altered plant reproduction Higher BVOC production and volatility at elevated temperatures might enhance plant–pollinator and plant–frugivore interactions. However, other components of global change, such as increased ozone, might also affect these interactions reducing the actual air BVOC concentrations. In fact, a decrease of maximum downwind distance of highly reactive floral scents has been reported, from kilometers during pre-industrial times to no more than 200 m under the current more polluted conditions [76]. This might lead to reduced searching and foraging efficiency of pollinators during ozone episodes. The effects of other global change drivers such as CO2 on floral BVOC production are largely unknown. As with herbivores, the pollinator responses will also depend on their traits. For example, it is very likely that the effects of interacting global change components will be different in moths and bees, as they have differing olfactory capacities, with moths typically using BVOC cues over longer distances and requiring higher emissions [88], whereas bees being able to distinguish between small differences in ratios of compounds [89]. As a result, the altered BVOC emissions will probably translate into changes in the competitive abilities between pollinators. These changes should be particularly evident among pollinators such as social bees which learn quickly to associate scent with the presence of nectar; their ability to do so is faster and more reliable than their ability to learn visual cues [90]. Environmental alterations mediated by changes in BVOC emissions Atmospheric chemistry: CO2, ozone, hydroxyl radicals, methane BVOC fluxes can account for up to 5–10% or even more of total net carbon exchange, particularly under stress conditions [7]. These BVOC emissions might therefore represent a small but significant plant carbon loss on an ecosystem basis and on a global basis. The average global BVOC emission for vegetated surfaces is 0.7 g carbon m–2 per year, but this could exceed 100 g m–2 per year in some tropical locations [10]. On a global scale, BVOCs are estimated to be emitted from vegetation at a rate of approximately 0.75–1.2  1015 g carbon per year [18,91] which is around 1–2% of the estimated global carbon assimilation by terrestrial ecosystems [92]. BVOC emissions might become an even more significant component in local and regional carbon budgets as they increase in response to climate and global changes. The exponential response of BVOC emissions to temperature (discussed above) entails a threefold to sixfold increase for a 10 8C rise in temperature (Q10 value), whereas the Q10 of the typical biochemical reactions such as those involved in photosynthetic carbon assimilation is only between twofold and threefold [93]. BVOC emissions should also therefore be considered in models of future net ecosystem productivity and carbon fluxes, particularly because of their high sensitivity to climate and land cover perturbations. They could even be taken into consideration for the calculation of ecosystem, regional and national carbon dioxide budgets [11]. 139

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trations of methane. For example, there is currently only a limited formation of spring or winter smog in high latitude and altitude habitats, but the conditions might become suitable for producing it if warming continues. Similar stronger effects on regional air quality can be expected in arid areas such as Nevada in the US [100]. The effects of increasing BVOC emissions on atmospheric chemistry will be multiple. In further evidence of the multiple interactions of these processes that involve BVOCs, as a result of atmospheric BVOC degradation including the reaction with NOx and other nitrogen containing compounds, changes in BVOC emissions can also influence the regional transport and deposition of airborne nitrogen [101], and hence be increasingly involved in the global terrestrial eutrophication phenomenon.

Figure 3. Effects of increased BVOC emissions on atmospheric chemistry and climate. Schematic figure of coupling of enhanced BVOC emissions and atmospheric and climatic changes: increased temperature will enhance BVOC emissions (+). Increased BVOC emissions will enhance aerosol formation and growth and therefore also enhance aerosol and CCN concentrations. Enhanced aerosol and CCN concentrations will decrease temperature (–) as a result of increased reflection of sunlight from low clouds back to space. However, other positive feedbacks (direct greenhouse effect of BVOCs, indirect greenhouse effect through ozone formation and methane lengthening lifetime, CO2 production and release of latent heat of water condensation) are also present and require further research.

BVOCs also seem to influence the oxidizing potential of the troposphere. BVOC degradation entails the formation of tropospheric ozone (Figure 3), which is a key pollutant in photochemical smog events [66,94] and the third most important greenhouse gas after CO2 and methane [17]. However, BVOCs also readily react with ozone and hence contribute to its destruction. Whether or not net ozone formation occurs depends mainly on the presence of NOx, which essentially derives from combustion processes in polluted urban areas. Recent studies have reported for the first time a long-term assessment of the significant impact of BVOCs on ozone levels at a continental scale, considering the key processes of NOx emissions, the photochemical activity, the transport and the ozone losses by dry deposition [95]. The latter study and others [96] yield relevance to modeling and estimating BVOC emission at a large scale in relation to air quality policies and future land use changes. These important aspects of alteration of air quality mediated by BVOCs should also be studied further in urban environments [32,97,98]. Nevertheless, even in an unpolluted atmosphere, BVOC emission can indirectly increase the concentrations of other important greenhouse gases, namely methane, because BVOC emissions seem to reduce the atmospheric oxidation capacity by depleting the level of OH (hydroxyl) radicals. OH radicals are very reactive oxidants and act as the primary cleansing agent for the atmosphere [99]. However, recent field studies in the remote Amazon basin have provided evidence that BVOC emissions have a considerably smaller negative effect on hydroxyl radical levels than previously thought [99]. The changes in BVOC emissions expected in response to global change will thus affect their oxidizing effect. If they increase as expected, they will probably increase the formation of ozone and the concen140

