Stimulation of insect vectors of pathogens by sublethal environmental contaminants: A hidden threat to human and environmental health?

Sublethal stimulation and hormetic responses are increasingly identified and acknowledged in scientific research. However, the occurrence and characteristics of such responses in insect vectors of pathogens are little explored and poorly understood. Here, we collate significant evidence from the scientific literature showing that sublethal doses of environmental contaminants, such as pesticides, microplastics, and plasticizers, induce stimulation and hormetic responses in insect vectors of pathogens of agricultural and public health importance, including mosquitoes, other dipterans, psyllids, aphids, and planthoppers. Physiological, behavioral, and demographic traits can be enhanced by exposure to lower subtoxic contaminant doses while being inhibited by higher toxic doses. Energetic trade-offs can also occur, especially at sublethal doses higher than the no-observed-adverse-effect level (NOAEL). The relevant literature is limited and so are the number of doses commonly included in the studies, precluding firm conclusions and enhanced understanding. Nevertheless, these effects are significant and could undermine human and environmental health, and thus sustainability agendas, if ultimately the transmission of pathogens and disease spread and severity are increased. Further research is urgently needed to tackle these phenomena, especially under field conditions. The findings discussed here are relevant to chemical risk assessment and chemical safety evaluations, in which all possible effects from the lowest to higher doses should be considered.

Sublethal chemical stimulation of arthropod parasitoids and parasites of agricultural and environmental importance.

An increasing number of studies have reported stimulation of various organisms in the presence of environmental contaminants. This has created a need to critically evaluate sublethal stimulation and hormetic responses of arthropod parasitoids and parasites following exposure to pesticides and other contaminants. Examining this phenomenon with a focus on arthropods of agricultural and environmental importance serves as the framework for this literature review. This review shows that several pesticides, with diverse chemical structures and different modes of action, applied individually or in combination at sublethal doses, commonly stimulate an array of arthropod parasitoids and parasites. Exposure at sublethal doses can enhance responses related to physiology (e.g., respiration, total lipid content, and total protein content), behavior (e.g., locomotor activity, antennal drumming frequency, host location, and parasitization), and fitness (longevity, growth, fecundity, population net and gross reproduction). Concordantly, the parasitic potential (e.g., infestation efficacy, parasitization rate, and parasitoid/parasite emergence) can be increased, and as a result host activities inhibited. There is some evidence illustrating hormetic dose-responses, but the relevant literature commonly included a limited number and range of doses, precluding a robust differentiation between sub- and superNOAEL (no-observed-adverse-effect level) stimulation. These results reveal a potentially significant threat to ecological health, through stimulation of harmful parasitic organisms by environmental contaminants, and highlight the need to include sublethal stimulation and hormetic responses in relevant ecological pesticide risk assessments. Curiously, considering a more utilitarian view, hormesis may also assist in optimizing mass rearing of biological control agents for field use, a possibility that also remains neglected.

Effect of ozone exposure on the foraging behaviour of Bombus terrestris.

Tropospheric ozone (O3) mixing ratios have increased substantially since preindustrial times and high O3 peaks are increasingly common. Plant-pollinator interactions are central to natural ecosystem functioning and food production systems but could be negatively affected by unfavourable environmental conditions such as elevated O3. Ecosystem functioning is threatened by O3, which can degrade floral volatile organic compounds (VOCs) used by pollinators as olfactory cues during foraging. It can also exert oxidative stress on VOC-emitting plants and receiving organisms, potentially disturbing the sending and receiving of VOC signals. The aim of this study was to determine the effects of elevated ozone on the foraging behaviour of Bombus terrestris on three species of the Brassicaceae, with a particular focus on bumblebee choices and the mechanisms underpinning differences observed. Moreover, the study was designed to fill a gap between observations in small-scale laboratory experiments and large-scale modelling through empirical observations in polytunnels that represent a medium-large-scale artificial environment. Using 10 × 3 × 2 m polytunnels the effects of O3 on pollinator foraging parameters on Sinapis alba, Sinapis arvensis and Raphanus raphanistrum were assessed. Significant effects of elevated O3 (100 ± 10 ppb) on the time taken for the first bee to alight on a flower and the cumulative amount of time spent on flowers was observed. To further investigate the underlying mechanisms, a laboratory test was conducted to determine the effects of ozone on the VOC blend composition of S. alba flowers. Synthetic VOC blends representing O3-altered and unaltered profiles were reconstituted and utilized in polytunnel and olfactometry experiments. The results indicated that a reduction of olfaction-mediated orientation, probably via VOC-degradation or direct effects of O3 on bees, was responsible for the altered foraging parameters of B. terrestris, suggesting that the presence of elevated O3 could have negative effects on the foraging efficiency of important pollinator species.

