Elevated O3 threatens biological communications mediated by plant volatiles: A review focusing on the urban environment

Abstract Plant volatiles, particularly biogenic volatile organic compounds (BVOCs), emitted in urban areas have attracted attention as olfactory signals between plants and other organisms, including insects. However, in urban areas, elevated ozone (O3) levels inhibit plant growth and degrade olfactory signals, including both insect pheromones and BVOCs, resulting in disrupted biological communication. In this article, we review recent findings on how O3 modifies olfactory interactions, focusing on both the emitters and receivers of these signals. The influence of O3 on herbivorous insects and their enemies alters the pressure caused by herbivorous damage in the field, which can affect the development of the defensive capacities of plants at the hereditary level. To address the challenges posed by O3 in biological interactions, BVOC characteristics (e.g., emission rate and species, blend composition, O3 reactivity, and oxidative products) and O3 effects on insects (e.g., preference and antennal detectivity) should be clarified. At the same time, BVOC emissions are expected to increase with rising temperatures, which will likely increase the impact of BVOCs on O3 formation in the future. Therefore, it is necessary to devise strategies, such as selecting non- or low BVOC emitters, to regulate BVOC emissions from urban greening plants and mitigate O3 risks to olfactory interactions and plant health. Graphical Abstract


Introduction
Increasing tropospheric ozone (O 3 ) is a major concern worldwide because of its negative impacts on plant health (Karmakar et al., 2022;Agathokleous et al., 2022) as well as human health (Zhang et al., 2019). For example, O 3 entered from stomata oxidizes plant tissues, causing photosynthetic suppression and visible injury. Particularly in urban areas, roadside trees, and plants are planted to provide urban greening for improving esthetics and the environment by decreasing temperature and air pollution. Therefore, O 3 -damaged plants cannot meet these requirements. Furthermore, because the above-and belowground parts of plants are connected, the O 3 effects on the belowground parts should not be ignored. The aboveground effects of elevated O 3 , such as defoliation and photosynthate allocation, can alter root growth, soil litter decomposition, and soil microorganisms, thus disrupting belowground ecosystems (Vitale et al., 2019). In turn, these belowground effects can affect the aboveground parts via lowered supportive functions of the roots and the soil environment. Agricultural cultivation in urban areas also faces such threats due to elevated O 3 (Kobayashi, 2022). In a situation where O 3 levels continue to increase in the future, the understanding of O 3 effects on plants should move beyond just foliar compositional traits to take a more holistic approach.
O 3 effects on herbivorous insects are a major factor because herbivorous damage contributes significantly to the loss of primary plant production (Lindroth, 2010). Elevated O 3 levels suppress photosynthesis and the capacity to defend against insects. For example, foliar defensive chemicals (e.g., condensed tannins and total phenolics) are lower in Japanese white birch (Betula platyphylla var. japonica) when exposed to elevated O 3 (Agathokleous et al., 2017;Abu ElEla et al., 2018). Moreover, herbivorous leaf beetles (Agelastica coerulea) preferred ozonated leaves to non-ozonated birch leaves in laboratory tests (Agathokleous et al., 2017). A similar phenomenon of defense capacity under elevated O 3 conditions has been reported in elm leaves (Sugai et al., 2020). In addition to severe damage by direct O 3 effects (e.g., withering and visible injuries), leaves exposed to elevated O 3 are vulnerable to attacks by herbivorous insects via qualitative changes in the leaves (Cotrozzi et al., 2021). Notably, O 3 and numerous other environmental stressors can positively affect plant physiological activities and growth at low levels within the framework of "hormesis" . For example, O 3 induced a biphasic response in the concentration of phenolic compounds in the leaves of a hybrid poplar, which was driven by a subset of phenylpropanoids such as condensed tannins (Li et al., 2021). Condensed tannins and other phenolic compounds act as defense chemicals against herbivorous insects. Thus, in this case, plants may suppress the herbivorous damage under moderate O 3 level. However, a vast body of literature illustrates that the current ambient O 3 exposure is considerably elevated and beyond the toxicological threshold for negative effects on vegetation worldwide, indicating that negative O 3 effects are more predictable than positive ones (Karmakar et al., 2022;Agathokleous et al., 2022).
Field observations sometimes do not align with expectations based on the defense capacities of leaves (or laboratory feeding tests). In the case of leaf beetles, there were few visits to trees under elevated O 3 despite the lower defensive capacities of the leaves (Agathokleous et al., 2017;Sugai et al., 2020). In these cases, the discrepancy can be explained by the O 3 -reactive plant volatiles acting as olfactory signals. Biogenic volatile organic compounds (BVOCs) emitted into the atmosphere act as olfactory signals, contributing to the biological communication between plants and insects such as herbivorous insects and pollinators (Šimpraga et al., 2016;Sharma et al., 2019). This explains why biological olfactory systems are essential in various landscapes such as forests, agricultural fields, and other urban plantations (Takabayashi & Shiojiri, 2019). Insects use BVOCs to detect target plants based on BVOCs attractiveness. However, the preference of insects (e.g., herbivorous pests and pollinators) for BVOCs can decrease as the O 3 level increases, although O 3 itself does not appear to exhibit any attractive or repellent influence at environmentally relevant concentrations (Fuentes et al., 2013;Masui et al., 2020). Irrespective of foliar quality, O 3 impedes plant-insect communication via the oxidation of key components among attractive BVOCs, which leads to a lower frequency of plant visitation under elevated O 3 . Therefore, when examining O 3 effects on biological interactions between plants and insects, it is crucial to consider not only foliar quality but also olfactory signals. (Blande, 2021;Masui et al., 2021). Moreover, BVOCs contribute to O 3 formation in the atmosphere. Hence, the control of BVOCs in urban areas leads to the preservation of BVOC-based biological interactions.
In this article, the atmospheric function of BVOCs is discussed, with a focus on the impact of BVOCs on O 3 formation via photochemical reactions. Various biological functions of olfactory signals have been reviewed from the viewpoint of both emitters and receivers in ecosystems. In addition to plant-insect communication with BVOCs, plant-plant interactions, and insect-insect communication are discussed based on damage-induced BVOCs and insect pheromones. Practical examples of the application of olfactory signals in agriculture are also presented. Finally, the negative influences of elevated O 3 on biological communication and possible associated risks are discussed, providing a perspective for enhancing ecological health in urban environments.