Climate In the past, less attention has been given to BVOC climate effects because it was thought that the short lifetime of BVOCs would preclude them from having any significant direct influence on climate. However, there is now emerging evidence that this influence might be significant on different spatial scales, from local to regional and global, through aerosol and cloud condensation nuclei formation, and direct and indirect greenhouse effects. This effect can be even more significant now, with increasing emission rates in response to warming and global change (Figure 3). BVOCs might be the most important factor behind the formation and growth of secondary organic aerosols [102,103]. Large and oxygenated BVOCs frequently found in the emissions of plant species seem particularly relevant in the nucleation and growth of particles [104]. The terpenoids are known to lead to aerosol formation by rapid reactions with atmospheric oxidants such as ozone, hydroxyl radicals and nitrate radicals [105]. Very low volatility products are formed from the ozonolysis reaction of some terpenes, which has been observed in several laboratory studies [106], and is becoming more important with the rise of tropospheric ozone concentrations as a result of anthropogenic activities [107]. These low volatility products readily take part in gas-to-particle conversion processes [108]. The increased BVOC emissions projected for the near future or in comparison with previous decades thus generate more condensable vapors, and aerosol particles theoretically grow to cloud condensation nuclei (CCN) sizes in a shorter time, thus also increasing CCN concentrations [109]. This will subsequently increase the optical thickness of individual clouds resulting in an increase in the reflection of sunlight back to space. Once formed, clouds influence the radiation budget of Earth extensively by contributing to albedo and greenhouse effects. As a result, there should be a more intense net cooling of the surface of Earth during the day because of radiation interception. Either directly, by reflecting more solar radiation, or indirectly, by increasing CCN, the increase in aerosols reduces the amount of solar radiation reaching the surface of Earth with a consequent cooling effect. A recent study [110] observed aerosol optical thickness resulting from BVOCs which in summer is sufficient to form a regional cooling haze over the southeastern US (i.e. it constitutes a significant potential for a regional

Review negative feedback on climate warming). Furthermore, aerosols scatter the light received by the canopy, increasing CO2 fixation [111] and providing another indirect, potentially negative feedback on warming. However, these increased BVOC emissions might instead add to global warming if isoprene responds more to warming than other BVOCs and if it reacts with OH radicals. It has been proposed [112] that the scavenging of OH radicals by isoprene reduces the occurrence of nucleation or condensation. However, the results of this study seem to contradict recent field measurements [99] and the results of laboratory experiments [113] which suggest that isoprene causes a relatively minor suppression of OH radical concentrations owing to efficient OH radical recycling. Field complex multicomponent multifactor experiments instead of only chamber studies are needed to clarify this question. It has also been observed that BVOCs help to slow down nocturnal cooling in areas with relatively dry air masses and active photosynthesis [114]. Extreme nocturnal inversions (5–10 8C warmer at 50 m above ground than at ground level) have been reported in the field over areas covered by high terpene emitters [115]. These retarded heat losses and the addition of heat to the lower atmosphere have been interpreted as a result of the greenhouse action of some BVOCs combined with the latent heat of water condensation into BVOC-derived aerosols being released into the environment [116]. These positive warming feedbacks could also be enhanced by increased BVOC emissions. Moreover, as mentioned above, BVOCs also increase ozone production and the atmospheric lifetime of methane, enhancing the greenhouse effect of these gases. It therefore seems that the increases in BVOC emissions expected as a result of the current warming and global changes could thus significantly contribute (via negative and positive feedbacks) to the complex processes associated with global warming. Whether the increased BVOC emissions will cool or warm the climate depends on the relative weights of the negative (increased albedo and CO2 fixation) and positive (increased greenhouse action) feedbacks (Figure 3) [7]. Laboratory experiments, global climate modeling and extensive international measurement campaigns are necessary to answer this question and to develop more quantitative estimations on its climatic significance. Unknowns and future directions Global change effects The large volume of existing data on elevated temperature and drought effects on BVOC emissions stems mostly from short-term experiments performed on young and often potted saplings. What these results mean in terms of the long-term responses of mature vegetation growing in complex communities should be questioned. Indeed, the results from field experiments on mature trees do not always match the findings from laboratory studies. For example, in free-air carbon dioxide enrichment experiments, Calfapietra et al. [117] observed no clear effect of elevated CO2 on isoprene emissions from field-grown aspen trees as predicted in previous studies [77]. Similarly, in a recent 2-year study of a holm oak forest, Lavoir et al.