Concurrent anthropogenic air pollutants enhance recruitment of a specialist parasitoid.

Air pollutants-such as nitrogen oxides, emitted in diesel exhaust, and ozone (O3)-disrupt interactions between plants, the insect herbivore pests that feed upon them and natural enemies of those herbivores (e.g. parasitoids). Using eight field-based rings that emit regulated quantities of diesel exhaust and O3, we investigated how both pollutants, individually and in combination, altered the attraction and parasitism rate of a specialist parasitoid (Diaeretiella rapae) on aphid-infested and un-infested Brassica napus plants. Individual effects of O3 decreased D. rapae abundance and emergence by 37% and 55%, respectively, compared with ambient (control) conditions. When O3 and diesel exhaust were emitted concomitantly, D. rapae abundance and emergence increased by 79% and 181%, respectively, relative to control conditions. This attraction response occurred regardless of whether plants were infested with aphids and was associated with an increase in the concentration of aliphatic glucosinolates, especially gluconapin (3-butenyl-glucosinolate), within B. napus leaves. Plant defensive responses and their ability to attract natural aphid enemies may be beneficially impacted by pollution exposure. These results demonstrate the importance of incorporating multiple air pollutants when considering the effects of air pollution on plant-insect interactions.

A potential ozone defense in intercellular air space: Clues from intercellular BVOC concentrations and stomatal conductance.

Ozone (O3) enters plants through the stomata, passes into the intercellular air space and is decomposed in cell walls. Two factors that affect the O3 level in the intercellular air space are the stomatal conductance and the concentration of biogenic volatile organic compounds (BVOCs). Stomatal conductance controls the O3 flux into the air space and the intercellular BVOCs react with the O3. Therefore, the intercellular air space serves as a place where O3 defense can occur, but it has received relatively little attention. This study aimed to explore potential plant-defense against O3 in the intercellular air space by measuring the stomatal conductance and intercellular BVOC concentrations of Scots pine (Pinus sylvestris) and Norway spruce (Picea abies). Seedlings of both species were exposed to two levels of O3, ambient (15 nmol mol-1) and 80 nmol mol-1 (dropping to an ambient level at night), in plant growth chambers for five days in both spring and summer. We found that O3 decreased stomatal conductance in both species and in both seasons, which can lower the O3 flux into the intercellular air space. Intercellular BVOC concentrations were decreased in spring while increased in summer for both species in response to O3. This suggests that the BVOC protection in the intercellular air space is only of consequence in summer. These results demonstrate the potential for BVOCs to provide intercellular O3 defense in both species, but with seasonal variation.

Volatile-mediated between-plant communication in Scots pine and the effects of elevated ozone.