O 3 formation in urban areas
Controlling the O 3 concentration requires removing the primary cause (precursors) from the atmosphere, especially in East Asia, where the emission of NO 2 (an O 3 precursor) is approximately four times larger than that in the EU and U.S.A. (Qu et al., 2022). O 3 formation occurs through photochemical reactions under ultraviolet rays, in which nitrogen oxides (NOx) and VOCs are the reactants (Hidy, 2022). The VOCs that affect O 3 formation are categorized as anthropogenic VOCs (AVOCs) and biogenic VOCs (BVOCs). The contribution of BVOCs to O 3 formation is of great concern (Calfapietra et al., 2013), partly because the total amount of BVOCs emitted into the atmosphere is estimated to be approximately 10 times higher than that of AVOCs (Lun et al., 2020). In addition, even if NOx emissions are maintained at lower levels, O 3 concentration is still high (Sicard et al., 2020a;Qu et al., 2022) as was recently shown during lockdowns worldwide during the COVID-19 pandemic (Querol et al., 2021). This occurred because the photochemical reaction occurred in a VOC-limited state, indicating that controlling VOC emissions into the atmosphere is crucial from the perspective of atmospheric chemistry (Sicard et al., 2020b).
The effect of BVOCs on O 3 formation depends on the characteristics of the emitted compounds, and plant phenological patterns (Panopoulou et al., 2020). There are many types of BVOC emitters, such as high/low/non-emitters, isoprene, and monoterpene (MT) emitters. The composition of each group varies widely (Tani & Mochizuki, 2021) as shown in Table S1 (Supporting Information). For example, in the same genus, Quercus serrata (isoprene emitter), Q. ilex (MT emitter), and Q. acutissima (non-emitter) can be categorized into different groups based on their ability to emit BVOCs. Similarly, different BVOCs emission abilities were also found in Fagus trees, specifically between European beech (Fagus sylvatica), an MT emitter, and Japanese beech (F. crenata), a non-emitter (van Meeningen et al., 2016;Tani & Mochizuki, 2021).
Generally, BVOCs emission rates depend on the temperature in MT emission of the storage type or both temperature and light (photosynthetic photon flux density) in isoprene emission (Guenther et al., 1993), with some exceptions, such as MT emission from Q. phillyraeoides following the isoprene-type algorithm (Okumura et al., 2008). Research on Acer palmatum also indicated that a 3 °C warmer environment resulted in the earlier beginning of the growing season and delayed the termination of BVOCs emission . Therefore, the duration of BVOC emissions increased, leading to larger loads of BVOCs, particularly from high BVOC emitters. In the business-as-usual (BAU) scenario with a 1.96 °C increase in temperature under representative concentration pathways 4.5 scenarios (RCP 4.5), it is estimated that current BVOCs emissions will increase by approximately 3 times by 2050 (Ren et al., 2017). With the ongoing global warming, the impact of BVOCs on O 3 formation will continue to increase in the future (Fitzky et al., 2019). In addition, a study on Japanese cedars indicated that geographical differences in climate and pathogen variability can affect BVOCs composition , which illustrates the importance of considering multiple environmental factors and seasonal variations when estimating BVOCs fluxes.