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[118] observed a strong and repeated inhibition of BVOC emissions during the summer drought periods, a rather surprising result given that in laboratory experiments the emissions of the same or closely related species were found to be highly resistant to drought [42]. Furthermore, not only the absolute strength of change of an environmental component but also its timing and duration determine the response of plants to this change. This response is further modulated by the many other stresses and competitors that plants constantly face under field conditions. The impact of some global environmental changes other than climate change on BVOC production have rarely been studied. For example, this is true of changes in the radiative properties of the atmosphere. Increasing UV radiation increases oxidative stress in plants and reduces photosynthetic carbon gain [119], whereas increased diffusive radiation through aerosols reduces oxidative stress and increases photosynthesis [111]. Whether this could strengthen or weaken BVOC releases is currently unknown. The effects of nutrient availability on BVOC fluxes should also be the focus of more attention. The available data are rather controversial, showing that our level of scientific understanding on this topic is still low. However, eutrophication has an important long-term impact on the functioning and the biodiversity of terrestrial ecosystems [120] and therefore cannot be ignored. The effects of changing nutrient availability on BVOC fluxes might be most relevant in boreal forests, the largest biome of the world. Boreal forests are composed of only a few tree species, mostly conifers, which emit substantial amounts of monoterpenes and sesquiterpenes in addition to isoprene and other BVOCs [121]. Tropical forests represent another potential major BVOC source because of their enormous standing biomass and high biological productivity under warm temperatures and strong irradiance [18]. These extremely species-rich forests are highly vulnerable to changes in precipitation patterns [122], as well as land use changes [123]. Assessing how their BVOC emissions could therefore change in the future and the possible feedback on the climate system of Earth is particularly important. Nonetheless, only a few studies have so far been undertaken to characterize the primary emission of BVOCs from tropical tree species [124,125], which is too preliminary to provide a reliable picture of the emissions from forests presenting a unique biodiversity. More field studies are thus warranted, particularly long-term studies, in the different biomes, and taking into account the different global change components in addition to the first steps already conducted in this area ([13,29–31] and references in Table S1 in the supplementary material online). Ecological and evolutive effects The ecological alterations generated by a world with very likely increased emissions require an in-depth research effort. With current global changes such as warming or increased ozone, the emission of terpenoid volatiles for the protection of plants against the abiotic stress generated for such global changes will become increasingly important. The interaction between plants and pathogens or herbivores and their predators might be disturbed moreover by 141

Review the response of these organisms to such enhanced abiotic stresses. Changes in volatile signal production might have a different impact on plant–plant communications compared with plant–insect interactions, given the absence in plants of the olfactory organs present in insects. In overall terms, the changes in BVOC production, pools, emission rates, timing and function with climate and global changes are likely to alter the interactions of plants with other plants, microorganisms and herbivores, and the resulting evolution of species, communities and ecosystems is a fruitful field for research. Research setups that are long-term field-based model systems enabling the detection of changes in BVOC emission profiles throughout the growth season and over many years, and the measurement of relevant insect abundances (natural and introduced), are particularly valuable. However, laboratory experimentation is still crucial in ascertaining the underlying specific mechanisms in the responses of plant and interacting organisms. Systems biology and transgenic approaches can provide a large amount of help in this area. In another sphere, research could also consider the enhanced competition of BVOC production in a warmer changed world with growth and photosynthesis [77]. Atmospheric and climatic effects Similarly, a quantification of the changes in atmospheric chemistry and in local, regional and global climate produced by increased BVOC emissions is still urgently needed. They warrant a multidisciplinary effort to quantify carbon emission, aerosol formation and reactions with hydroxyl radicals and ozone, among other processes including soil or water deposition. As is the case with so many environmental and ecological issues, interactive interdisciplinary research among biologists, physicists and chemists at foliar, ecosystem, regional and global levels is needed to produce data on genetic, biochemical, physiological and ecological controls of BVOC emissions associated with climate and global change, and new models need to be implemented at leaf, whole-plant and vegetation levels [1,44,126] to solve these environmental puzzles. Concluding remarks Based upon the work reviewed above, we can be reasonably sure that climate and global change in general will have an impact on BVOC emissions, that the most likely overall impact is an increase in BVOC emissions mostly driven by current warming, and that the altered emissions will affect their physiological and ecological functions and their environmental role. However, although great progress has been made in the fundamental understanding and mechanistic modeling of environmental controls over the emissions of some BVOCs, our level of knowledge is still insufficient to make reliable quantitative predictions of the evolution of emissions and its consequences in a changing world, partly because of the complexity of the problem and partly because of the limited research. This is particularly true for emissions of sesquiterpenes and other BVOCs associated with defense against biotic stresses and for oxygenated BVOCs. Further research to fill knowledge gaps in this fundamental issue 142

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in life functioning and environmental conditions is strongly warranted. The effort is intellectually and environmentally worthwhile. Acknowledgements This research was supported by the European Science Foundation Grant ‘‘VOCBAS’’, grants from the Spanish Government (CGL2006-04025/BOS and Consolider-Ingenio Montes CSD2008-00040) and by the Catalan Government grant SGR 2009-458.

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