Conifers are dominant tree species in boreal forests, but are susceptible to attack by bark beetles. Upon bark beetle attack, conifers release substantial quantities of volatile organic compounds known as herbivore-induced plant volatiles (HIPVs). Earlier studies of broadleaved plants have shown that HIPVs provide information to neighbouring plants, which may enhance their defences. However, the defence responses of HIPV-receiver plants have not been described for conifers. Here we advance knowledge of plant-plant communication in conifers by documenting a suite of receiver-plant responses to bark-feeding-induced volatiles. Scots pine seedlings exposed to HIPVs were more resistant to subsequent weevil feeding and received less damage. Receiver plants had both induced and primed volatile emissions and their resin ducts had an increased epithelial cell (EC) mean area and an increased number of cells located in the second EC layer. Importantly, HIPV exposure increased stomatal conductance and net photosynthesis rate of receiver plants. Receiver-plant responses were also examined under elevated ozone conditions and found to be significantly altered. However, the final defence outcome was not affected. These findings demonstrate that HIPVs modulate conifer metabolism through responses spanning photosynthesis and chemical defence. The responses are adjusted under ozone stress, but the defence benefits remain intact.

Volatile-Mediated Induced and Passively Acquired Resistance in Sagebrush (Artemisia tridentata).

Plants produce a diversity of secondary metabolites including volatile organic compounds. Some species show discrete variation in these volatile compounds such that individuals within a population can be grouped into distinct chemotypes. A few studies reported that volatile-mediated induced resistance is more effective between plants belonging to the same chemotype and that chemotypes are heritable. The authors concluded that the ability of plants to differentially respond to cues from related individuals that share the same chemotype is a form of kin recognition. These studies assumed plants were actively responding but did not test the mechanism of resistance. A similar result was possible through the passive adsorption and reemission of repellent or toxic VOCs by plants exposed to damage-induced plant volatiles (DIPVs). Here we conducted exposure experiments with five chemotypes of sagebrush in growth chambers; undamaged receiver plants were exposed to either filtered air or DIPVs from mechanically wounded branches. Receiver plants exposed to DIPVs experienced less herbivore damage, which was correlated with increased expression of genes involved in plant defense as well as increased emission of repellent VOCs. Plants belonging to two of the five chemotypes exhibited stronger resistance when exposed to DIPVs from plants of the same chemotypes compared to when DIPVs were from plants of a different chemotype. Moreover, some plants passively absorbed DIPVs and reemitted them, potentially conferring associational resistance. These findings support previous work demonstrating that sagebrush plants actively responded to alarm cues and that the strength of their response was dependent on the chemotypes of the plants involved. This study provides further support for kin recognition in plants but also identified volatile-mediated associational resistance as a passively acquired additional defense mechanism in sagebrush.

Amplified Drought and Seasonal Cycle Modulate Quercus pubescens Leaf Metabolome.

The intensification of summer drought expected with climate change can induce metabolism modifications in plants to face such constraints. In this experiment, we used both a targeted approach focused on flavonoids, as well as an untargeted approach, to study a broader fraction of the leaf metabolome of Quercus pubescens exposed to amplified drought. A forest site equipped with a rainfall exclusion device allowed reduction of natural rainfall by ~30% over the tree canopy. Leaves of natural drought (ND) and amplified drought (AD) plots were collected over three seasonal cycles (spring, summer, and autumn) in 2013 (the second year of rain exclusion), 2014, and 2015. As expected, Q. pubescens metabolome followed a seasonal course. In the summer of 2015, the leaf metabolome presented a shifted and early autumnal pattern because of harsher conditions during this year. Despite low metabolic modification at the global scale, our results demonstrated that 75% of Quercus metabolites were upregulated in springs when trees were exposed to AD, whereas 60 to 73% of metabolites (93% in summer 2015), such as kaempferols and quercetins, were downregulated in summers/autumns. Juglanin, a kaempferol pentoside, as well as rhododendrin derivatives, were upregulated throughout the year, suggesting an antioxidant ability of these metabolites. Those changes in terms of phenology and leaf chemistry could, in the end, affect the ecosystem functioning.

Volatile-mediated plant-plant interactions: volatile organic compounds as modulators of receiver plant defence, growth, and reproduction.