Tree selection to control BVOCs emissions in urban areas
Countermeasures are required to decrease the O 3 concentrations in cities. In urban areas, there is urban greenery such as street trees, roofs, and parks. Selecting plantation species based on the characteristics of BVOC emissions is a strategy for controlling BVOC emissions as a precursor of O 3 from these urban sources (Sicard et al., 2018). Low or non-emitters of BVOCs are suitable for plantations. However, it should be considered that non-and low-BVOC emissions may imply plant susceptibility to O 3 stress since some plants emit BVOCs to protect themselves from oxidation (Pinto et al., 2010;. Before selecting plant species as urban greening materials, it is critical to evaluate whether non-and low-BVOC emitters can survive various environmental stresses, including elevated O 3 levels. As a defense against O 3 stress, glandular trichomes act as a barrier to reduce O 3 uptake (Oksanen, 2018). Although non-glandular trichomes do not have such a defensive role against O 3 stress, they provide resistance to other environmental stresses, such as pathogens, insect herbivores, and radiation, particularly UV-B (Karabourniotis et al., 2020). Furthermore, it is important to consider the O 3 -removal ability of urban plants (Sicard et al., 2022). Broadleaved trees can remove more O 3 from the atmosphere than conifers, and their removal abilities differ between species (Sicard et al., 2018) as shown in Table S2. For example, Fraxinus excelsior has a high O 3 removal ability, whereas that of Robinia pseudocacia is low. It is worth mentioning that some plant species have a higher impact on O 3 formation than on their O 3 removal ability (Ren et al., 2017). Therefore, the selection of urban plant species should be conducted carefully, considering both properties, the degree of impact on O 3 formation, and O 3 removal ability. Simultaneously, using a more comprehensive approach, cost-benefit relationships should be evaluated, focusing on factors such as VOC uptake and pollen allergenicity. In terms of VOC uptake by plants, knowledge has been accumulated that some VOCs such as oxygenated ones are absorbed via the stomata of leaves (Tani & Mochizuki, 2021). Absorbed VOCs are metabolized in the leaves, some of which are emitted again as different compounds into the atmosphere (Tani et al., 2022); for instance, methyl vinyl ketone, a VOC with a high impact on O 3 formation, is converted to methyl ethyl ketone in the leaves (Cappellin et al., 2019;Tani et al., 2020). There is still a lack of knowledge regarding the effects of environmental factors (e.g., O 3 and temperature) on the exchange of VOCs in the real world. Further research in this field will contribute to an accurate understanding of VOC dynamics and the estimation of O 3 trends.

Plant-plant/insect communication via olfactory signals
There are two processes by which insects locate target leaves or flowers: short-range attraction using visual cues and long-range attraction using olfactory cues. For example, visual cues such as color, size, shape, and abundance of flowers are essential for attracting bees, but the visual detectability of most flowers is only a few meters (Kapustjansky et al., 2010). Although visual cues should not be ignored, BVOCs play a primary role as olfactory signals because of their long-range function. There are a variety of compositions (blends), even with the same set of compounds, in many plant species. In most cases, a certain blend is highly attractive, whereas the attractiveness of the individual components is lower than that of the blend (Bruce & Pickett, 2011;Proffit et al., 2020). Insects locate their target plants by detecting specific BVOC compositions from far away, even hundreds of meters (Bruce et al., 2005;Krishnan et al., 2020). In particular, some cases exhibit species-specific communication, called obligate-mutualistic interactions, such as those between Phyllanthaceae plants and Epicephala moths (Gracillariidae). Phyllanthaceae plants emit different BVOC compositions depending on their sex (staminate or pistillate flowers). Epicephala moths visit pistillate flowers after staminating them to pollinate and foster the production of seeds that are fed to their descendent larvae hatched on the seeds (Okamoto et al., 2013;Huang et al., 2022).
Plants not only passively suffer attacks by herbivorous insects but can also suppress pest populations by inducing BVOC emissions, namely herbivore-induced plant volatiles (HIPVs). HIPVs are induced not only by herbivore damage but also by insect oviposition and pathogen infection. The emission induced by herbivore damage depends on the difference in the types of secretions in damaged leaves (Turlings & Tumlinson, 1992;Shiojiri et al., 2000b), feeding vibrations (Body et al., 2019), and herbivore guilds, such as chewing or sucking (Davidson-Lowe & Ali, 2021), which are mainly related to the jasmonic acid (chewing) and salicylic acid (sucking) pathways (Leitner et al., 2005). HIPVs also act as repellents to herbivorous insects, whereas in other cases, they act as attractants (De Moraes et al., 2001;Davidson-Lowe & Ali, 2021). Therefore, attacked plants can suppress damage by avoiding herbivores by using HIPVs. Furthermore, HIPVs attract natural enemies and induce defenses in neighboring plants. Attracting natural enemies is an indirect defense mechanism, as has been shown in cabbage for instance (Shiojiri et al., 2000b). Cabbage plants damaged by the larvae of the diamondback moth (Plutella xylostella) or cabbage white butterfly (Pieris rapae) emit HIPVs with different blends depending on the pest, although the components are mostly the same. Each blend of HIPVs induced by P. xylostella or P. rapae attracts the natural enemies of the corresponding herbivore, such as the parasitoid Cotesia vestalis (synonym: Cotesia plutellae) or Cotesia glomerata, respectively (Shiojiri et al., 2000a). However, the interaction between P. xylostella and C. vestalis was more complex when caterpillars of P. rapae coexisted in the same cabbage field. As mentioned previously, the blend is an important determinant of whether BVOCs act as insect attractants. C. vestalis struggles to find P. xylostella in the presence of P. rapae feeding because the blend of HIPVs induced by P. xylostella is downgraded by HIPVs induced by P. rapae. Another possibility is that C. vestalis avoids the risk of accidental parasitism to non-host caterpillars of P. rapae infested on the same plants. In addition, adult females of P. xylostella prefer to oviposit on cabbages infested with P. rapae (Shiojiri et al., 2002), as if they knew that the parasitoid C. vestalis could not recognize the plants (Shiojiri et al., 2000b; Figure 1). In the case of the moth species (Heliothis virescens), adult females avoid ovipositing on tobacco plants previously infested with conspecific Cotesia vestalis (the synonym is Cotesia plutellae). P. xylostella and Pieris rapae induce same plant volatiles by feeding cabbage leaves but the composition is different depending on the pest. the color and size of circles indicate the compound species and the amount of induced plant volatiles, respectively. C. vestalis as a parasitoid for P. xylostella specifically detects the induced plant volatiles by P. xylostella (right red allow). on the other hand, adults of P. xylostella prefer to oviposit on cabbage plants infested with P. rapae (left red allow). C. vestalis has a hard time to detect its prey with the altered composition by P. rapae (blue arrow). larvae, which is considered a strategy to avoid potential risks, such as competitors for their offspring and natural enemies attracted by HIPVs (De Moraes et al., 2001). In addition, silkworms are less suffered to parasitoids because they suppress the emission of parasitoid-attractive HIPVs using an enzyme, namely Bombyx mori fatty acid hydroperoxide dehydratase (BmFHD) (Takai et al., 2018). Hence, herbivorous insects recognize the risks posed by parasitoids and have developed strategies to defend themselves against them. Complex insect (herbivores)-insect (natural enemies) communications are constructed via each plant-insect communication based on HIPVs.
The second effect of HIPVs is to induce defense in undamaged branches/plants via plant-plant communication; plants can also detect volatiles . Plants receiving HIPVs prepare for the biosynthesis of defensive compounds and emit volatiles that are attractive to natural enemies or repellent to pests in a similar manner as damaged plants do (Paudel Timilsena et al., 2020;Shiojiri et al., 2021). For example, undamaged branches of young beech (Fagus crenata) trees suppress herbivorous damage when they receive HIPVs released from other beech individuals with damaged branches (Hagiwara & Shiojiri, 2020). The effective distance between conspecific individuals is approximately 7 m in the field (Hagiwara et al., 2021). The effective distance depends on factors that affect the emission of volatiles, such as the size of the plants, plant species, extent of damage, and environmental conditions (Karban et al., 2006;Hagiwara et al., 2021). Furthermore, BVOC emissions and the number of kindreds in a plant are positively correlated (Ishizaki et al., 2012). Plants can self-recognize their volatiles; the greater the degree of kindred, the higher the herbivore resistance exhibited by receiver plants as a response to HIPVs from emitters (Karban & Shiojiri, 2009;Karban et al., 2013). Within the same plant, signals can be sent to the entire plant through the phloem pathway (Gaupels et al., 2017). In contrast, in plants that do not engage in phloem signaling, for example, sagebrushes, BVOC-mediated communication is necessary to send signals to different branches (Karban et al., 2006). HIPVs is an essential factor for various ecological communities, as described above, and it is noteworthy that water availability, as well as other environmental stresses on plants, can change the emission of HIPVs and the derived indirect defense against herbivores (Erb, 2018;Lin et al., 2022). Droughts (low water availability) and excessive precipitation (high water availability), which are expected to occur more frequently in the future, may alter interactions via HIPVs.