It is firmly established that plants respond to biotic and abiotic stimuli by emitting volatile organic compounds (VOCs). These VOCs provide information on the physiological status of the emitter plant and are available for detection by the whole community. In the context of plant-plant interactions, research has focused mostly on the defence-related responses of receiver plants. However, responses may span hormone signalling and both primary and secondary metabolism, and ultimately affect plant fitness. Here we present a synthesis of plant-plant interactions, focusing on the effects of VOC exposure on receiver plants. An overview of the important chemical cues, the uptake and conversion of VOCs, and the adsorption of VOCs to plant surfaces is presented. This is followed by a review of the substantial VOC-induced changes to receiver plants affecting both primary and secondary metabolism and influencing plant growth and reproduction. Further research should consider whole-plant responses for the effective evaluation of the mechanisms and fitness consequences of exposure of the receiver plant to VOCs.

Risk of herbivory negatively correlates with the diversity of volatile emissions involved in plant communication.

Plant-to-plant volatile-mediated communication and subsequent induced resistance to insect herbivores is common. Less clear is the adaptive significance of these interactions; what selective mechanisms favour plant communication and what conditions allow individuals to benefit by both emitting and responding to cues? We explored the predictions of two non-exclusive hypotheses to explain why plants might emit cues, the kin selection hypothesis (KSH) and the mutual benefit hypothesis (MBH). We examined 15 populations of sagebrush that experience a range of naturally occurring herbivory along a 300 km latitudinal transect. As predicted by the KSH, we found several uncommon chemotypes with some chemotypes occurring only within a single population. Consistent with the MBH, chemotypic diversity was negatively correlated with herbivore pressure; sites with higher levels of herbivory were associated with a few common cues broadly recognized by most individuals. These cues varied among different populations. Our results are similar to those reported for anti-predator signalling in vertebrates.

Bank vole alarm pheromone chemistry and effects in the field.

Chemical communication plays an important role in mammalian life history decisions. Animals send and receive information based on body odour secretions. Odour cues provide important social information on identity, kinship, sex, group membership or genetic quality. Recent findings show, that rodents alarm their conspecifics with danger-dependent body odours after encountering a predator. In this study, we aim to identify the chemistry of alarm pheromones (AP) in the bank vole, a common boreal rodent. Furthermore, the vole foraging efficiency under perceived fear was measured in a set of field experiments in large outdoor enclosures. During the analysis of bank vole odour by gas chromatography-mass spectrometry, we identified that 1-octanol, 2-octanone, and one unknown compound as the most likely candidates to function as alarm signals. These compounds were independent of the vole's sex. In a field experiment, voles were foraging less, i.e. they were more afraid in the AP odour foraging trays during the first day, as the odour was fresh, than in the second day. This verified the short lasting effect of volatile APs. Our results clarified the chemistry of alarming body odour compounds in mammals, and enhanced our understanding of the ecological role of AP and chemical communication in mammals.

Exposure to (Z)-11-hexadecenal [(Z)-11-16:Ald] increases Brassica nigra susceptibility to subsequent herbivory.

It is well established that plants emit, detect and respond to volatile organic compounds; however, knowledge on the ability of plants to detect and respond to volatiles emitted by non-plant organisms is limited. Recent studies indicated that plants detect insect-emitted volatiles that induce defence responses; however, the mechanisms underlying this detection and defence priming is unknown. Therefore, we explored if exposure to a main component of Plutella xylostella female sex pheromone namely (Z)-11-hexadecenal [(Z)-11-16:Ald] induced detectable early and late stage defence-related plant responses in Brassica nigra. Exposure to biologically relevant levels of vapourised (Z)-11-16:Ald released from a loaded septum induced a change in volatile emissions of receiver plants after herbivore attack and increased the leaf area consumed by P. xylostella larvae. Further experiments examining the effects of the (Z)-11-16:Ald on several stages of plant defence-related responses showed that exposure to 100 ppm of (Z)-11-16:Ald in liquid state induced depolarisation of the transmembrane potential (Vm), an increase in cytosolic calcium concentration [Ca2+]cyt, production of H2O2 and an increase in expression of reactive oxygen species (ROS)-mediated genes and ROS-scavenging enzyme activity. The results suggest that exposure to volatile (Z)-11-16:Ald increases the susceptibility of B. nigra to subsequent herbivory. This unexpected finding, suggest alternative ecological effects of detecting insect pheromone to those reported earlier. Experiments conducted in vitro showed that high doses of (Z)-11-16:Ald induced defence-related responses, but further experiments should assess how specific the response is to this particular aldehyde.