Practical use of BVOCs-mediated communication
BVOCs are expected to be applied in agriculture. Global changes, such as global warming, have recently been linked to higher pest activity. It is of concern that the number of pest species, outbreak frequency, and habitat area also increase as long as the changing environmental conditions are favorable to pests (Skendžić et al., 2021;Guedes et al., 2022). At the same time, global changes may also decrease the efficacy of pesticides. For instance, elevated temperatures alter the molecular mechanisms (e.g., ion channels and gene expression) to lower the susceptibility of pests to some types of pesticides (Benelli et al., 2021). In addition, elevated temperatures and carbon dioxide levels accelerate metabolism and alter the translocation of pesticides in treated plants, resulting in the effective duration (residual efficacy) of pesticides for some target pests becoming shorter than expected (Matzrafi, 2019). Therefore, worldwide pesticide use to control pest populations is expected to increase further. Increased pesticide use leads to risks (e.g., resurgence and development of resistance) by affecting chemical stability in the future (Matzrafi, 2019;Ma et al., 2021). This is also important in urban areas because suburban agriculture is becoming increasingly prevalent, and the toxicity of pesticides is a concern for human health as well as for a plethora of beneficial insects, such as honey bees (Chmiel et al., 2020). Reducing the use of synthetic pesticides is of international interest (Lu et al., 2022), hence, pest management requires more sustainable agricultural applications.
Integrated pest management (IPM), which aims to reduce pesticide application to the environment, also relies on BVOCs, including insect pheromones (Brilli et al., 2019;Huang et al., 2020). Because plant volatiles influence the instinct activity of pests (e.g., feeding and oviposition), volatile-based IPM is useful and will become more necessary in agroforestry in the future. For example, the application of the interaction between the diamondback moth P. xylostella and the parasitoid C. vestalis in IPM has recently indicated its practicality in greenhouses and may provide a basis for extending it to the field (Shiojiri et al., 2010;Abe et al., 2020;Uefune et al., 2020). In addition, the "push-pull strategy," one of the IPM methods, has been developed based on plant-insect communication (Cook et al., 2007;Bhattacharyya, 2017;Cui et al., 2022). "push" plants planted in the same cultivated field emit volatiles repellent to target pests and "pull" plants planted around the field trap the pests by their attractive volatiles. In the field, the entire ecosystem is expected to be conserved through integrated biodiversity management (IBM), which means IPM plus the conservation of ecosystems (Kiritani, 2000). For instance, forests that are home to parasitic wasps near villages are preserved under human activities using fewer pesticides.
Plant-to-plant communication using HIPVs has also attracted attention in IPM. The finding that plant-plant communication also occurs interspecifically, as well as between conspecific plants, is considerably useful in IPM. For example, damage by herbivores in a soybean (Glycine max) field was lower when exposed to volatiles of weeded goldenrod (Solidago altissima), which resulted in a significant increase in soybean yield (Shiojiri et al., 2017). Similarly, the coexistence of some mints indicates the suppression of herbivore damage in legumes and Brassicaceae plants by boosting the expression of defense genes; thus, these mints appear to be promising companion plants (Sukegawa et al., 2018). In an IPM strategy, an appropriate blend and concentration are crucial for attracting natural enemies and enhancing the defensive capacities of neighboring plants (Heil & Karban, 2010). Additionally, the IPM strategy may be adopted for forest tree management (Hagiwara et al., 2021). These new insights indicate the potential applicability of olfactory signal-based IPM in agroforestry systems in urban environments, which warrants further research. Detailed information on the practical use of the above-mentioned BVOCs is presented in Table S3.