Diurnal variation in BVOC emission and CO2 gas exchange from above- and belowground parts of two coniferous species and their responses to elevated O3.

Increased tropospheric ozone (O3) concentrations in boreal forests affect the emission of biogenic volatile organic compounds (BVOCs), which play crucial roles in biosphere-atmosphere feedbacks. Although it has been well documented that BVOC emissions are altered in response to elevated O3, consequent effects on the carbon budget have been largely unexplored. Here, we studied the effects of elevated O3 (80 nmol mol-1) on diurnal variation of BVOC emissions and gas exchange of CO2 from above- and belowground parts of Norway spruce (Picea abies) and Scots pine (Pinus sylvestris) and further investigated effects on the carbon budget. In spring, elevated O3 decreased BVOC emissions and net photosynthesis rate (Pn) from above-ground parts of both species. As BVOC emissions have a causal relationship with dormancy recovery, O3-induced decreases in BVOC emissions indicated the inhibition of dormancy recovery. Contrary to the spring results, in summer BVOC emissions from aboveground parts were increased in response to elevated O3 in both species. Decreases in Pn indicated O3 stress. O3-induced monoterpene emissions from aboveground were the main volatile defense response. Elevated O3 had little effect on BVOC emissions from belowground parts of either species in spring or summer. In spring, elevated O3 decreased the proportion of carbon emitted as BVOCs relative to that assimilated by photosynthesis (the proportion of BVOC-C loss) at the soil-plant system levels in both species. In summer, elevated O3 resulted in a net CO2-C loss at the soil-plant system level of Scots pine. During this process, O3-induced BVOC-C loss can represent a significant fraction of carbon exchange between the atmosphere and Scots pine. In Norway spruce, the effects of O3 were less pronounced. The current results highlight the need for prediction of BVOC emissions and their contributions to the carbon budget in boreal forests under O3 stress.

The phytotoxic air-pollutant O3 enhances the emission of herbivore-induced volatile organic compounds (VOCs) and affects the susceptibility of black mustard plants to pest attack.

Stress-induced changes to plant biochemistry and physiology can influence plant nutritional quality and subsequent interactions with herbivorous pests. However, the effects of stress combinations are unpredictable and differ to the effects of individual stressors. Here we studied the effects of exposure to the phytotoxic air-pollutant ozone (O3), feeding by larvae of the large cabbage white butterfly (Pieris brassicae), and a combination of the two stresses, on the emission of volatile organic compounds (VOCs) by black mustard plants (Brassica nigra) under field and laboratory conditions. Field-grown B. nigra plants were also measured for carbon-nitrogen (C-N) content, net photosynthetic activity (Pn), stomatal conductance (gs) and biomass. The effects of O3 on interactions between plants and a herbivorous pest were addressed by monitoring the abundance of wild diamondback moth larvae (Plutella xylostella) and feeding-damage to B. nigra plants in an O3-free air concentration enrichment (O3-FACE) field site. Herbivore-feeding induced the emission of VOCs that were not emitted by undamaged plants, both under field and laboratory conditions. The combination of O3 and herbivore-feeding stresses resulted in enhanced emission rates of several VOCs from field-grown plants. Short-term O3 exposure (of 10 days) and P. brassicae-feeding did not affect C-N content, but chronic O3 exposure (of 34 and 47 days) and P. brassicae-feeding exacerbated suppression of Pn. Ozone exposure also caused visible injury and decreased the plant biomass. Field-grown B. nigra under elevated O3 were infested with fewer P. xylostella larvae and received significantly less feeding damage. Our results suggest that plants growing in a moderately polluted environment may be of reduced quality and less attractive to foraging herbivores.

Ozone affects plant, insect, and soil microbial communities: A threat to terrestrial ecosystems and biodiversity.

Elevated tropospheric ozone concentrations induce adverse effects in plants. We reviewed how ozone affects (i) the composition and diversity of plant communities by affecting key physiological traits; (ii) foliar chemistry and the emission of volatiles, thereby affecting plant-plant competition, plant-insect interactions, and the composition of insect communities; and (iii) plant-soil-microbe interactions and the composition of soil communities by disrupting plant litterfall and altering root exudation, soil enzymatic activities, decomposition, and nutrient cycling. The community composition of soil microbes is consequently changed, and alpha diversity is often reduced. The effects depend on the environment and vary across space and time. We suggest that Atlantic islands in the Northern Hemisphere, the Mediterranean Basin, equatorial Africa, Ethiopia, the Indian coastline, the Himalayan region, southern Asia, and Japan have high endemic richness at high ozone risk by 2100.

Does ozone exposure affect herbivore-induced plant volatile emissions differently in wild and cultivated plants?

Concentrations of tropospheric ozone have more than doubled in the Northern Hemisphere since pre-industrial times. Plant responses to single abiotic or biotic stresses, such as ozone exposure and herbivore-feeding, have received substantial attention, especially for cultivated plants. Modern cultivated plants have been subjected to selective breeding that has altered plant chemical defences. To understand how ozone might affect plant responses to herbivore-feeding in wild and cultivated plants, we studied the volatile emissions of brassicaceous plants after exposure to ambient (~ 15 ppb) or elevated ozone (80 ppb), with and without Plutella xylostella larvae-feeding. Results indicated that most of the wild and cultivated plants increased volatile emissions in response to herbivore-feeding. Ozone alone had a weaker and less consistent effect on volatile emissions, but appeared to have a greater effect on wild plants than cultivated plants. This study highlights that closely related species of the Brassicaceae have variable responses to ozone and herbivore-feeding stresses and indicates that the effect of ozone may be stronger in wild than cultivated plants. Further studies should investigate the mechanisms by which elevated ozone modulates plant volatile emissions in conjunction with biotic stressors.

Deposition of α-pinene oxidation products on plant surfaces affects plant VOC emission and herbivore feeding and oviposition.

White cabbage, Brassica oleracea, plants and artificial leaves covered with B. oleracea epicuticular wax were exposed to α-pinene and α-pinene oxidation products formed through the oxidation of α-pinene by ozone (O3) and hydroxyl (OH) radicals. O3 and OH-induced oxidation of α-pinene led to the formation of oxygenated volatile organic compounds (OVOCs) and secondary organic aerosol particles (SOA), referred to together as oxidation products (OP). Exposure of cabbage plants to O3 and OH-induced α-pinene OP led to the deposition and re-emission of gas-phase OP by exposed cabbage plants. In a series of 2-choice bioassays, the specialist cruciferous herbivore, Plutella xylostella adults deposited less eggs on artificial leaves exposed to α-pinene OP than on control plants exposed to clean filtered air. P. xylostella larvae did not show a specific feeding preference when offered leaves from different exposure treatments. However, the generalist Indian stick insect, Carausius morosus, fed more on control filtered air-exposed plants than on those exposed to α-pinene OP. Taken together, our results show that exposure to α-pinene oxidation products affects VOC emissions of B. oleracea and alters P. xylostella oviposition and C. morosus feeding responses.

Microorganisms in the phylloplane modulate the BVOC emissions of Brassica nigra leaves.