Effects of O 3 on BVOC emissions
In air-polluted environments such as urban cities, O 3 changes the emissions of BVOCs synthesized through photosynthetic products depending on the plant species. Some emitters are stimulated by O 3 to emit more BVOCs while other species do not respond or decrease the emission (Kivimäenpää et al., 2016). Different BVOCs emissions affect olfactory biological interactions. Considering the impact of atmospheric pollution, there is an unfavorable loop for producing more O 3 in the atmosphere if O 3 increases BVOC emissions. Elevated O 3 levels accelerate HIPVs emissions, as observed in Scots pine (Ghimire et al., 2017). Furthermore, the O 3 sensitivity of plants may differ depending on the amount of nitrogen (N) deposition (Feng et al., 2019;Qu et al., 2022), and N deposition itself affects BVOC emissions (Yuan et al., 2020). The O 3 effects on BVOCs emissions depend on the species of emitted compounds and leaf stages and seasons (Kivimäenpää et al., 2022). Therefore, an investigation of the BVOC profiles of various plant species is needed, especially in urban environments with different gradients of O 3 pollution.

Effects of O 3 on post-emitted BVOCs in the atmosphere
In addition to the direct effect of O 3 on BVOC emissions through physiological changes, O 3 has high reactivity with some BVOCs (Atkinson & Arey, 2003;Conchou et al., 2019). After being emitted into the atmosphere, the concentrations of these BVOCs decrease below the threshold of the detection ability of insects and/or change to different compositions from the original, which are attractive to insects. This raises the question of what changes occur in ecosystems when BVOC-mediated communication is disrupted by O 3 . Regarding the decreased concentrations of BVOCs, O 3 shortened the effective distance (as shown in the aforementioned example with beech) compared with cleaner air (Fuentes et al., 2016). This is alarming because one of the advantages of BVOCs, compared with other attraction factors (e.g., color and shape), is that they can be detected even far away where visual signals cannot be received. The effective distance between BVOCs refers to the range within which insects can detect host plants to perform their activities (e.g., feeding and pollination). The overlapping of some ranges contributes to the interactions between organisms and gene flow. Narrowing the ranges results in communication patches and, thus, the isolation of each community in an ecosystem (Figure 2). For example, if damaged plants emit HIPVs against other individuals, there is a concern that non-damaged plants growing at a distant location cannot receive olfactory emergency signals in the presence of elevated O 3 . In addition, the concentration and exposure time of BVOCs are important for receiver plants to take defensive actions in response to the perception of BVOCs from emitters (Girón-Calva et al., 2012;Yoneya & Takabayashi, 2014). Even within an effective range, induced responses are not exhibited in receiver plants because of the lack of BVOC concentration and exposure time in air-polluted environments.
Alteration of the BVOCs composition is a severe problem caused by elevated O 3 because the BVOCs composition plays a key role in sustaining the attractiveness of insects. Various components in a blend are crucial to its overall attractiveness, and the loss of just one component may cause the blend to lose its attractiveness. As described previously, numerous insects locate their target plants by detecting the unique composition of their BVOCs. Moreover, insect pheromones are altered, and their original functions, such as the aggregation and alarm of other individuals, can be diminished under elevated O 3 (Mondor et al., 2004;Boullis et al., 2016).
Oxidative products are also important and worth considering. The oxidative products of emitted BVOCs exist as secondary organic aerosols (SOA) in the atmosphere (Pinto et al., 2010). For example, α-pinene, a volatile emitted from many plants, changes into some oxidative products through the oxidation and subsequent aging processes; such as norpinic acid, 10-hydroxypinonic acid, diaterpenylic acid acetate, dinorpinic acid, and 8-hydroxypinonic acid (Yasmeen et al., 2012). SOA, some types of chemicals such as alcohols, acids, and aldehydes, can be deposited as secondary organic materials (SOM) on plant surfaces because of their low volatility . Contrary to BVOCs, which can be detected by insects from distant locations, these oxidative products affect the behavior of insects at close or contact scales. The longer chemical lifetimes of SOM compared to the original BVOCs, their toxicity, and their repellent function against insects (Li et al., 2016), indicate a large influence of SOM in an ecosystem.

Effects of O 3 on insects' detectability to BVOCs
There has a direct effect of O 3 on insects, in addition to the effects on BVOCs described previously. In a Y-tube preference test between O 3 and cleaned air (with no BVOCs), O 3 exhibited neither attractant nor repellent effects on insects (Fuentes et al., 2013;Masui et al., 2020). However, there are two possibilities: O 3 has no direct effect on insects, and O 3 impedes the olfactory ability of insect antennae (Dötterl et al., 2016;Vanderplanck et al., 2021). The latter possibility is critical for olfactory communication because insects detect volatiles using their olfactory receptors on the antennae. Interestingly, Dötterl et al. (2016) reported that O 3 impeded each volatile receptor in the olfactory system of honeybees, for example, by decreasing the response to (Z)-3-hexenyl acetate and not significantly changing the response to linalool and 2-phenyl ethanol. Contrary to the detectability of honeybee, the lifetime of (Z)-3-hexenyl acetate is long (7.3 h at 7*10 11 molecule cm −3 O 3 ), whereas that of linalool is considerably short (55 min at 7*10 11 molecule cm −3 O 3 ). Therefore, even if volatiles, such as (Z)-3-hexenyl acetate, do not diminish in the presence of elevated O 3 , insects cannot recognize them with inactive olfactory receptors. As a result, by affecting both the olfactory receptors and target volatiles, O 3 impedes biological communication via the olfactory system.

Risks associated with elevated O 3 in BVOC-mediated communication
O 3 inhibits numerous types of communication, including insect and plants (Masui et al., 2021;Knaden et al., 2022). Consequently, O 3 disturbed the original ecological and agricultural functions of the BVOCs (Figure 3). Regarding ecological roles, the secondary risks derived from altered insect-plant communication due to O 3 are of concern. First, there are modifications to the ecological balance in the field, and changes in the population and activity of insects can affect neighboring plant species (Hahn & Maron, 2016). For example, alder leaf beetles prefer some host plants of Betulaceae species (Park et al., 2004;Masui et al., 2022), but their reactivity with O 3 depends on their composition. Therefore, if the attractiveness of a primary host plant decreases due to the O 3 -derived degradation of volatiles, herbivorous damage can concentrate on other candidate host plants that retain their attractiveness with comparably lower O 3 -reactive volatile blends. The effects of O 3 may indirectly spread to neighboring plants by bringing new herbivorous insects and their natural enemies, which change the habitat distribution and organisms in the ecosystem. The chemical defensive system depends on the frequency of herbivorous attacks under a tradeoff scheme, which ultimately influences defensive evolution (Hull-Sanders et al., 2007;Fukano & Nakayama, 2018). Moreover, in the case of vectors, such as aphids, that mediate viruses to plants (Lu et al., 2022), fluctuating odor detectability in vectors also results in changes in pathogen distribution in the field. In the agricultural use of BVOCs, such as within IPM, biological communication by O 3 leads to the loss of agricultural products and risks to agroecosystem health (Girón-Calva et al., 2016;Ryalls et al., 2022a). For instance, possible risks under elevated O 3 conditions include natural enemies that are unable to locate the HIPVs of the target insects and an inability to transport plant-plant signals, which are intended to stimulate preparative defense systems, to other individuals. Pollinators are exposed to risks similar to those of herbivores, threatening plant reproductive success (Ryalls et al., 2022b). The effective range of flower volatiles is estimated to be less than 200 m under elevated O 3 in open fields (McFrederick et al., 2008). In the case of bumble bees, approximately 100 ppb O 3 disrupted pollination efficacy even in a 10-meter-long polytunnel, which raised the concern that controlled-environment agriculture (e.g., greenhouse cultivation) can also be affected by elevated O 3 (Saunier et al., 2023). Furthermore, there has been geographical evolution of floral scents (Byers et al., 2014). Changing the emission and composition of floral scents leads to the spoiling of the accumulated evolution and the relationship between flowers and target pollinators. Bees, which are the most popular pollinators, can be affected by O 3 -induced modifications in rewards (pollen and nectar), in addition to short-(visual) and long-range (olfactory) attraction (Figure 4). Because many bee species construct comprehensive sociality, they can learn and communicate with each other about the location of their preferred rewards. O 3 alters the amount and chemical composition of pollen and nectar, which may lower bee performance when visiting flowers (Duque et al., 2021). When the negative impacts of O 3 on all attraction systems occur concurrently, pollination efficacy may dramatically decrease compared to estimations based on the O 3 effect on each attraction system. Approximately 80-95% of flowering plants rely on insect pollination (Ollerton et al., 2011;Krishnan et al., 2020). Thus, with disrupted pollination systems, both ecologically (biodiversity) and economically (agriculture) important problems arise under elevated O 3 . BVOC-mediated communication occurs both above-and belowground (Papadopoulou & van Dam, 2017;Preece & Peñuelas, 2020). Plants receive BVOC messages emitted from the roots of the emitters in the soil. In addition, above and belowground organs interact with each other; for example, when belowground roots are infested by diseases and damaged by insects, the same individual plant emits induced volatiles from the leaves and vice versa (Escobar-Bravo et al., 2022). Although belowground communication with BVOCs is assumed to be less sensitive to O 3 (Acton et al., 2018), elevated O 3 conditions indirectly influence belowground communication via aboveground responses, such as altering the emission of volatiles from roots (Wang et al., 2016). However, O 3 indirect effects on belowground biological communication are under investigated and largely ununderstood. The possible risks of O 3 in biological communications are summarized in Table S4.