Numerous factors can affect the Biogenic Volatile Organic Compounds (BVOC) emitted by plants. One of these factors is the microbial communities living on leaf surfaces (phylloplane). Bacteria and fungi can use compounds produced and emitted by plants for their own metabolism. Thus, microorganism communities can modulate BVOC emissions and affect interactions between plants and other organisms. The aim of this study was to evaluate the role of microbial communities on BVOC emissions of Brassica nigra leaves. Therefore, we removed bacteria and/or fungi by using bactericide/fungicide treatments in a factorial design experiment with Brassica nigra grown in pots. BVOC emissions were sampled before and after the treatment application. Our results showed that four new compounds (cyclohexanone, cyclohexyl cyanide and two unknown compounds) were emitted after the removal of fungi, whereas no effect was detected in response to the bactericide treatment. This suggests that fungi inhibit or reduce the production of the above mentioned BVOCs from Brassica nigra leaves or use those compounds for their own metabolism. The origin and the roles of the novel compounds emitted requires further investigation.

The effect of elevated ozone on floral chemistry of Brassicaceae species.

Tropospheric ozone is a major atmospheric pollutant; it is phytotoxic and has a strong effect on phytochemicals, which are constitutively present in plant tissues, but also produced de novo in response to stress. It has been shown that ozone exposure can modify volatile phytochemical emissions from leaves, which could disturb interactions between plants and other organisms. However, there is a lack of knowledge on the effects of ozone on floral chemistry. The aim of this study was to determine the effects of two elevated ozone exposure scenarios (80 and 120 ppb during daylight hours for 5 consecutive days) on the floral volatile emissions and floral chemical (molecular size range C6-C20) content of four Brassicaceae species: Sinapis alba, Sinapis arvensis, Brassica napus and Brassica nigra. The results showed that the emissions of individual compounds and their relative contributions to volatile blends are both affected by ozone exposure. In addition, for all four species studied, three diterpenes (neophytadiene, cis-phytol and trans-phytol) were present in significantly lower amounts and a fourth diterpene (hexahydrofarnesyl acetone) in significantly greater amounts in ozone-exposed plants. Consistent effects of ozone exposure on volatile emissions and terpene content were observed for each of the four species studied with no significant effect of exposure level. It appeared that B. napus is the most ozone-sensitive species, whereas B. nigra is the most ozone-tolerant. Since earlier studies have indicated that ratios of phytochemicals can have substantial effects on the efficacy of chemical use by pollinators, these changes may have ecological and biological relevance that should be the focus of further elucidation.

Climate Change Effects on Secondary Compounds of Forest Trees in the Northern Hemisphere.

Plant secondary compounds (PSCs), also called secondary metabolites, have high chemical and structural diversity and appear as non-volatile or volatile compounds. These compounds may have evolved to have specific physiological and ecological functions in the adaptation of plants to their growth environment. PSCs are produced by several metabolic pathways and many PSCs are specific for a few plant genera or families. In forest ecosystems, full-grown trees constitute the majority of plant biomass and are thus capable of producing significant amounts of PSCs. We summarize older literature and review recent progress in understanding the effects of abiotic and biotic factors on PSC production of forest trees and PSC behavior in forest ecosystems. The roles of different PSCs under stress and their important role in protecting plants against abiotic and biotic factors are also discussed. There was strong evidence that major climate change factors, CO2 and warming, have contradictory effects on the main PSC groups. CO2 increases phenolic compounds in foliage, but limits terpenoids in foliage and emissions. Warming decreases phenolic compounds in foliage but increases terpenoids in foliage and emissions. Other abiotic stresses have more variable effects. PSCs may help trees to adapt to a changing climate and to pressure from current and invasive pests and pathogens. Indirect adaptation comes via the effects of PSCs on soil chemistry and nutrient cycling, the formation of cloud condensation nuclei from tree volatiles and by CO2 sequestration into PSCs in the wood of living and dead forest trees.