Perspectives for O 3 -polluted environments
Perspectives for biological and atmospheric aspects of BVOCs in O 3 -polluted environments, written below subsections, are summarized in Table S5.

Emission and uptake of BVOCs in soil
BVOCs emitted from the soil are a source contributing to O 3 formation in the atmosphere, similar to BVOCs emitted from plants aboveground. Soil BVOCs are emitted from plant roots and soil microbes and are affected by factors such as pH, organic matter, and soil microbial activities (Bourtsoukidis et al., 2018). Soil BVOCs are also positively correlated with soil temperature (Meischner et al., 2022), thus soil BVOC fluxes are expected to increase with global warming in the future. Microplastics are emerging as 'new' precursors of soil BVOCs. Microplastics are abiotic matter from anthropogenic products that accumulate in the pedosphere and other environmental compartments. Photodegradation and biodegradation of microplastic debris in soil or on the ground lead to the production of VOCs that are eventually released into the atmosphere (Agathokleous et al., 2021). In particular, because the microplastic load is larger in the pedosphere than in the oceanosphere, its impact is estimated to increase in urban and agricultural areas (Helmberger et al., 2020). Hence, further research is needed to reveal the degree to which microplastics accelerate the emission of VOCs from soils and how they can directly and/or indirectly change biological communication in O 3 -polluted environments.
However, soil also acts as a VOC sink. Contrary to the apparent sink (reversible reaction) by adsorption and dissolution into the soil, the degradation of VOCs by abiotic and microbial activities is a true sink because these processes are irreversible (Rinnan & Albers, 2020). When it comes to microbial activity, similar to soil-BVOCs emissions, soil temperature, and other environmental factors regulate the uptake of VOCs in soil. Furthermore, forest soils with ectomycorrhizal fungi can take up more VOCs, such as methanol, than forest soils with arbuscular mycorrhizal fungi, which is a valuable factor for both estimating soil-BVOCs fluxes and selecting tree species and appropriate locations for urban greening (Trowbridge et al., 2020). The net flux (uptake or emission) of VOCs in the soil is also regulated by the time of day, season, and volatile compounds (Bourtsoukidis et al., 2018). The balance between the source and sink of soil BVOCs is expected to become a more controversial topic in the future because both are related to microbial activity in a changing environment. How soil contributes to VOC uptake should be investigated as a possible practical application in O 3 -polluted environments.

New aspects of olfactory signals
Leaf surface wax chemicals, lipids, and long-chain fatty acids (LCFAs) also regulate the behavior of insects within a short range, such as attractant or repellent function and stimulation of oviposition (Debnath et al., 2021). Similar to BVOCs, these signaling chemicals react with O 3 and decrease the amount of olfactory information (Chu et al., 2019). The oxidation of LCFAs was observed, as indicated by malondialdehyde (MDA), an oxidative product of LCFAs (Yan et al., 2010). The decrease in LCFAs due to oxidation indicates the collapse of short-range communication in air-polluted environments. Therefore, the effect of O 3 on olfactory-mediated communication is divided into two stages: first, impeding the attraction of insects via BVOCs (long-range), and second, impeding the attraction via other olfactory signals and repelling with SOM (short-range). If olfactory signals are blocked at both stages, the odds of insects visiting the target plants decrease compared to when only the BVOC-mediated route is impeded. Despite the biological importance of LCFAs, information on actual changes in the amounts and compositions of LCFAs under elevated O 3 fields is limited and should be clarified.
Some exceptions cannot explain insect behavior with BVOCs under specific conditions. For example, in cases where Brevicoryne brassicae is a pest aphid on oilseed and Diaeretiella rapae is its natural enemy, higher O 3 levels decrease the populations of D. rapae and other parasitoids, which follows the previously discussed hypothesis of disrupted olfactory signals by O 3 . However, the recruitment of D. rapae increased when oilseed plants were simultaneously exposed to O 3 and diesel exhaust, whereas the population of other natural enemies decreased (Ryalls et al., 2022a). Therefore, BVOC was not an explanatory factor in the relationship between oilseed plants and D. rapae under combined air pollutants, indicating a species-specific attraction scheme of natural enemies and the importance of the interactive effects of multiple air pollutants. In addition, D. rapae corresponded to an O 3 -increased amount of glucosinolate, a precursor of isothiocyanates. Isothiocyanate is also a volatile compound that is often found in Brassicaceae plants, not categorized as terpenoid BVOCs, attracting natural enemies (Blande et al., 2007). Because the exceptional phenomenon of D. rapae was a case of moderate O 3 concentration (approximately 40 ppb; i.e., current ambient in many areas of the world), it is necessary to determine how the behavior of natural enemies changes at high air pollutant levels, including various combinations of O 3 with other air pollutants.

Strategies with innovative techniques in response to changing environments
To estimate and evaluate the O 3 risks on ecosystems, accurate data on insect dynamics and plant communities are required. However, unlike immobile plants, it is technically extremely difficult to track insects with high mobility and different active times. When herbivorous damage is observed on leaves, the culprit insect species can often not be detected. Traditional methods such as observation and traps require considerable time and effort, even with the use of contemporary electronic devices. To understand biodiversity patterns and populations in the field, "environmental DNA (eDNA)" has recently been investigated as a novel technique for studying the ecology of insects (van Klink et al., 2022) and other organisms (Thomsen & Willerslev, 2015). In herbivorous feeding, the species of the culprit insects can be detected as mitochondrial DNA fragments from feeding marks. Furthermore, airborne eDNA, cells, and tissue fragments of organisms can sense the existence of other entomofauna, including pollinators, such as flies (Diptera), butterflies (Lepidoptera), and bees (Hymenoptera) (Roger et al., 2022). Thus, if new insect species are introduced into an ecosystem and/or existing ones go extinct under changing environments, eDNA can help identify changes in biodiversity patterns.
There are many candidate insect-attracting compounds among the BVOCs emitted from certain plant species, making it difficult to identify the key compounds using only a single GC-MS analysis. The Y-tube preference test is a method used to check the behavior of insects toward odors, which does not imply the attractiveness of each compound from the whole range of BVOCs. A comparison of BVOCs among multiple host plant species enables us to trace the similarities that may contribute to attractiveness (Masui et al., 2022); however, this still lacks a strong explanation. For the efficient screening of attractive BVOCs, gas chromatography-electroantennography (GC-EAD) has been investigated in biological science (Shuttleworth & Johnson, 2020). If the emission rate of a compound was high, it was not necessarily attractive to insects. GC-EAD can detect compounds on insect antennae as electrical stimuli corresponding to the peaks in gas chromatography (Pawlowski et al., 2020). It should be noted that GC-EAD cannot distinguish a peaked compound as "attractant" or "repellent," although no peak in EAD analysis means that a compound does not have any function to the insect. Therefore, coupling GC-EAD with traditional bioassays, such as the Y-tube preference test, will increase the accuracy and efficiency of screening attractant compounds and/or composition from BVOCs.
If the increase in the O 3 concentration cannot be halted or decreased to an optimal level, research programs and agroforestry applications should consider the use of artificial volatiles with low O 3 -reactivity and the introduction of volatile emitters as companion plants. For example, linalool, β-caryophyllene, and myrcene may be biologically useful to control pests and pollinators in IPM strategy because these volatiles are detected as olfactory signals on the antenna in a wide range of insect species (e.g., Lepidoptera, Coleoptera, Hemiptera, Diptera, Hymenoptera) (Bruce et al., 2005). However, these volatiles have high reactivity to O 3 , and their lifetimes are shorter than 1 h, even under normal O 3 concentration of 710 11 molecule cm −3 (28.4 ppb) (Atkinson & Arey, 2003). Thus, olfactory signals containing these volatiles cannot be transmitted effectively to target insects and plants under elevated O 3 . Methyl salicylate (MeSA), which is less reactive with O 3 can be proposed as a useful candidate. Even if other abiotic factors (e.g., OH radicals) simultaneously react with MeSA, the lifetime is a few days (Ren et al., 2020). As MeSA induces physiological plant defenses and attracts natural enemies (Ayelo et al., 2021;Riedlmeier et al., 2017), its application is expected to be relatively stable and useful in O 3 -polluted areas.

Estimation of O 3 effects on ecosystems in long term
From the viewpoint of evolutionary biology, it is unclear how elevated O 3 levels will affect insects in the future (Kozlov, 2022). Previous research has been based on acutely elevated O 3 exposure (multi-fold increase over the ambient level) but not on increasing exposure over years, decades, or even centuries. With some exceptions (e.g., during spontaneous, O 3 episodes that last a few days), O 3 concentration rarely increases so highly "all of sudden" and remains constantly such high throughout the growing season(s) in the real world. Démares et al. (2022) reported that O 3 -derived olfactory disability in honeybees recovered 2 h after the termination of acute elevated O 3 exposure. Moreover, although it is experimentally difficult to research increasing O 3 exposure in the long term (e.g., over decades), it is worth simulating insect acclimation to changing environments on a scale of years and laboratory assays. For example, a moth has learned about O 3 -altered BVOCs as a new host (Cook et al., 2020). These findings indicate that insects can maintain BVOC-mediated communication even under elevated O 3 . To achieve progress in accurately evaluating biological communication, many aspects of BVOCs should be clarified against various plants comprising the ecosystems in urban lignose areas. These aspects of BVOCs include emission rate and composition, reactivity to O 3 , attractiveness to insects, and induced defense in plant-plant communications. Recognizing the difficulties in revealing the long-term evolutionary impacts of O 3 on biological communication, mathematical modeling will facilitate the addressing of such complex and multidimensional evolutionary phenomena, accounting for Mendel's laws of inheritance, mutations, natural selection, and neutral evolution, among other aspects of evolutionary theory.

Conclusion
Elevated O 3 disrupts numerous biological communications based on olfactory signals, including plant volatiles and insect pheromones. In this article, we review the original functions of these olfactory communications and the O 3 -derived risks that may lead to the collapse of the ecosystem balance and food crises in agro-ecosystems in urban areas and their vicinities. However, the relationships and properties of plant volatiles in the presence of elevated O 3 remain unknown. Furthermore, as shown with examples, biological communication is not always "one on one" (mono-dimensional) but also involves interactions with multiple organisms (multi-dimensional), e.g., tritrophic system. Therefore, including atmospheric aspects, such as the impact of BVOCs on O 3 formation, more research is needed to unravel the mechanisms underlying complex multilevel interactions in O 3 -polluted atmospheres. Hull-Sanders, H. M., Clare, R., Johnson, R. H., & Meyer, G. A. (2007). Evaluation of the evolution of increased